Persoonia 36, 2016: 1–36
www.ingentaconnect.com/content/nhn/pimj
RESEARCH ARTICLE
http://dx.doi.org/10.3767/003158516X688027
Redefining Microascus, Scopulariopsis and allied genera
M. Sandoval-Denis1, J. Gené1, D.A. Sutton 2, J.F. Cano-Lira1, G.S. de Hoog 3,
C.A. Decock 4, N.P. Wiederhold 2, J. Guarro1
Key words
Ascomycota
Microascaceae
Microascales
multigene phylogeny
taxonomy
Abstract The genera Microascus and Scopulariopsis comprise species commonly isolated from soil, decaying
plant material and indoor environments. A few species are also recognised as opportunistic pathogens of insects
and animals, including humans. In the past, the taxonomy of these fungi has been based on morphology only. With
the aim to clarify the taxonomy and phylogeny of these fungi, we studied a large set of clinical and environmental
isolates, including the available ex-type strains of numerous species, by means of morphological, physiological and
molecular analyses. Species delineation was assessed under the Genealogical Phylogenetic Species Recognition (GCPSR) criterion using DNA sequence data of four loci (ITS region, and fragments of rDNA LSU, translation
elongation factor 1-α and β-tubulin). The genera Microascus and Scopulariopsis were found to be separated in
two distinct lineages. The genus Pithoascus is reinstated and the new genus Pseudoscopulariopsis is erected,
typified by P. schumacheri. Seven new species of Microascus and one of Scopulariopsis are described, namely
M. alveolaris, M. brunneosporus, M. campaniformis, M. expansus, M. intricatus, M. restrictus, M. verrucosus and
Scopulariopsis cordiae. Microascus trigonosporus var. macrosporus is accepted as a species distinct from M. trigo
nosporus. Nine new combinations are introduced. Microascus cinereus, M. longirostris, P. schumacheri and S. flava
are neotypified. A table summarising the morphological features of the species treated and identification keys for
each genus are provided.
Article info Received: 17 July 2014; Accepted: 24 February 2015; Published: 15 April 2015.
INTRODUCTION
Scopulariopsis was erected by Bainier (1907) for a group of
fungi with asexual propagation, with S. brevicaulis as type species and two additional taxa, S. rubellus and S. rufulus. Sco
pulariopsis brevicaulis was originally described as Penicillium
brevicaule by Saccardo (1882) and included in the Penicillium
section Anomala (Biourge 1923). In the current sense, the distinctive features of Scopulariopsis are its annellidic conidiogenesis with mostly thick-walled, basally truncate conidia arranged
in long, dry chains and its colony colour varying from white to
brown or black, but never in bright green shades like Penicillium
(Morton & Smith 1963, Samson et al. 2010). Some asexual
genera with morphological features similar to those of Scopu
lariopsis, such as Acaulium, Masoniella, Phaeoscopulariopsis
and Torula were considered to be synonymous (Curzi 1930,
Morton & Smith 1963). Scopulariopsis currently comprises species with a worldwide distribution that are commonly isolated
from soil, air, plant debris and dung (Domsch et al. 2007). In
addition, some species have been described as colonisers or
pathogens of mammals, including humans and insects (de
Hoog et al. 2011, Iwen et al. 2012, Sandoval-Denis et al. 2013).
Several authors (Curzi 1930, 1931, Abbott et al. 1998, Abbott
& Sigler 2001, Issakainen et al. 2003) have demonstrated
by culturing, mating studies and molecular methods, that the
1
2
3
4
Unitat de Micologia, Facultat de Medicina i Ciències de la Salut, IISPV,
Universitat Rovira i Virgili, Reus, Spain;
corresponding author e-mail: josep.guarro@urv.cat.
Fungus Testing Laboratory, Department of Pathology, University of Texas
Health Science Center, San Antonio, Texas, USA.
CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht,
The Netherlands.
Mycothèque de l’Université Catholique de Louvain (MUCL, BCCMTM),
Earth and Life Institute - Microbiology (ELIM), Université Catholique de
Louvain, Louvain-la-Neuve, Belgium.
sexual morphs of Scopulariopsis belong to the ascomycete
genus Microascus. Abbott & Sigler (2001) confirmed the existence of both homothallic and heterothallic species. Microascus
was included in the family Microascaceae (1951), order Micro
ascales, together with other fungi with annellidic conidiogenesis
(Lumbsch & Huhndorf 2007). Microascus is characterised by
globose to ampulliform perithecial ascomata with cylindrical or
papillate necks, and a dark peridium of textura angularis. The
asci are ovate to globose, unitunicate, non-pedicellate, and eva
nescent, formed in basipetal rows and containing eight 1-celled
ascospores. The ascospores are typically asymmetrical, reniform, lunate or triangular, dextrinoid when young, often with an
inconspicuous germ-pore, and extruded in a long cirrhus or a
gelatinous ball at the top of the ascomata (Barron et al. 1961,
Morton & Smith 1963, Guarro et al. 2012).
Von Arx (1973a) erected Pithoascus with three species, i.e. P. in
termedius, P. nidicola (type species) and P. schumacheri. These
three species were previously included in Microascus and had
ascomata with rudimentary or inconspicuous ostioles, navicular
to fusiform ascospores without germ pores, while they lacked
asexual morphs. Von Arx (1978) added Pithoascus langeronii,
which produced an arthroconidial asexual morph. Nevertheless,
species of Pithoascus (i.e. P. intermedius, P. schumacherii)
were shown to produce a reduced, scopulariopsis-like asexual
morph (Roberts 1985, Valmaseda et al. 1986). Valmaseda
et al. (1986) erected the new monotypic genus Pithoascina
for the arthroconidia-forming species P. langeronii. Based on
these features, P. langeronii was later transferred to the genus
Eremomyces (Eremomycetaceae, Dothideomycetes) by Malloch & Sigler (1988) and more recently to Arthrographis, being
renamed as Arthrographis arxii (Giraldo et al. 2014).
Several authors consider Pithoascus s.str. as a synonym of Microascus (Malloch & Hubart 1987, Abbott et al. 2002, Guarro
et al. 2012) since some species show intermediate morpho-
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2
logical characteristics. In addition, other asexual genera of the
Microascaceae phylogenetically close to Scopulariopsis, i.e.
Wardomyces and Wardomycopsis, also produce a Microascus
sexual form (Malloch 1970, Udagawa & Furuya 1978); these
authors maintained wider generic concepts.
Barron et al. (1961) and later Morton & Smith (1963) published
comprehensive monographic reviews on Microascus and Sco
pulariopsis based on morphological criteria. Morphology seems
to be insufficient for establishing species limits in these fungi.
Although most species can be identified by detailed morphological study, phenotypic characters appear to overlap in several
cases (Sandoval-Denis et al. 2013). DNA sequencing and
multilocus phylogenetic analysis have considerably improved
our understanding of species concepts in many fungal groups
(Lackner & de Hoog 2011, Summerbell et al. 2011, Lackner et
al. 2014, Samson et al. 2014), but as yet no such study has
been undertaken to revise Microascus, Scopulariopsis and
allied genera.
Presently, 77 species are accepted in Scopulariopsis and 32
in Microascus. In addition, many described species are of
doubtful identity because their type materials are lost and their
protologues are uninterpretable. A further complicating factor
is that the new International Code of Nomenclature for Fungi,
Algae and Plants no longer allows dual nomenclature for those
fungal species that present both sexual and asexual morphs
(Hawksworth et al. 2011, Hibbett & Taylor 2013). However, to
resolve which name has priority, both at genus and species
levels, requires understanding of relationships among species,
as well as a stable and well-defined generic circumscription. In
the case if Scopulariopsis and Microascus would be congruent,
the former name has been recommended (Hawksworth 2012,
Sandoval-Denis et al. 2013).
In a recent study on Scopulariopsis and Microascus species
associated with human disease, we characterised several
isolates that could not be identified (Sandoval-Denis et al.
2013). The present work aims to clarify the taxonomic position
of these putative new species using the Genealogical Phylogenetic Species Recognition (GCPSR) criterion (Taylor et al.
2000). We provide a multigene phylogeny of Scopulariopsis,
Microascus and related fungi based on a large set of isolates,
which includes all available ex-type cultures and well-identified
reference strains from international culture collections.
MATERIALS AND METHODS
Isolates
In the present study we evaluate a total of 141 fungal strains,
representing 67 fungal species (Table 1). The strains were
mainly obtained from different international culture collections,
but also from human clinical specimens in the USA.
DNA extraction, amplification and phylogenetic analysis
All the strains were cultured on YES agar (20 g yeast extract,
150 g sucrose, 20 g agar, 1 L distilled water) for 5 d at 25 °C.
Fresh mycelium was removed by scrapping the agar surface
and total genomic DNA extraction was obtained using the PrepmanUltra sample preparation reagent (Applied Biosystems,
Foster City, CA, USA), according to manufacturer’s conditions.
Four nuclear DNA regions were amplified and sequenced.
These comprised a fragment (490 bp) including the internal
transcribed spacer ITS-1 and ITS-2 and the 5.8S rDNA gene
(ITS), a fragment (450 bp) including the D1/D2 regions of
the LSU rDNA gene, a fragment (820 bp) of the translation
elongation factor 1-alpha (EF-1α) and a fragment (470 bp) of
the beta-tubulin gene (TUB). The different loci were amplified
Persoonia – Volume 36, 2016
using the primer pairs ITS5 /ITS4 for the ITS region (White
et al. 1990), NL1/NL4b for the LSU region (O’Donnell 1993),
983F/2218R for EF-1α (Rehner & Buckley 2005) and BT2a/
BT2b for TUB (Glass & Donaldson 1995). PCR amplification
reaction had a total volume of 40 µL and consisted in 20 mM
Tris-HCl (pH 8.4), 50 mM KCl (10X PCR reaction buffer; Invi
trogen, Life Technologies Ltd, Paisley, UK) 1.5 mM MgCl2
(Invitrogen, Life Technologies Ltd, Paisley, UK), 125 µM of
each deoxynucleoside triphosphate (GeneAmp® dNTP mix
with dTTP, Applied Biosystems, Life Technologies Corporation,
Carlsbad, CA, USA), 5 % dimethyl sulfoxyde (DMSO; Panreac
Química S.L.U, Barcelona, Spain), 1.2 µM of each primer and
1.25 U of Taq DNA Polymerase (Invitrogen, Life Technologies
Ltd, Paisley, UK). The amplification programme consisted of an
initial denaturation at 94 °C for 5 min, followed by 35 cycles of
denaturation at 95 °C for 30 s, annealing at a suitable temperature for 1 min, extension for 1 min and 20 s at 72 °C, and a final
extension for 1 min at 72 °C. Annealing temperatures for each
gene were 55 °C for ITS, 51 °C for LSU and 57 °C for EF-1α
and TUB. The amplified products were purified with Diffinity
Rapid Tip® purification system (Sigma-Aldrich, St. Louis, MO,
USA) and stored at -20 °C until sequencing.
Sequencing was conducted in both directions with the same
primer pair used for amplification at Macrogen Europe (Macrogen Inc. Amsterdam, The Netherlands). Consensus sequences
were obtained using SeqMan v. 7.0.0 (DNASTAR Lasergene,
Madison, WI, USA). The newly generated sequences obtained
in this study and their GenBank accession numbers are summarised in Table 1. Additionally, 167 relevant sequences, obtained
from public databases (GenBank, NITE) and selected on the
basis of BLAST homology search results, were incorporated
in the phylogenetic analyses (Table 1).
Sequences were aligned individually for each locus using Clu
stalW (Thompson et al. 1994), under MEGA v. 5.05 (Tamura et
al. 2011), refined with MUSCLE (Edgar 2004) under the same
platform and manually adjusted if needed. Phylogenetic recon
structions by maximum likelihood (ML) and bayesian inference
were carried out using MEGA v. 5.05 and MrBayes v. 3.1.2
(Huelsenbeck & Ronquist 2001), respectively. The best nucleotide substitution model for each locus and the combined
dataset (GTR+G+I) were estimated using MrModeltest v. 2.3
(Nylander 2004). ML phylogeny was first made separately for
each locus (data not shown) and assessed for their concor
dance by comparing the phylogenetic placement and monophyly of the terminal clades and internal nodes with significant
bootstrap (bs) support. Since there was no discordance, the
loci were combined into two different datasets. A first analysis
was carried out using sequences of both ITS and LSU loci in
order to establish the boundaries of the genera with all the
available ex-type strains of Microascus / Scopulariopsis species complemented with several sequences of related genera
of the Microascaceae and Graphiaceae. To establish the species distribution among the genera, a second combined dataset
was created including LSU, ITS, EF-1α and TUB sequences
made up of a subset of those previously analysed strains and
numerous environmental and clinical isolates morphologically
identified as Microascus or Scopulariopsis species.
For ML analysis, the trees were inferred using Nearest-Neigh
bour-Interchange as a heuristic method and gaps were treated
as partial deletion with a 95 % site coverage cut-off. The robust
ness of branches was assessed by a bootstrap analysis of
1 000 replicates (Felsenstein 1985). Bootstrap values over 70 %
were considered significant.
The Bayesian analyses consisted of two parallel runs of four
incrementally heated Markov Chains starting from a random
tree topology. The analyses lasted for five million generations
Microascus giganteus†
Microascus gracilis comb. nov.
Microascus expansus sp. nov.
Microascus croci comb. nov.
Microascus cirrosus
Microascus albonigrescens†
Microascus brunneosporus
sp. nov.
Microascus campaniformis
sp. nov.
Microascus caviariformis†
Microascus chartarus comb. nov.
Microascus cinereus
Aspergillus baarnensis
Doratomyces purpureofuscus
Doratomyces stemonitis
Gamsia aggregata
Gamsia simplex
Graphium penicillioides
Hypocrea atroviridis
Kernia nitida
Kernia pachypleura
Lophotrichus macrosporus
Lophotrichus plumbescens
Microascus alveolaris sp. nov.
Current name
Strain number 1
Source
Microascus giganteus
Paecilomyces fuscatus
Scopulariopsis gracilis
Scopulariopsis gracilis
Scopulariopsis gracilis
Microascus caviariformis
Masonia chartarum
Microascus cinereus
Microascus cinereus
Microascus cinereus
Microascus cinereus
Microascus cinereus
Microascus griseus
Microascus cirrosus
Microascus cirrosus
Microascus desmosporus
Microascus cirrosus
Microascus cirrosus
Scopulariopsis chartarum
Microascus cirrosus
Scopulariopsis croci
Masoniella tertia
Microascus sp.
Microascus sp.
Microascus sp.
Microascus sp.
Microascus sp.
Microascus sp.
Microascus albonigrescens
Microascus sp.
Scopulariopsis halophilica
Doratomyces purpureofuscus
Doratomyces stemonitis
Wardomyces aggregatus
Wardomyces simplex
Graphium penicillioides
Hypocrea atroviridis
Magnusia nitida
Kernia pachypleura
Lophotrichus macrosporus
Lophotrichus plumbescens
Microascus sp.
Microascus sp.
Microascus sp.
Microascus sp.
Microascus sp.
Microascus sp.
CBS 380.74 (ex-type)
Undaria pinnatifida
CBS 139.42; NBRC 7677
Manure
CBS 127.22; MUCL 4031
Seed
CBS 251.69 (ex-isotype)
Dung of carnivore
CBS 546.69 (ex-isotype)
Milled Oryza sativa
CBS 102632 (ex-epitype)
Wood, Populus nigra
CBS 110086; NBRC 101776 (ex-type)
Decorticated wood
CBS 282.52; NBRC 8200
Chrysolina sanguinolenta
NBRC 30413; UAMH 8858
Soil of paddy field
FMR 5571; NBRC 32894
Sheep dung
NBRC 30864; UAMH 8710 (ex-type)
Soil
UTHSC 04-1534; FMR 12354
Human BAL
UTHSC 05-3416; FMR 12350
Human BAL
UTHSC 05-1041; FMR 12351
Human sputum
UTHSC 06-3152; FMR 12346
Human BAL
UTHSC 07-1823; FMR 12342
Human Sputum
CBS 139501; UTHSC 07-3491;
Human BAL
FMR 12252 (ex-type)
UTHSC 08-886; FMR 12340
Human BAL
UTHSC 10-214; FMR 12336
Human BAL
UTHSC R-4634; FMR 12333
Human lung Tissue
IHEM 18560
Litter treated with urea
CBS 138276; UTHSC 06-4312;
Human BAL
FMR 12343 (ex-type)
CBS 138126; UTHSC 10-565;
Human BAL
FMR 12334 (ex-type)
CBS 536.87: UAMH 5592 (ex-type)
Decaying meat
CBS 294.52; MUCL 9001 (ex-type)
Mouldy wall-paper in a house
UTHSC 06-3278; FMR 12345
BAL
UTHSC 08-3181: FMR 12339
Human sternum tissue
UTHSC 09-573; FMR 12239
Human BAL
UTHSC 10-2805; FMR 12217 (ex-neotype) Human BAL
UTHSC 11-383; FMR 12331
Human BAL
CBS 365.65; ATCC 16204 (ex-type)
Soil
CBS 217.31 (ex-type)
Leaf of Prunus sp.
CBS 277.34; MUCL 9050
Roots of Vitis vinifera
CBS 301.61; MUCL 9054
Unknown
UTHSC 07-1887: FMR 12256
Induced human sputum
UTHSC 11-14; FMR 12332
Human BAL
FMR 3997
Aquatic sediment, Ebro river
FMR 4004
Aquatic sediment, Besós river
CBS 158.44; MUCL 9002 (ex-type)
From Crocus sp.
CBS 296.61; MUCL 9005 (ex-type)
Air
UTHSC 06-2519; FMR 12267
Human pleural fluid
CBS 138127; UTHSC 06-4472;
Human sputum
FMR 12266 (ex-type)
CBS 746.69 (ex-type)
Insect frass in dead log
CBS 369.70 (ex-isotype)
Food
UTHSC 09-1351; FMR 12234
Human joint fluid
UTHSC 09-1829; FMR 12231
Human BAL
UTHSC 10-390; FMR 12335
Human BAL
LM652499
00767701*
DQ836907
LM652500
LM652501
AF175961
11776205*
00820001*
03041301*
03289401*
03086401*
HG380482
HG380483
HG380488
HG380487
HG380489
HG380484
HG380485
HG380486
HG380490
LM652502
HG380497
HG380495
LM652503
HG380463
HG380347
HG380348
HG380349
HG380350
HG380351
HG380346
HG380429
LM652504
LM652505
HG380431
HG380432
LM652506
LM652507
LM652508
LM652509
HG380491
HG380492
LM652510
HG380467
HG380476
HG380477
LM652511
LM652376
00767701*
LM652377
LM652378
LM652379
AB038432
11776204*
00820001*
03041301*
03289401*
03086401*
LM652380
LM652381
LM652382
LM652383
LM652384
LM652385
LM652386
LM652387
LM652388
LM652389
LM652390
LM652391
LM652392
LM652393
LM652394
LM652395
LM652396
LM652397
LM652398
LM652399
LM652400
LM652401
LM652402
LM652403
LM652404
LM652405
LM652406
LM652407
LM652408
LM652409
LM652410
LM652411
LM652412
LM652413
LM652414
LM652415
USA
Belgium
England: London.
USA
USA
USA
USA
USA
India: Maharashtra
Italy
Italy
UK
USA
USA
Spain: Tarragona
Spain: Barcelona
The Netherlands: Lisse
Brazil: Pernambuco
USA
USA
Canada: Ontario
Japan
USA
USA
USA
USA
USA
USA
Japan: Nemuro-shi
USA
Japan
The Netherlands: Limburg
The Netherlands: Wageningen
USA
Japan
Czech Republic
France
France
Japan
Iraq
Thailand; Bangkok
USA
USA
USA
USA
USA
USA
LSU
–
HG380390
HG380399
HG380400
LM652562
–
HG380386
HG380424
HG380425
HG380426
HG380427
HG380428
HG380423
HG380352
LM652556
LM652557
HG380354
HG380355
LM652558
LM652559
LM652560
LM652561
HG380414
HG380415
HG380418
HG380408
HG380409
HG380413
–
HG380420
–
–
–
–
–
–
–
–
–
–
–
HG380405
HG380406
HG380411
HG380410
HG380412
HG380407
EF-1α
Sequence accession number 2
ITS
Origin
Original name
Table 1 Strains and sequence accession numbers included in this study.
–
LM652625
LM652626
LM652627
LM652628
–
LM652607
LM652608
LM652609
LM652610
LM652611
LM652612
LM652613
LM652614
LM652615
LM652616
LM652617
LM652618
LM652619
LM652620
LM652621
LM652622
LM652623
LM652624
LM652606
LM652602
LM652603
LM652604
–
LM652605
–
–
–
–
–
–
–
–
–
–
–
LM652596
LM652597
LM652598
LM652599
LM652600
LM652601
TUB
M. Sandoval-Denis et al.: Phylogeny of Microascus and Scopulariopsis
3
Phitoascus intermedius
Phitoascus nidicola
Pithoascus platysporus†
Phitoascus stoveri
Pseudallescheria ellipsoidea
Pseudoscopulariopsis hibernica
comb. nov.
Petriella sordida
Petriellopsis africana
Phitoascus ater comb. nov.
Phitoascus exsertus
Parascedosporium tectonae
Petriella setifera
Microascus verrucosus sp. nov.
Microascus senegalensis
Microascus singularis†
Microascus trigonosporus
Microascus pyramidus
Microascus restrictus sp. nov.
Microascus macrosporus
comb & stat. nov.
Microascus murinus comb. nov.
Microascus paisii comb. nov.
Microascus longirostris
Microascus hyalinus comb. nov.
Microascus intricatus sp. nov.
Current name
Table 1 (cont.).
Strain number 1
Source
Origin
Graphium tectonae
Petriella setifera
Petriella setifera
Petriella sordida
Petriellidium africanum
Scopulariopsis atra
Microascus exsertus
Microascus exsertus
Microascus intermedius
Microascus nidicola
Pithoascus platysporus
Microascus stoveri
Petriellidium ellipsoideum
Scopulariopsis hibernica
Microascus senegalensis
Microascus singularis
Microascus trigonosporus var.
trigonosporus
Microascus trigonosporus
Scopulariopsis coprophila
Microascus sp.
Microascus sp.
Microascus longirostris
Microascus longirostris
Microascus trigonosporus var.
macrosporus
Scopulariopsis murina
Scopulariopsis brumptii
Scopulariopsis brumptii
Scopulariopsis brumptii
Scopulariopsis brumptii
Scopulariopsis brumptii
Scopulariopsis brumptii
Scopulariopsis brumptii
Scopulariopsis brumptii
Masonia grisea
Torula paisii
Scopulariopsis brumptii
Scopulariopsis chartarum
Scopulariopsis melanospora
Scopulariopsis sphaerospora
Microascus pyramidus
Microascus sp.
Microascus cinereus
Microascus cinereus
Kernia hyalina
Microascus sp.
CBS 199.61; MUCL 9061
CBS 262.35; MUCL 9841
CBS 138278; UTHSC 10-2601;
FMR 12219 (ex-type)
CBS 127.84 (ex-type)
CBS 437.75
FMR 7736; NBRC 100025
CBS 124169
CBS 311.72 (ex-type)
CBS 400.34; IHEM 18608 (ex-type)
CBS 583.75
CBS 819.70 (ex-type)
CBS 217.32 (ex-type)
CBS 197.61 (ex-epitype)
CBS 419.73 (ex-type)
CBS 176.71 (ex-type)
CBS 418.73 (ex-type)
UAMH 2643; ATCC 16690
CBS 830.70; IHEM 18567 (ex-type)
UTHSC 07-639; FMR 12263
UTHSC 08-1734; FMR 12248
UTHSC 09-2391; FMR 12229
UTHSC 09-457; FMR 12241
UTHSC 09-482; FMR 12240
UTHSC 10-2920; FMR 12215
UTHSC 11-708; FMR 12210
CBS 896.68; MUCL 8989
CBS 295.52; MUCL 9003 (ex-type)
CBS 213.27; MUCL 7915 (ex-type)
MUCL 8990
CBS 897.68; MUCL 8993
CBS 272.60; MUCL 9040 (ex-isotype)
CBS 402.34; MUCL 9045 (ex-type)
CBS 212.65 (ex-isotype)
CBS 138277; UTHSC 09-2704;
FMR 12227 (ex-type)
CBS 277.74; IHEM 18561 (ex-type)
CBS 414.64
CBS 218.31 (ex-type)
CBS 195.61; MUCL 9048
CBS 300.61; MUCL 9049
CBS 766.70 (ex-isotype)
CBS 138128; UTHSC 07-156;
FMR 12264 (ex-type)
FMR 12362
CBS 196.61; MUCL 9058 (ex-neotype)
CBS 415.64
CBS 662.71
Burma, Japan
UK
USA
Jamaica
Hong Kong
Spain; Canary Islands
The Netherlands
Namibia
Unknown
Denmark: Sjaelland
Denmark: Tastrup
USA: North Carolina
USA: Utah
The Netherlands
USA: Ohio
Tajikistan
Ireland
Seed
Wood panel in coastal water
Soil
Corner of a bathroom
Brown sandy soil
Unknown
From Osmia rufa
From Megachile willoughbiella
Root of Fragaria vesca
From Dipodomys merriami
Agricultural soil
Root of Beta vulgaris
Soil
From soil
Senegal
Japan: Tokyo
USA
Mangrove soil
Laboratory contaminant
Unknown
Milled rice
Mushroom bed
Human BAL
Germany: Giessen
USA
USA
USA
USA
USA
USA
USA
Germany: Schleswig
England
Italy
Germany: Schleswig-Holstein
Germany
USA
Austria
USA: California
USA
Argentina: Iguazú
USA: Maine
Japan
USA
England
USA: Iowa
USA
USA
Composed municipal waste
Human BAL
Human BAL
Human sputum
Human sputum
Human BAL
Human BAL
Human sputum
Soil on a Triticum sativum field
Culture contaminant
Man
Soil
Soil on a wheat field
Milled Oriza sativa
Unknown
Desert soil
Human left hallux
Soil
Wasp’s nest
Soil
Soil
Soil
Seed of Zea mays
Dung of cow
Human BAL
Original name
LM652514
LM652515
LM652516
LM652517
HG380481
HG380451
HG380452
HG380453
HG380454
HG380455
HG380456
HG380457
HG380449
HG380450
LM652518
LM652519
LM652520
LM652521
LM652522
HG380435
HG380494
LM652523
LM652524
HG380436
HG380438
LM652525
HG380493
LM652420
LM652421
LM652422
LM652423
LM652424
LM652425
LM652426
LM652427
LM652428
LM652429
LM652430
LM652431
LM652432
LM652433
LM652434
LM652435
LM652436
LM652437
LM652438
LM652439
LM652440
LM652441
LM652442
LM652443
LM652444
LM652445
LM652446
EF151332
DQ470969
10002501*
AY281099
EF151331
LM652526
LM652527
LM652528
LM652529
LM652530
LM652531
LM652532
EF151323
LM652533
HG380468
LM652512
LM652513
HG380496
LM652416
LM652417
LM652418
LM652419
AY228113
–
10002501*
GQ426957
AJ888425
LM652447
LM652448
LM652449
LM652450
LM652451
LM652452
LM652453
EF151323
LM652454
LSU
EF151409
DQ836911
–
–
–
LM652576
LM652577
LM652578
LM652579
LM652580
–
LM652581
–
LM652582
HG380361
LM652575
HG380416
LM652574
–
HG380359
HG380404
HG380374
HG380375
HG380376
HG380377
HG380378
HG380379
HG380380
HG380372
HG380373
LM652569
LM652570
LM652571
LM652572
LM652573
HG380358
HG380417
LM652565
LM652566
LM652567
LM652568
HG380391
LM652563
LM652564
HG380419
EF-1α
Sequence accession number 2
ITS
–
–
–
–
–
LM652659
LM652660
LM652661
LM652662
LM652663
–
LM652664
–
LM652665
LM652656
LM652657
LM652658
LM652654
–
LM652655
LM652637
LM652638
LM652639
LM652640
LM652641
LM652642
LM652643
LM652644
LM652645
LM652646
LM652647
LM652648
LM652649
LM652650
LM652651
LM652652
LM652653
LM652633
LM652634
LM652635
LM652636
LM652629
LM652630
LM652631
LM652632
TUB
4
Persoonia – Volume 36, 2016
CBS 435.86 (ex-neotype)
Scedosporium aurantiacum
Pseudallescheria boydii
Scopulariopsis danica
Scopulariopsis acremonium
Scopulariopsis acremonium
Microascus niger
Microascus niger
Scopulariopsis asperula
Scopulariopsis fusca
Scopulariopsis fusca
Torula bestae
Microascus brevicaulis
Scopulariopsis alboflavescens
Scopulariopsis brevicaulis
Scopulariopsis brevicaulis
Scopulariopsis brevicaulis
Scopulariopsis brevicaulis
Scopulariopsis brevicaulis
Scopulariopsis brevicaulis
Scopulariopsis brevicaulis
Scopulariopsis brevicaulis
Scopulariopsis brevicaulis
Scopulariopsis brevicaulis
Scopulariopsis insectivora
Scopulariopsis koningii
Scopulariopsis stercoraria
Scopulariopsis canadensis
Scopulariopsis alboflavescens
Scopulariopsis brevicaulis var. alba
Scopulariopsis candelabrum
Scopulariopsis candida
Scopulariopsis candida
Scopulariopsis candida
Microascus manginii
Nephrospora manginii
Scopulariopsis carbonaria
Scopulariopsis fimicola
Scopulariopsis sp.
CBS 116910
CBS 330.93
CBS 290.38; MUCL 9028 (ex-type)
MUCL 8274
MUCL 8409
MUCL 40729; UAMH 7879
MUCL 40746; UAMH 9029
CBS 853.68
UTHSC 10-3405; FMR 12212
CBS 401.34; MUCL 9032 (ex-type)
CBS 289.38; MUCL 9012 (ex-type)
MUCL 40726 (ex-type)
CBS 399.34 (ex-type)
UTHSC 06-277; FMR 12273
UTHSC 06-619; FMR 12271
UTHSC 06-1072; FMR 12247
UTHSC 07-1812; FMR 12257
UTHSC 07-1888; FMR 12255
UTHSC 09-1092; FMR 12236
UTHSC 09-1373; FMR 12233
UTHSC 11-1240; FMR 12206
UTHSC 11-1563; FMR 12204
UTHSC 11-427; FMR 12211
CBS 335.35; MUCL 9035
CBS 208.61
MUCL 14213
CBS 204.61 (ex-type)
MUCL 9007
CBS 119.43; MUCL 9016
CBS 205.27; MUCL 9026
MUCL 40743 (ex-epitype)
UTHSC 09-3241; FMR 12226
UTHSC 09-2576; FMR 12228
MUCL 41467
CBS 170.27 (ex-type)
MUCL 9027 (ex-type)
CBS 206.61
CBS 138129; UTHSC 09-866;
FMR 12338 (ex-type)
Scopulariopsis sp.
UTHSC 05-3453; FMR 12349
Scopulariopsis flava
CBS 207.61; MUCL 9031 (ex-neotype)
Scopulariopsis parvula
MUCL 9041 (ex-type)
Microascus soppii
UAMH 9169 (ex-type)
Trichoderma asperellum
CBS 433.97; NBRC 101777 (ex-type)
Trichurus spiralis
NBRC 100833
Trichurus terrophilus
NBRC 7660; CBS 448.51; UAMH 8848
Wardomyces hughesii
CBS 216.61 (ex-isotype)
Scopulariopsis humicola
CBS 487.66 (ex-type)
Wardomycopsis inopinata
FMR 10305
Microascus schumacheri
11058901*
00766001*
LM652496
LM652497
LM652498
Japan: Kumamoto-shi
South Africa
Canada: Québec
Canada: Ontario
Myanmar
11058901*
00766001*
LM652553
LM652554
LM652555
HG380498
HG380464
LM652551
LM652552
11776301*
LM652492
LM652493
LM652494
LM652495
11776302*
USA
UK
Canada
Canada: Alberta
USA: Maryland
Human JP Drain
Cheese
Soil
wood of Populus tremuloides
Sclerotia of Sclerotinia minor
buried in soil
Mushroom
Timber of Eucalyptus saligna
Wood, Acer sp.
Soil
Soil
LM652534
EF151326
AY882372
HG380439
LM652535
LM652536
LM652537
HG380434
JQ434669
HG380461
HG380465
LM652538
HG380440
LM652539
HG380441
HG380442
LM652540
HG380443
HG380444
HG380445
LM652541
HG380446
HG380447
HG380448
LM652542
LM652543
LM652544
LM652545
LM652546
LM652547
LM652548
HG380458
HG380460
HG380459
HG380433
LM652549
HG380462
LM652550
HG380499
LM652455
HQ231818
AY863196
LM652456
LM652457
LM652458
LM652459
LM652460
LM652461
LM652462
LM652463
LM652464
LM652465
LM652466
LM652467
LM652468
LM652469
LM652470
LM652471
LM652472
LM652473
LM652474
LM652475
LM652476
LM652477
LM652478
LM652479
LM652480
LM652481
LM652482
LM652483
LM652484
LM652485
LM652486
LM652487
LM652488
LM652489
LM652490
LM652491
Spain
The Netherlands
Denmark
Germany: Schleswig-Holstein
Germany: Schleswig-Holstein
Canada: Alberta
Canada: Alberta
Germany
USA
Austria
Italy
Canada: Alberta
Austria
USA
USA
USA
USA
USA
USA
USA
USA
USA
USA
The Netherlands
Unknown
Belgium: Heverlee
Canada
Unknown
The Netherlands
France
Canada
USA
USA
France
France
Panama
UK
USA
Spain: Puerto de la Quesera
Ulcer of ankle
Bronchial secretion
Skin of a horse
Wheat field soil
Soil
Indoor air
Dung of Mephitis mephitis
Compost soil
Toenail
Carcass of rabbit
From man
Indoor air
Diseased skin
Human hair
Human toenail
Human BAL
Human toenail
Human spine
Human toe
Human sputum
Human lung mass
Human BAL
Human sputum
Pupa of Pteronus pini
Elephant
Soil
Seed of Beta vulgaris
Unknown
Soil
Unknown
Indoor air
Scalp
Sputum
Cheese ‘Tome de Savoie’
Unknown
Soil
Mushroom bed
Human finger
From soil
–
–
–
–
–
HG380421
HG380387
–
LM652595
–
–
–
HG380362
–
–
LM652584
HG380357
JQ434621
HG380384
HG380388
LM652585
HG380363
JQ434600
HG380364
HG380365
LM652586
HG380366
HG380367
HG380368
LM652587
HG380369
HG380370
HG380371
LM652588
LM652589
LM652590
–
LM652591
LM652592
LM652593
HG380381
HG380383
HG380382
HG380356
LM652594
HG380385
–
HG380422
LM652583
–
–
–
–
–
LM652696
LM652697
–
LM652698
–
–
–
–
–
–
LM652667
LM652668
JQ434558
LM652669
LM652670
LM652671
LM652672
JQ434537
LM652674
LM652675
LM652676
LM652677
LM652678
LM652679
LM652680
LM652681
LM652682
LM652683
LM652684
LM652685
LM652686
–
LM652687
LM652688
LM652689
LM652690
LM652691
LM652692
LM652693
LM652694
LM652695
–
LM652673
LM652666
1
ATCC: American type culture collection, Manassas, VA, USA; CBS: CBS Fungal Biodiversity Centre, Utrecht, The Netherlands; FMR: Facultat de Medicina i Ciències de la Salut, Reus, Spain; IHEM: Biomedical Fungi and Yeasts Collection, Scientific Institute of Public Health, Belgium; MUCL: Université Catholique de Louvain, Louvain-la-Neuve, Belgium; NBRC: National Biological Resource Centre, Japan; UAMH: University of Alberta Microfungus Collection and Herbarium, Canada; UTHSC: Fungus Testing Laboratory, Department of Pathology, University
of Texas Health Science Center, San Antonio, USA.
2
ITS: Internal transcribed spacer regions of the rDNA and 5.8S region; LSU: partial large subunit of the rDNA; EF-1α: Partial translation elongation factor gene; TUB: partial beta-tubulin gene.
† Excluded or doubtful species name. * Sequences obtained from the NBRC database. Sequences newly generated in this study are indicated in bold.
Trichurus spiralis
Trichurus terrophilus
Wardomyces inflatus
Wardomycopsis humicola
Wardomycopsis inopinata
Scopulariopsis flava
Scopulariopsis parva
Scopulariopsis soppii
Trichoderma asperellum
Scopulariopsis carbonaria†
Scopulariopsis coprophila†
Scopulariopsis cordiae sp. nov.
Scopulariopsis canadensis†
Scopulariopsis candida
Scopulariopsis brevicaulis
Scopulariopsis asperula
Pseudoscopulariopsis schumacheri comb. nov.
Scedosporium aurantiacum
Scedosporium boydii
Scopulariopsis acremonium†
M. Sandoval-Denis et al.: Phylogeny of Microascus and Scopulariopsis
5
6
Persoonia – Volume 36, 2016
74/--
CBS 218.31T Microascus trigonosporus (type of M. trigonosporus var. trigonosporus)
MUCL 9001T Scopulariopsis chartarum (type of Masonia chartarum)
CBS 365.65T Microascus cinereus (type of Microascus griseus)
CBS 212.65T Microascus pyramidus
CBS 217.31T Microascus cirrosus
CBS 369.70T Scopulariopsis gracilis (type of Paecilomyces fuscatus)
CBS 662.71 Microascus trigonosporus var. macrosporus
IHEM 18561T Microascus senegalensis
79/--
MUCL 9005T Scopulariopsis brumptii (type of Masoniella tertia)
MUCL 9002T Scopulariopsis croci (type of Masoniella croci)
93/1.00
CBS
766.70T Kernia
Microascus
hyalina
MUCL 9040T Scopulariopsis brumptii (type of Scopulariopsis melanospora)
92/1.00
MUCL 9003T Scopulariopsis brumptii (type of Masonia grisea)
83/1.00
MUCL 7915T Microascus cirrosus (type of Torula paisii)
94/0.96
78/1.00
MUCL 9045T Scopulariopsis sphaerospora
IHEM 18567T Scopulariopsis murina
MUCL 9058 Microascus longirostris
IHEM 18608T Scopulariopsis atra
83/1.00
CBS 176.71T Microascus stoveri (type of Pithoascus stoveri)
CBS 197.61T Microascus nidicola
Pithoascus
CBS 819.70T Microascus exsertus
95/1.00
CBS 217.32T Microascus intermedius
MUCL 9027T Scopulariopsis carbonaria
UAMH 9169T Microascus soppii
MUCL 9031 Scopulariopsis flava
92/--
MUCL 40726T Microascus brevicaulis
CBS 170.27T Microascus manginii (type of Nephrospora manginii)
MUCL 40743T Scopulariopsis candida
Scopulariopsis
MUCL 9032T Scopulariopsis asperula (type of Scopulariopsis fusca)
MUCL 40746 Microascus niger
78/0.97
Microascaceae
MUCL 9012T Scopulariopsis asperula (type of Torula bestae)
CBS 435.86 Microascus schumacheri
91/1.00
UAMH 2643 Scopulariopsis hibernica
CBS 487.66 Wardomycopsis humicola
T
Pseudoscopulariopsis
Wardomycopsis
FMR 10305 Wardomycopsis inopinata
CBS 414.64 Microascus singularis
MUCL 8274 Scopulariopsis acremonium
MUCL 8409 Scopulariopsis acremonium
MUCL 9028T Scopulariopsis acremonium (type of Scopulariopsis danica)
78/--
Acaulium?
IHEM 18560 Microascus albonigrescens
CBS 536.87T Microascus caviariformis
90/1.00
CBS 251.69T Gamsia aggregata (type of Wardomyces aggregatus)
96/1.00
CBS 546.69T Gamsia simplex (type of Wardomyces simplex)
74/0.99
94/--
CBS
746.69T
Microascus giganteus
Gamsia
Wardomyces
CBS 216.61T Wardomyces inflatus
NBRC 100833 Trichurus spiralis
NBRC 7660 Trichurus terrophilus
99/--
CBS 139.42 Doratomyces purpureofuscus
CBS 127.22 Doratomyces stemonitis
NBRC 30864T Lophotrichus plumbescens
NBRC 32894 Lophotrichus macrosporus
NBRC 8200 Kernia nitida
--/1.00
0.05
Cephalotrichum
Lophotrichus
Kernia
NBRC 30413 Kernia pachypleura
CBS 418.73T Pseudallescheria ellipsoidea (type of Petriellidium ellipsoideum)
Scedosporium
CBS 330.93 Pseudallescheria boydii
CBS 116910 Scedosporium aurantiacum
CBS 127.84T Parascedosporium tectonae (type of Graphium tectonae)
98/0.97
CBS 311.72T Petriellopsis africana (type of Petriellidium africanum)
FMR 7736 Petriella setifera
Petriella
CBS 124169 Petriella sordida
CBS 102632T Graphium penicillioides
NBRC 101776T Hypocrea atroviridis
Parascedosporium
Petriellopsis
Graphium
Graphiaceae
NBRC 101777T Trichoderma asperellum
Fig. 1 Maximum likelihood (ML) tree obtained from the combined LSU and ITS sequences of 61 representative taxa of Microascaceae and Graphiaceae.
Numbers on the branches are ML bootstrap values (bs) above 70 %, followed by Bayesian posterior probabilities (pp) above 0.95. Full supported branches
are indicated in bold. Branch lengths are proportional to distance. Strains considered current members of the genera Microascus or Scopulariopsis genera are
represented in bold. Ex-type strains are indicated with T. The original name of each strain, when applied, is given between parenthesis. The tree was rooted
to Hypocrea atroviridis (NBRC 101776) and Trichoderma asperellum (NBRC 101777).
M. Sandoval-Denis et al.: Phylogeny of Microascus and Scopulariopsis
with a sampling frequency of every 100 generations. The 50 %
majority rule consensus trees and posterior probabilities (pp)
were calculated from 37 500 trees after discarding 12 500 trees
for burn-in. Posterior probability values equal or above 0.95
were considered significant. The resulting trees were plotted using FigTree v.1.3.1 (http://tree.bio.ed.ac.uk/software/figtree/).
The alignments originated in this study have been deposited
in TreeBASE (http://www.treebase.org).
Morphology
All isolates were grown on oatmeal agar (OA; 30 g filtered oat
flakes, 20 g agar, 1 L distilled water) and potato-carrot agar
(PCA; 20 g each of filtered potatoes and carrots, 20 g agar, 1 L
distilled water). They were incubated at different temperatures
(5, 15, 25, 30, 35, 37, 40 and 45 °C) and examined at 7 and 14 d
to determine colony growth rates. In descriptions, colour notations of the colonies were from Kornerup & Wanscher (1978).
Measurements and descriptions of microscopic structures were
made using an Olympus CH2 light microscope (Olympus Corporation, Tokyo, Japan) from cultures on PCA or OA at 25 °C
for 14 and 21 d to ensure ascomata development. All isolates
were examined on slides mounted on 85 % lactic acid. Features
of the sexual morph structures were obtained from squash preparations or spore mounts. Photographs of the microscopic structures were made using a Zeiss Axio Imager M1 light microscope
(Zeiss, Oberkochen, Germany) with a mounted DeltaPix Infinity
X digital camera using Nomarski differential interference contrast and phase contrast optics. Nomenclatural data was deposited in MycoBank (Crous et al. 2004).
RESULTS
Generic circumscription of the Microascaceae
To delineate generic boundaries, we conducted a phylogenetic
analysis using the combined LSU and ITS datasets including
54 currently accepted species belonging to 12 genera of Micro
ascaceae and one species of the family Graphiaceae. Tricho
derma asperellum and Trichoderma atroviride were selected
as outgroup (Fig. 1). The final alignment consisted of 63 taxa
and contained 996 characters (LSU 504, ITS 492), of which
618 were conserved and 297 were phylogenetically informative
(LSU 98, ITS 199). Fig. 1 shows the ML tree including bs and
pp values. The trees obtained from ML and Bayesian analyses of the individual loci and the combined analysis showed
congruent topologies.
The phylogenetic inferences showed that Microascus / Scopu
lariopsis were polyphyletic, with species distributed into several
distant lineages. However, most species of Microascus / Scopu
lariopsis clustered into a single large, well-supported lineage
(bs = 95 % / pp = 1.00). This lineage comprised four sublineages, which we interpret as three distinct genera, Microascus,
Pithoascus and Scopulariopsis, the fourth one representing a
putative undescribed genus.
The members of a sublineage referred to as Microascus were
characterised by dark-coloured colonies and mostly brown to
green-brown mycelia, conidiogenous apparatus and conidia.
The conidiogenous cells (annellides) were born singly on aerial
hyphae or on penicillate conidiophores. They were ampulliform
or lageniform and usually had a long and narrow cylindrical
annellated zone tapering gradually to the conidiogenous locus,
and produced smooth to roughened conidia. Sexual morphs
were observed in 13 species. Ascomata were ostiolate, rarely
non-ostiolate, mostly globose to ampulliform, glabrous or hairy,
papillate or with long cylindrical necks, and had a dark brown
to black peridium of textura angularis with exception of the
unidentified strains FMR 12362 and UTHSC 07-156, which show-
7
ed perithecia with peridia of textura intricata. The ascospores
ranged from reniform to ellipsoidal, triangular or quadrangular,
were straw-coloured to pale brown and exhibited a single,
mostly inconspicuous germ pore (Fig. 2a–h).
Members of the Pithoascus sublineage showed flat, white to
grey colonies without aerial mycelia. The mycelium and the
conidiogenous apparatus were subhyaline and the latter con
sisted of solitary, short, mostly ampulliform annellides with a
short-cylindrical neck. With the exception of strain IHEM 18608,
all strains of the Pithoascus clade exhibited a sexual morph
characterised by black ascomata with an inconspicuous ostiole and navicular to fusiform ascospores without germ pores
(Fig. 2i–n).
The Scopulariopsis sublineage included fungi with white, pale
grey, tan or brown colonies. The mycelium was mostly hyaline.
Annellides were hyaline or pale brown, more or less cylindrical,
with a wide, flat conidiogenous opening and mostly formed on
densely penicillate conidiophores. Conidia were hyaline or pale
brown, smooth or distinctly roughened, often showing a protru
ding base. A sexual morph was observed in four species and
was characterised by dark, globose to subglobose perithecia
with a peridium of textura angularis and with a papillate or a long
cylindrical ostiolar neck. Ascospores were reniform to broadly
lunate, hyaline or pale yellow, with a single, inconspicuous
germ pore (Fig. 2s–y).
The reference strains of Microascus schumacheri (CBS 435.86)
and Scopulariopsis hibernica (UAMH 2643) formed a well-supported clade (bs 91, pp 1.00), basal to the Scopulariopsis clade.
Because the former two taxa shared several morphological
features that deviated from those of Scopulariopsis, they were
accommodated in a new genus named Pseudoscopulariopsis.
Members of this clade were characterised by forming grey or
olivaceous colonies and hyaline to subhyaline conidiogenous
cells, which usually consisted of annellides arising from swollen
basal cells. The annellides were short, more or less ampulliform and with a cylindrical annellated zone. The sexual morph
was only observed in P. schumacheri, which produced black
perithecia and fusiform or navicular, straw-coloured ascospores
without germ pores (Fig. 2o–r).
However, this phylogenetic approach had insufficient resolution
to establish the limits among the different species included in
each genus. Similarly, the ex-type strain of Scopulariopsis car
bonaria (MUCL 9027) was related to the Scopulariopsis clade,
but its position was not resolved with this analysis.
The reference strain of Microascus singularis (CBS 414.64)
formed a solitary branch in an incertae sedis position. The main
morphological distinction of this isolate was the production of
conidia showing longitudinal bands. A strongly-supported clade,
composed by the ex-type strains of Microascus caviariformis
(CBS 536.87) and Scopulariopsis danica (MUCL 9028), two
reference strains of Scopulariopsis acremonium (MUCL 8274
and MUCL 8409) and a reference strain of Microascus al
bonigrescens (IHEM 18560), clustered apart from the genera
included in the study. The ex-type strain of Microascus gigan
teus (CBS 746.69) was placed very far from the Microascus
clade. It formed a well-supported clade with the ex-type strain
of Wardomyces inflatus (CBS 216.61) and with another fully
supported clade, which included several reference strains of the
genera Doratomyces and Trichurus. Our phylogenetic analyses
were concordant with the observations made by Abbott (2000),
who considered Doratomyces and Trichurus as congeneric with
Cephalotrichum, all being characterised by the formation of dryspored synnemata and lacking sexual morphs.
Lophotrichus and Kernia, characterised by hairy ascomata and
ellipsoidal ascospores with two germ-pores and graphium- or
8
Persoonia – Volume 36, 2016
Fig. 2 Key morphological features to distinguish Microascus (a – h), Pithoascus (Pi.) (i – n), Pseudoscopulariopsis (Ps.) (o – r) and Scopulariopsis (s – y). a, i,
o, s. Colonies on PCA after 21 d at 25 °C; b, c, j, k, p, t, u. conidiogenous cells; d – f, l, v, w. ascospores (germ pores indicated with arrows); g, h, m, n, q, r, x, y.
conidia (a, b, d. M. cinereus CBS 365.65; c. M. restrictus CBS 138277; e. M. trigonosporus CBS 218.31; f. M. pyramidus CBS 212.65; g. M. chartarus MUCL
9001; h. M. gracilis CBS 369.70; i, k, l, n. Pi. nidicola CBS 197.61; j, m. Pi. ater IHEM 18608; o – r. Ps. hibernica UAMH 2643; s, u, x. S. brevicaulis MUCL
40726; t, v, y. S. candida MUCL 40743; w. S. soppii UAMH 9169. — Scale bars: 5 µm.
9
M. Sandoval-Denis et al.: Phylogeny of Microascus and Scopulariopsis
scopulariopsis-like asexual morphs, respectively, formed wellsupported clades related to Scedosporium and allied genera
(i.e., Parascedosporium, Petriella and Petriellopsis), characterised by scedosporium-like asexual morphs with slimy conidia.
Some species traditionally included in Pithoascus and Scopu
lariopsis clustered in orders different from Microascales. The extype strain of Pithoascus platysporus (CBS 419.73) and a reference strain of Scopulariopsis coprophila (CBS 206.61) were
closely related to the Hypocreales; the ex-type strain of Scopulariopsis canadensis (CBS 204.61) grouped with members
of the Xylariales; the ex-type strains of Scopulariopsis parva
(MUCL 9041) and Scopulariopsis halophilica (CBS 380.74)
clustered outside the Sordariomycetes, being related to members of the Eurotiales (data not shown).
Species distribution in Microascus, Pithoascus,
Pseudoscopulariopsis and Scopulariopsis
The final alignment of the combined matrix included 106 strains
from Microascus, Pithoascus, Scopulariopsis and Pseudosco
pulariopsis species and involved 2 219 characters (LSU 437,
ITS 493, EF-1α 816, TUB 473), of which 1 493 were conserved,
673 were variable and 486 were phylogenetically informative
(LSU 47, ITS 112, EF-1α 176, TUB 151). Petriella setifera and
Parascedosporium tectonae were selected as outgroup taxa.
The resulting ML tree is shown in Fig. 3 including bs and pp values. The topology of the trees obtained from ML and Bayesian
analyses from each individual locus and the combined analysis
were concordant. The multilocus analysis confirmed the results
obtained from phylogenetic inferences using the combined LSU
and ITS dataset. In total 34 well-supported clades were resolved
and were distributed among four main lineages corresponding
to Microascus, Pithoascus, Scopulariopsis and the new genus
Pseudoscopulariopsis proposed here. The Microascus lineage
comprised 20 well-supported subclades, 13 of which included
an ex-type strain of a known species or a strain considered to be
authentic for a particular species, while seven subclades corresponded to new species, which are described here. Pithoascus
comprised five well-supported monophyletic subclades, each of
which included an ex-type strain of a known species. Scopulari
opsis encompassed six well-supported subclades, of which five
included an ex-type strain or a strain considered as authentic,
while one subclade corresponded to a new species described
here. The new genus Pseudoscopulariopsis encompassed two
subclades, each one including a single reference strain of a
species previously identified as Microascus or Scopulariopsis,
respectively.
In the combined phylogenetic analysis, the ex-type strain of
Scopulariopsis carbonaria (MUCL 9027) was basal to the
Microascus and Pithoascus clades. According to the original
description (Morton & Smith 1963), this species showed a high
similarity in annellidic and conidial morphology with members
of the Microascus lineage; however, after several attempts to
induce sporulation this strain remained sterile, and thus its
taxonomic position could not be resolved.
TAXONOMY
Based on the results of the above multilocus sequence analysis
and a morphological analysis, the boundaries of the genera
Microascus, Pithoascus and Scopulariopsis have been reassessed accordingly. Their current circumscription is revised and
several new taxa and combinations are proposed as follows:
Microascus Zukal, Verh. Zool.-Bot. Ges. Wien 35: 339. 1885
= Peristomium Lechmere, Compt. Rend. Hebd. Séances Acad. Sci. 154:
178. 1912.
= Masonia G. Sm., Trans. Brit. Mycol. Soc. 35: 149. 1952.
≡ Masoniella G. Sm., Trans. Brit. Mycol. Soc. 35: 237. 1952.
Type species. Microascus longirostris Zukal.
Colonies restricted or spreading, pale grey, brown, olivaceous
or black, velvety, floccose or fasciculate, granular and often
forming concentric rings due to the production of ascomata.
Ascomata perithecial, immersed or superficial, scattered or
aggregated, globose to ampulliform, glabrous or covered with
scattered hairs, ostiolate, usually with a neck of variable length
and shape, sometimes with a tuft of ostiolar hairs; peridium dark
brown or black, composed of thick-walled, slightly flattened
cells, textura angularis or textura intricata. Asci unitunicate,
8-spored, obovate, barrel-shaped or nearly globose, formed
in basipetal rows, evanescent. Ascospores 1-celled, asymmetrical, reniform, heart-shaped, triangular or quadrangular,
dextrinoid when young, extruded through the ostiole into a
gelatinous drop or a long cirrhus. Conidiogenous cells annellidic, borne singly and laterally on the vegetative hyphae, or in
groups of 2–5 on short simple or little branched conidiophores,
ampulliform or lageniform, subhyaline or darkening with age,
smooth- or rough-walled with a distinct cylindrical annellated
zone, Conidia 1-celled, pale yellowish to dark brown, globose
to subglobose, obovate or clavate, with a truncate base and
rounded or pointed at the apex, smooth- and thin-walled or
finely rough- and thick-walled, produced singly or in basipetal
dry chains. Solitary conidia present in some species, borne
sessile or on short stalks from the vegetative hyphae.
Microascus alveolaris Sandoval-Denis, Gené & Guarro, sp.
nov. — MycoBank MB809418, Fig. 4
Etymology. In reference to the isolation source of most isolates.
Colonies on OA and PCA at 25 °C attaining 31–36 and 18–29
mm diam, after 14 d, respectively, flat, slightly velvety, somewhat granular at the centre due to the presence of ascomata,
white to grey (4B1), abundant submerged mycelium in the outer
zone, with a wide white margin; reverse white to grey (4B1).
Vegetative hyphae septate, hyaline to light brown, smooth- and
thin-walled, 1.5–3 µm wide. Ascomata superficial or immersed,
formed predominantly at the centre of the colony, globose
to subglobose, 110 – 290 µm diam, usually with an ostiolar
cylindrical neck up to 100 µm long, black, glabrous, the apice
sometimes with a tuft of hyaline, septate and acicular hairs, up
to 60 µm long; peridium of textura angularis. Asci irregularly
ellipsoidal, 8–12 × 7.5–11 µm. Ascospores broadly triangular,
rarely reniform, 4–6 × 3–5 µm, with a single germ pore, straw
coloured, bright yellow in mass. Conidiophores absent or as a
basal single cell of 5–12 × 2–2.5 µm, bearing groups of 2–3
annellides, rarely slightly branched up to 80 µm long, hyaline
to subhyaline, smooth-walled. Annellides mostly sessile, single
and lateral on vegetative hyphae, lageniform, 6–17 × 1.5–3.5
µm, tapering slightly towards the annellated zone 1–2 µm wide,
hyaline to subhyaline, smooth- and thin-walled. Conidia ellipsoidal, navicular or bullet-shaped, 3–5 × 2–3.5 µm, with truncate
base and rounded apex, subhyaline to pale brown, brown in
mass, thin- and smooth-walled, arranged in long chains. Solitary conidia sometimes present, borne laterally from vegetative
hyphae, sessile or on short stalks, unicellular, subglobose or
obovoidal, 3–5 × 2.5–4 µm, subhyaline or pale brown, smoothand more or less thick-walled.
Cardinal temperature for growth — Optimum 25 – 30 °C,
maximum 40 °C, minimum 15 °C.
10
Persoonia – Volume 36, 2016
UTHSC 08-886 Microascus sp.
--/0.99
UTHSC 05-3416 Microascus sp.
UTHSC 07-3491T Microascus sp.
0.05
UTHSC 10-214 Microascus sp.
UTHSC 04-1534 Microascus sp.
UTHSC 06-3152 Microascus sp.
M. alveolaris
UTHSC 07-1823 Microascus sp.
92/1.00
UTHSC R-4634 Microascus sp.
UTHSC 05-1041 Microascus sp.
CBS 369.70T Scopulariopsis gracilis (Isotype of Paecilomyces fuscatus)
UTHSC 09-1829 Scopulariopsis gracilis
MUCL 9049 Microascus cinereus
UTHSC 09-1351 Scopulariopsis gracilis
M. gracilis
UTHSC 10-390 Scopulariopsis gracilis
MUCL 9048 Microascus cinereus
MUCL 9054 Microascus desmosporus
UTHSC 07-1887 Microascus cirrosus
UTHSC 11-14 Microascus cirrosus
89/1.00
CBS 217.31T Microascus cirrosus
88/1.00
CBS 138709NT Microascus cinereus
UTHSC 11-383 Microascus cinereus
85/--
UTHSC 09-573 Microascus cinereus
UTHSC 06-3278 Microascus cinereus
M. cinereus
UTHSC 08-3181 Microascus cinereus
79/1.00
CBS 365.65T Microascus cinereus (Type of Microascus griseus)
73/0.95
CBS 212.65T Microascus pyramidus
CBS 662.71 Microascus trigonosporus var. macrosporus
--/0.95
IHEM 18561T Microascus senegalensis
MUCL 9001T Scopulariopsis chartarum (Type of Masonia chartarum)
CBS 218.31T Microascus trigonosporus
73/0.97
M. cirrosus
MUCL 9050 Microascus cirrosus
MUCL 9061 Microascus trigonosporus
MUCL 9841 Scopulariopsis coprophila
CBS 138127T Microascus sp.
UTHSC 06-2519 Microascus sp.
CBS 766.70 Kernia hyalina
T
90/0.96
72/0.97
MUCL 9005T Scopulariopsis brumptii (Type of Masoniella tertia)
MUCL 9002T Scopulariopsis croci (Type of Masoniella croci)
MUCL 4004 Scopulariopsis croci
72/0.95
M. pyramidus
M. macrosporus
M. senegalensis
M. chartarus
Microascus
M. trigonosporus
M. expansus
M. hyalinus
M. croci
FMR 3997 Scopulariopsis brumptii
CBS 138126T Microascus sp.
M. campaniformis
MUCL 7915T Scopulariopsis paisii (Type of Torula paisii)
83/1.00
MUCL 9045T Scopulariopsis sphaerospora
MUCL 8991 Scopulariopsis chartarum
MUCL 8989 Scopulariopsis brumptii
MUCL 9003T Scopulariopsis brumptii (Type of Masoniella grisea)
--/1.00
MUCL 8993 Scopulariopsis chartarum
UTHSC 09-2391 Scopulariopsis brumptii
MUCL 9040T Scopulariopsis brumptii (Type of Scopulariopsis melanospora)
M. paisii
MUCL 8990 Scopulariopsis brumptii
UTHSC 07-639 Scopulariopsis brumptii
93/0.95
UTHSC 11-708 Scopulariopsis brumptii
98/0.99
UTHSC 10-2920 Scopulariopsis brumptii
UTHSC 09-457 Scopulariopsis brumptii
UTHSC08-1734 Scopulariopsis brumptii
IHEM 18567T Scopulariopsis murina
CBS 138278T Microascus sp.
CBS 138277T Microascus sp.
CBS 138276T Microascus sp.
97/0.99
93/1.00
CBS 138128T Microascus sp.
FMR 12362 Microascus sp.
CBS 196.61NT Microascus longirostris
CBS 415.64 Microascus longirostris
M. murinus
M. verrucosus
M. restrictus
M. brunneosporus
M. intricatus
M. longirostris
Fig. 3 Maximum likelihood (ML) tree obtained from the combined ITS, LSU, EF-1α and TUB sequences of 105 strains from Microascus, Pithoascus, Pseudo
scopulariopsis and Scopulariopsis species. Numbers on the branches are ML bootstrap values (bs) above 70 %, followed by Bayesian posterior probabilities
(pp) above 0.95. Full supported branches are indicated in bold. Branch lengths are proportional to distance. Ex-type strains are indicated with T. Ex-neotype
strains are indicated with NT. The original name of each strain, when applied, is given on parenthesis. The tree was rooted to Petriella setifera (CBS 437.75)
and Parascedosporium tectonae (CBS 127.84).
11
M. Sandoval-Denis et al.: Phylogeny of Microascus and Scopulariopsis
IHEM 18608T Scopulariopsis atra
CBS 176.71T Microascus stoveri (Type of Pithoascus stoveri)
90/1.00
--/1.00
96/0.98
97/1.00
CBS 197.61T Microascus nidicola
CBS 217.32T Microascus intermedius
CBS 819.70T Microascus exsertus
P. ater
P. stoveri
P. nidicola
P. intermedius
Pithoascus
P. exsertus
CBS 583.75 Microascus exsertus
MUCL 9027T Scopulariopsis carbonaria
MUCL 9031NT Scopulariopsis flava
88/--
S. flava
S. soppii
UAMH 9169T Microascus soppi
81/0.99
UTHSC 09-3241 Scopulariopsis candida
85/0.97
UTHSC 09-2576 Scopulariopsis candida
--/1.00
MUCL 9026 Scopulariopsis candelabrum
CBS 170.27T Microascus manginii (Type of Nephrospora manginii)
S. candida
MUCL 9007 Scopulariopsis alboflavescens
MUCL 12598 Microascus manginii
MUCL 40743T Scopulariopsis candida
MUCL 40746 Microascus niger
MUCL 9012T Scopulariopsis asperula (Type of Torula bestae)
MUCL 9032T Scopulariopsis asperula (Type of Scopulariopsis fusca)
CBS 853.68 Scopulariopsis asperula
S. asperula
MUCL 40729 Microascus niger
UTHSC 10-3405 Scopulariopsis fusca
71/0.97
CBS 138129T Scopulariopsis sp.
S. cordiae
UTHSC 05-3453 Scopulariopsis sp.
99/1.00
Scopulariopsis
UTHSC 08-1920 Scopulariopsis brevicaulis
CBS 208.61 Scopulariopsis koningii
88/--
CBS 399.34T Scopulariopsis alboflavescens
92/1.00
UTHSC 09-1092 Scopulariopsis brevicaulis
UTHSC 09-1373 Scopulariopsis brevicaulis
UTHSC 11-427 Scopulariopsis brevicaulis
UTHSC 11-1240 Scopulariopsis brevicaulis
S. brevicaulis
UTHSC 07-1888 Scopulariopsis brevicaulis
99/--
UTHSC 11-1563 Scopulariopsis brevicaulis
UTHSC 06-619 Scopulariopsis brevicaulis
UTHSC 06-277 Scopulariopsis brevicaulis
UTHSC 07-1812 Scopulariopsis brevicaulis
MUCL 9035 Scopulariopsis insectivora
MUCL 14213 Scopulariopsis stercoraria
MUCL 40726T Scopulariopsis brevicaulis (Type of Microascus brevicaulis)
UAMH 2643 Scopulariopsis hibernica
CBS 435.86NT Microascus schumacheri
CBS 437.75 Petriella setifera
P. hibernica
Pseudoscopulariopsis
P. schumacheri
CBS 127.84T Parascedosporium tectonae (Type of Graphium tectonae)
0.05
Fig. 3 (cont.)
Specimens examined. USA, from bronchoalveolar lavage fluid, 2007,
D.A. Sutton (holotype CBS H-22111, culture ex-type CBS 139501 = UTHSC
07-3491 = FMR 12252); from sputum, 2005, D.A. Sutton (UTHSC 05-1041 =
FMR 12351); from bronchoalveolar lavage fluid, 2005, D.A. Sutton (UTHSC
05-3416 = FMR 12350); from bronchoalveolar lavage fluid, 2006, D.A. Sutton
(UTHSC 06-3152 = FMR 12346); from sputum, 2007, D.A. Sutton (UTHSC
07-1823 = FMR 12342); from bronchoalveolar lavage fluid, 2004, D.A. Sutton
(UTHSC 04-1534 = FMR 12354); from bronchoalveolar lavage fluid, 2008,
D.A. Sutton (UTHSC 08-886 = FMR 12340); from bronchoalveolar lavage
fluid, 2010, D.A. Sutton (UTHSC 10-214 = FMR 12336); from lung tissue,
D.A. Sutton (UTHSC R-4634 = FMR 12333).
Notes — All the strains included in this species were isolated
from the respiratory tract of human patients. Morphologically,
M. alveolaris is close to M. campaniformis, M. macrosporus,
M. pyramidus and M. trigonosporus, all showing similar triangularshaped ascospores. Microascus alveolaris can be differentiated
by its membranous and white colonies, the smaller size of the
ascospores and narrower conidia.
Microascus brunneosporus Sandoval-Denis, Gené & Guarro,
sp. nov. — MycoBank MB809419, Fig. 5
Etymology. From the Latin brunneus-, brown, referring to the colour of
the ascospores.
Colonies on OA at 25 °C attaining 21–25 mm diam in 14 d, flat,
velvety, granular at the centre due to the presence of ascomata,
dull green (30E3) to olive-brown (4F4), with submerged mycelium towards the outer zone, margin regular; reverse dark
green (30F4). On PCA at 25 °C attaining 15–17 mm diam in
14 d, slightly elevated, downy, fasciculate at the centre, dull
green (30E3), with a white and regular margin; reverse dull
green (30D4). Vegetative hyphae septate, subhyaline to pale
brown, smooth- and thin-walled, 1.5–3 µm wide. Ascomata
immersed, globose, 110–205 µm diam, with a short cylindrical
ostiolar neck up to 40 µm long, black, glabrous; peridium with a
textura angularis. Asci irregularly ellipsoidal or ovoidal, 11–14
× 7–8 µm. Ascospores ellipsoidal to allantoid, 5–7 × 2–3 µm,
light yellow-brown, brown in mass, with a single and inconspicuous germ pore. Conidiophores absent or as a basal single cell
of 5–15 × 1.5–2.5 µm, bearing 1–3 annellides, rarely slightly
12
Persoonia – Volume 36, 2016
Fig. 4 Microascus alveolaris CBS 139501. a, b. Colonies on OA and PCA, respectively, after 21 d at 25 °C; c. ascoma; d. peridium; e – g. asci and ascospores;
h – j. conidiophores, annellides and conidia; k, l. solitary conidia. — Scale bars: c = 30 µm; h, i = 10 µm; all others = 5 µm.
M. Sandoval-Denis et al.: Phylogeny of Microascus and Scopulariopsis
13
Fig. 5 Microascus brunneosporus CBS 138276. a, b. Colonies on OA and PCA, respectively, after 21 d at 25 °C; c. ascoma; d. peridium; e – h. asci and
ascospores; i–k. conidiophores, annellides and conidia; l. conidial chain. — Scale bars: c = 50 µm; all others = 5 µm.
14
Persoonia – Volume 36, 2016
Fig. 6 Microascus campaniformis CBS 138126. a, b. Colonies on OA and PCA, respectively, after 21 d at 25 °C; c. ascoma; d. peridium; e, f. asci and ascospores; g–j. conidiophores, annellides and conidia. — Scale bars: c = 50 µm; g = 10 µm; all others = 5 µm.
15
M. Sandoval-Denis et al.: Phylogeny of Microascus and Scopulariopsis
branched up to 30 µm long, subhyaline, smooth-walled. Annel
lides mostly sessile, single and lateral on vegetative hyphae,
more or less lageniform, 9–14 × 2–2.5 µm, tapering to a cylindrical
annellated zone 1–1.5 µm wide, subhyaline, smooth- or roughwalled, thin-walled. Conidia subglobose, ellipsoidal or navicular, 4 – 5 × 2.5 – 5 µm, with truncate base, light green-brown,
thin- and smooth-walled, arranged in long chains. Solitary conidia not observed.
Cardinal temperature for growth — Optimum 25 – 30 °C,
maximum 35 °C, minimum 15 °C.
Microascus chartarus (G. Sm.) Sandoval-Denis, Gené &
Guarro, comb. nov. — MycoBank MB809206
Specimen examined. USA, from bronchoalveolar lavage fluid, 2006, D.A.
Sutton (holotype CBS H-21783, culture ex-type CBS 138276 = UTHSC 064312 = FMR 12343).
Notes — Microascus chartarus has been reported from soil,
dust and indoor-air (Domsch et al. 2007). It was originally de
scribed as a member of Masonia G. Sm. (1952a). However, Ma
sonia is an illegitimate homonym of Masonia Hansford (1944),
and thus the new genus Masoniella was erected (Smith 1952b).
Most members of Masoniella were later transferred to Scopu
lariopsis (Morton & Smith 1963); both genera share the same
conidiogenesis (annellidic, percurrent) and conidiogenous cells,
distinctly narrower at the base, then swollen, and ending in a
slender annellidic zone. Our phylogenetic analysis shows that
M. chartarus is included in the Microascus sublineage and it is
closely related to M. trigonosporus. Microascus trigonosporus
can be distinguished by the production of a sexual morph, with
triangular ascospores and mostly globose to subglobose and
pale brown conidia. No sexual morph is known for M. chartarus
and its conidia are ovate, often with a pointed end, green-brown
(Morton & Smith 1963). Microascus croci and M. paisii resemble
M. chartarus and also lack a sexual morph. However, these two
species can be differentiated from M. chartarus by their conidial
shape and colour, which are globose and ellipsoidal to short
clavate in M. croci and M. paisii, respectively, and pale brown in
both species. In addition, M. croci is able to grow from 5–30 °C
and M. paisii grows from 15–37 °C, while M. chartarus has a
narrower temperature range growing from 15 –25 °C.
Notes — This species is similar to M. cinereus and M. graci
lis. However, the latter two species produce reniform or broadly
lunate, straw coloured ascospores with an often conspicuous
germ pore.
Microascus campaniformis Sandoval-Denis, Cano & Deanna
A. Sutton, sp. nov. — MycoBank MB809205, Fig. 6
Etymology. From the Latin campanus-, bell, referring to the shape of the
ascospores.
Colonies on OA at 25 °C attaining 27–34 mm diam in 14 d, flat,
velvety to slightly granular at the centre, dull green (30E4), with
an irregular margin; reverse dull green (30E4). On PCA at 25 °C,
colonies attaining 14 – 25 mm diam in 14 d, flat, velvety, fluffy
at the centre, dull green (28E4) to dark green (30E4), with a
white and regular margin; reverse dark green (28F3). Vegetative
hyphae septate, subhyaline, smooth- or rough- and thin-walled,
1.5–2.5 µm wide. Ascomata immersed or superficial, usually
formed at the periphery of the colony, globose to subglobose,
150–220 µm diam, with a short cylindrical ostiolar neck up to
80 µm long, widening at the ostiolar opening, rarely with a tuft
of hyaline, straight and septate hairs up to 50 µm long, black,
glabrous; peridium with a textura angularis. Asci irregularly ellipsoidal or subglobose, 18–21 × 10–15 µm. Ascospores broadly triangular, 6 –7 × 4 – 4.5 µm, often with an elongated side towards a single germ pore, straw coloured, bright yellow-orange
in mass. Conidiophores absent or as a basal cell of 5 × 2 µm,
bearing groups of 5 – 8 annellides, or slightly branched up to
60 µm long, hyaline to subhyaline, smooth-walled. Annellides
somewhat lageniform, 9 –14 × 2 – 3 µm, with a more or less
swollen base and tapering abruptly to a cylindrical annellated
zone, 1–1.5 µm wide. Conidia subglobose to broadly ellipsoidal,
4–5 × 2.5–3.5 µm, with a truncate base, light green-brown, dark
brown in mass, thick-walled, arranged in long chains. Solitary
conidia and chlamydospores not observed.
Cardinal temperature for growth — Optimum 25 – 30 °C,
maximum 40 °C, minimum 15 °C.
Specimen examined. USA, from bronchoalveolar lavage fluid, 2010, D.A.
Sutton (holotype CBS H-21784, culture ex-type CBS 138126 = UTHSC 10565 = FMR 12334).
Notes — Microascus campaniformis is similar to M. alveo
laris, M. macrosporus, M. pyramidus and M. trigonosporus in
having distinctive triangular shaped ascospores. However,
M. campaniformis can be differentiated by its green colonies
and inequilateral ascospores that show an elongation at one
side towards the germ pore. In contrast, the ascospores of
M. alveolaris, M. macrosporus and M. trigonosporus are almost
equilateral with rounded ends, while those of M. pyramidus have
attenuated ends acquiring a nearly square shape. Microascus
campaniformis is phylogenetically close to M. paisii sharing
similar annellides. However, a sexual morph has not been ob
served in M. paisii.
Basionym. Masonia chartarum G. Sm., Trans. Brit. Mycol. Soc. 35: 150.
1952.
≡ Masoniella chartarum (G. Sm.) G. Sm., Trans. Brit. Mycol. Soc. 35:
237. 1952.
≡ Scopulariopsis chartarum (G. Sm.) F.J. Morton & G. Sm., Mycol. Pap.
86: 64. 1963.
Specimen examined. UK, London, isolated from mouldy wall-paper, 1950,
K. Maunsell (Masonia chartarum ex-type culture CBS 294.52 = MUCL 9001).
Microascus cinereus (Émile-Weil & Gaudin) Curzi, Boll. Staz.
Patolog. Veget. Roma 11: 60. 1931.
Basionym. Scopulariopsis cinerea Émile-Weil & Gaudin, Arch. Méd. Exp.
Anat. Path. 28: 452. 1919.
= Scopulariopsis oidiospora Zach, Oesterr. Bot. Z. 83: 182. 1934.
= Microascus lunasporus P.M. Jones, Mycologia 28: 503. 1936.
≡ Scopulariopsis lunaspora P.M. Jones, Mycologia 28: 504. 1936.
= Microascus pedrosoi C.A. Fuentes & F.A. Wolf, Mycologia 48: 63. 1956.
= Microascus griseus P.N. Matur & Thirum., Sydowia 16: 49. 1962.
= Microascus reniformis Orr, Persoonia 8: 194. 1975.
Specimens examined. India, Maharashtra, Poona, from soil, 1965, M.J.
Thirumalachar (M. griseus ex-type culture CBS 365.65 = ATCC 16204). –
USA, from bronchoalveolar lavage fluid, 2010, D.A. Sutton (neotype of M. cinereus designated here CBS H-21937, MBT198511) culture ex-neotype CBS
138709 = UTHSC 10-2805 = FMR 12217; from bronchoalveolar lavage fluid,
2006, D.A. Sutton (UTHSC 06-3278 = FMR 12345); from sternum tissue,
2008, D.A. Sutton (UTHSC 08-3181 = FMR 12339); from bronchoalveolar
lavage fluid, 2009, D.A. Sutton (UTHSC 09-573 = FMR 12239); from bronchoalveolar lavage fluid, 2009, D.A. Sutton (UTHSC 11-383 = FMR 12331).
Notes — Microascus cinereus has a widespread distribution
and a wide range of substrates. It has been isolated mainly from
stored cereals, soil and dung (Barron et al. 1961, Udagawa
1962, Guarro et al. 2012), but it has also been described as
an opportunistic pathogen of animals and humans (Baddley
et al. 2000, de Hoog et al. 2011, Sandoval-Denis et al. 2013).
Descriptions of M. cinereus are available in Barron et al. (1961)
and Guarro et al. (2012). However, according to our observations, their measurements might have included isolates of
Microascus gracilis from which M. cinereus has to be differentiated (Sandoval-Denis et al. 2013). The isolates of M. cinereus
studied here showed asci 7–12 × 5–10 µm, ascospores 4–5.5
× 2.5 – 4 µm and conidia 3 – 5 × 2 – 3 µm. In addition, while
16
Persoonia – Volume 36, 2016
Fig. 7 Microascus expansus CBS 138127. a, b. Colonies on OA and PCA, respectively, after 21 d at 25 °C; c – g. conidiophores, annellides and conidia;
h. conidial chains. — Scale bars: c, d = 10 µm; all others = 5 µm.
17
M. Sandoval-Denis et al.: Phylogeny of Microascus and Scopulariopsis
M. cinereus produces pale to dark or black-grey colonies, at
first velvety becoming slightly granular due to the presence of
ascomata, M. gracilis produces dull green colonies, becoming
olive-grey to olive-brown with ascomata mostly covered by
aerial mycelium. Since no ex-type material of M. cinereus is
available, the strain CBS 138709 (UTHSC 10-2805) is proposed
here as neotype. Despite the existence of an ex-type culture of
M. griseus, a synonym of M. cinereus, we consider it important
to neotypify M. cinereus in order to conserve the oldest and
most widely used epithet of this taxon. The original description of
M. cinereus was based on an isolate obtained from a human nail
but none of the isolates available share this original substrate.
However, we believe that the isolate CBS 138709 (UTHSC 102805), obtained from human bronchoalveolar fluid agrees with
the original and modern descriptions of this species (Émile-Weil
& Gaudin 1919, Barron et al. 1961, Guarro et al. 2012).
Microascus cirrosus Curzi, Boll. Staz. Patol. Veg. Roma 10:
308. 1930
Specimens examined. Italy, from a leaf of Prunus sp., 1931, M. Curzi
(ex-type culture CBS 217.31); from root of Vitis vinifera, 1934, M. Curzi (CBS
277.34 = MUCL 9050). – UK, from unknown substrate, 1961, G. Smith (CBS
301.61 = MUCL 9054). – USA, from sputum, 2007, D.A. Sutton (UTHSC 071887 = FMR 12256); from bronchoalveolar lavage fluid, 2011, D.A. Sutton
(UTHSC 11-14 = FMR 12332).
Notes — Microascus cirrosus is a saprobic species with a
worldwide distribution, commonly isolated from soil and dung
(Barron et al. 1961, von Arx et al. 1988, Guarro et al. 2012).
It has also been associated to superficial and respiratory human infections (de Hoog et al. 2011, Sandoval-Denis et al.
2013). Morton & Smith (1963) considered the asexual morph
of this species to be conspecific with Scopulariopsis paisii
(see Microascus paisii ). However, according to our results,
the ex-type strain of Torula paisii (MUCL 7915) was shown to
be phylogenetically distant to the ex-type strain of M. cirrosus
(CBS 217.31), and thus should be considered as a distinct
species. Microascus cirrosus can be distinguished by having
subglobose to obovate conidia measuring 4 – 6.5 × 4–6 µm,
while those of M. paisii are broadly ellipsoidal to short clavate,
measuring 4–6 × 2–4.5 µm. Microascus cirrosus is also similar
to M. cinereus. However, M. cirrosus produces broadly reniform
ascospores measuring 5–6 × 3–4 µm and larger conidia, while
M. cinereus produces broadly lunate or almost triangular asco
spores measuring 4 –5.5 × 2.5 – 4 µm, and obovate to clavate
conidia measuring 3 – 5 × 2 – 3 µm.
Microascus croci (J.F.H. Beyma) Sandoval-Denis, Gené &
Guarro, comb. nov. — MycoBank MB809207
Basionym. Scopulariopsis croci J.F.H. Beyma, Antonie van Leeuwenhoek
10: 52. 1945.
≡ Masoniella croci (J.F.H. Beyma) G. Sm., Trans. Brit. Mycol. Soc. 37:
166. 1954.
= Masoniella tertia Bat., J.A. Lima & C.T. Vasconc., Publções Inst. Micol.
Recife. 263: 14. 1960.
Specimens examined. Brazil, Pernambuco, Recife, isolate from air, 1952,
A. Batista (Masoniella tertia ex-type culture MUCL 9005 = CBS 296.61). –
Spain, Tarragona, Riumar, from aquatic sediment of the Ebro River, May
1991, K. Ulfig & J. Gené (FMR 3997); Barcelona, from aquatic sediment of
the Besós river, July 1991, J. Gené (FMR 4004). – The Netherlands, Lisse,
from Crocus sp. Queen of the blues, 1943, H. Diddens (Scopulariopsis croci
ex-type culture MUCL 9002 = CBS 158.44).
Notes — The clade representing M. croci included isolates
from air, aquatic sediments, soil and plants, originating from
Europe and South America. Masoniella tertia was considered
a synonym of S. melanospora (Udagawa 1959) and a later
synonym of S. brumptii (Morton & Smith 1963). However, the
current combined analysis showed that the ex-type cultures of
M. tertia and S. melanospora are phylogenetically unrelated,
which agrees with their morphological features. All the isolates
included in this clade have mostly globose conidia and are able
to grow from 5–30 °C. Although no sexual morph has been
reported for this species, one of the strains tested here (FMR
4004) was able to produce small and sterile peritecial-like
ascomata after 8 mo of incubation on OA.
Microascus expansus Sandoval-Denis, Gené & Cano, sp. nov.
— MycoBank MB809208, Fig. 7
Etymology. From the Latin expansio-, expansion, referring to the quick
growth of the colonies.
Colonies on OA and PCA at 25 °C growing rapidly, 65–81 and
70–75 mm diam, respectively, in 14 d, flat, velvety to powdery,
more or less funiculose at the centre, olive (3F3) to grey-brown
(4–5F3), with an irregular margin; reverse olive grey (2F2) or
olive (2F4). Vegetative hyphae septate, hyaline to pale brown,
smooth- and thin-walled, 1.5–3 µm wide. Conidiophores absent
or as a basal single cell of 4–5 × 2–4 µm, bearing groups of
2–5 annellides, or slightly branched up to 20 µm long, hyaline
to subhyaline, smooth-walled. Annellides slightly lageniform or
somewhat subulate, 5–12 × 1.5–3.5 µm, tapering to a cylindrical annellated zone 1.5–2 µm wide, smooth-walled. Conidia
bullet-shaped or broadly clavate, 4–8 × 2.5–3.5 µm, with a
distinctive truncate base and rounded or slightly pointed apex,
subhyaline to pale brown in mass, smooth- or finely roughened,
thick-walled, arranged in long chains. Sexual morph not observed.
Cardinal temperature for growth — Optimum 25 – 30 °C,
maximum 40 °C, minimum 15 °C.
Specimens examined. USA, from sputum, 2006, D.A. Sutton (holotype
CBS H-21785, culture ex-type CBS 138127 = UTHSC 06-4472 = FMR
12266); from pleural fluid, 2006, D.A. Sutton (UTHSC 06-2519 = FMR 12267).
Notes — Microascus expansus is known thus far from clinical
isolates of human origin. Both isolates are able to grow at 40 °C.
Other Microascus species able to grow at this temperature
are M. alveolaris, M. campaniformis, M. cinereus, M. cirrosus,
M. gracilis, M. intricatus, M. macrosporus, M. pyramidus and
M. restrictus. However, except M. restrictus, all these species
produce sexual morphs, while M. expansus produces only the
asexual morph. Microascus expansus can be differentiated
from M. restrictus by a faster growth rate, reaching > 60 mm
diam at 25–30 °C in 14 d.
Microascus gracilis (Samson) Sandoval-Denis, Gené &
Guarro, comb. nov. — MycoBank MB809209
Basionym. Scopulariopsis gracilis Samson, Arch. Mikrobiol. 85: 179.
1972.
≡ Paecilomyces fuscatus N. Inagaki, Trans. Mycol. Soc. Japan 4: 4. 1962.
Specimens examined. Japan, from wheat flour, 1970, N. Inagaki (Paecilo
myces fuscatus ex-type culture CBS 369.70). – UK, isolate from soil, 1959,
J. Mendy (MUCL 9048 = CBS 195.61). – USA, Iowa, isolate from a seed of
Zea mays, 1961, G.L. Barron (MUCL 9049 = CBS 300.61); from synovial fluid,
2009, D.A. Sutton (UTHSC 09-1351 = FMR 12234); from bronchoalveolar
lavage fluid, 2009, D.A. Sutton (UTHSC 09-1829 = FMR 12231); from bronchoalveolar lavage fluid, 2010, D.A. Sutton (UTHSC 10-390 = FMR 12335).
Notes — Scopulariopsis gracilis was proposed by Samson &
von Klopotek (1972) as a new name for Paecilomyces fuscatus,
probably to avoid nomenclatural conflict with Scopulariopsis
fusca (Zach 1934).
Microascus gracilis has been isolated mainly from food in Asia,
North and South America, and from soil in Europe. Recently,
this species was reported from human clinical specimens, but
its pathogenicity has not been demonstrated (Sandoval-Denis
18
Persoonia – Volume 36, 2016
Fig. 8 Microascus intricatus CBS 138128. a, b. Colonies on OA and PCA, respectively, after 21 d at 25 °C; c. ascoma; d. peridium; e, f. asci and ascospores;
g, h. conidiophores, annellides and conidia; i. conidial chain. — Scale bars: c = 40 µm; all others = 5 µm.
M. Sandoval-Denis et al.: Phylogeny of Microascus and Scopulariopsis
et al. 2013). Microascus gracilis and M. cinereus are very similar
making their identification difficult in the absence of the sexual
morph; in fact two reference strains (MUCL 9048 and MUCL
9049) and some clinical isolates were previously identified as
M. cinereus. However, sequence comparison revealed that
these species only showed 98.1 %, 97.8 % and 97 % sequence
similarity for ITS, EF-1α and TUB, respectively. Morphologically
M. gracilis can be differ-entiated from M. cinereus by its lunate
ascospores, measuring 4.5 – 6.5 × 2 – 4 µm (as opposed to reniform to broadly lunate ascospores measuring 4 – 5.5 × 2.5–4
µm in M. cinereus), asci measuring 8 –18 × 6 –10 µm (against
7–12 × 5 –10 µm in M. cinereus), the formation of complex
conidiophores and the morphology and colour of the colony.
The asexual-morph of M. gracilis also resembles to that of
M. murinus and M. paisii. However, M. gracilis produces annel
lides 5 – 20 × 1– 2.5 µm, usually formed on well-defined and
branched conidiophores, and subglobose to ellipsoidal conidia
3.5–5.5 × 2–3.5 µm; the annellides of M. murinus and M. paisii are
shorter (6.5 –11 × 1.7– 2.5 µm and 10 –14 × 2 – 2.5 µm, respec
tively) borne mostly from the aerial mycelium and producing
cylindrical and broadly ellipsoidal conidia, respectively.
Microascus hyalinus (Malloch & Cain) Sandoval-Denis, Gené
& Guarro, comb. nov. — MycoBank MB809210
Basionym. Kernia hyalina Malloch & Cain, Canad. J. Bot. 49: 860. 1971.
Specimen examined. USA, from cow dung, 1964, J.C. Krug (ex-type
culture CBS 766.70).
Notes — This species has been isolated from soil and dung
in Europe and North America (Malloch & Cain 1971, Guarro
et al. 2012). The species was originally described in Kernia by
Malloch & Cain (1971), although deviating considerably from
the typical features of Kernia such as restricted growth, nonostiolate, hairy ascomata, and ellipsoidal to reniform, orange
to copper coloured ascospores with a germ pore at each end
(Malloch & Cain 1971, von Arx 1978). Although several species of Kernia have been described with a scopulariopsis-like
asexual morph, our phylogenetic analysis based on a combined
LSU and ITS sequence dataset (Fig. 1) showed Kernia to be
phylogenetically distant to both Scopulariopsis and Microascus.
However, K. hyalina is shown to have more affinity with species
of Microascus rather than with species of Kernia nested within
the Microascus lineage, a relationship previously suggested by
Issakainen et al. (2003). The lack of ascomatal appendages,
the production of hyaline to yellowish ascospores with a single
germ pore, the shape and colour of the annellides and conidia,
and the growth rate of the colonies point toward Microascus
rather than toward Kernia. Therefore, our phylogenetic and
morphological data confirm this taxon as a distinct species in
Microascus.
Microascus intricatus Sandoval-Denis, Stchigel & Deanna A.
Sutton, sp. nov. — MycoBank MB809211, Fig. 8
Etymology. Referring to the textura intricata of the peridium.
Colonies on OA at 25 °C growing rather slowly, attaining 28–30
mm diam in 14 d, flat, finely granular, with scarce aerial mycelium, olive grey (2F2), with a white regular margin; reverse
white to grey. On PCA at 25 °C colonies attaining 35 –38 mm
diam in 14 d, flat, velvety to finely granular, with a densely
fasciculate centre, olive brown (4F3/4F4), with a white regular
margin; reverse olive brown (4F3/4F4). Vegetative hyphae
septate, subhyaline to light brown, smooth- and thin-walled,
2–2.5 µm wide. Ascomata immersed or superficial, globose
to subglobose, 140 – 200 µm diam, with a papillate to short
cylindrical ostiolar neck up to 40 µm long, black, glabrous;
peridium with a textura intricata. Asci irregularly ellipsoidal or
19
subglobose, 7.5–9.5 × 5.5–6.5 µm. Ascospores fusiform, 5–6
× 2.5–3.5 µm, straw coloured, yellow-orange in mass, with one
inconspicuous germ pore. Conidiophores absent or as a basal
single cell, of 2.5–3 × 3–5 µm, bearing groups of 2–3 annellides, or slightly branched up to 50 µm long, septate, subhyaline,
smooth-walled. Annellides mostly sessile, single and lateral
on vegetative hyphae, more or less ampulliform, 8–10(–11) ×
2–2.5 µm, with a swollen base, tapering abruptly to a cylindrical
annellated zone, 1–1.5 µm wide, subhyaline, smooth-walled.
Conidia globose to broadly ellipsoidal, 4–5 × 3–3.5 µm, with
truncate base, pale brown, dark brown in mass, and smooth- to
rough-walled, thin-walled, arranged in long chains.
Cardinal temperature for growth — Optimum 25 – 30 °C,
maximum 40 °C, minimum 15 °C.
Specimens examined. Argentina, Iguazú, from soil, Calduch, Guarro
& Stchigel (FMR 12362). – USA, from bronchoalveolar lavage fluid, 2007,
D.A. Sutton (holotype CBS H-21786, culture ex-type CBS 138128 = UTHSC
07-156 = FMR 12264).
Notes — Microascus intricatus is described on the basis
of two strains, isolated from a clinical (human) sample in the
USA and from soil, in Argentina. This species deviates from the
other congeneric species in having a perithecial peridium wall
with textura intricata and by forming short fusiform ascospores.
Nonetheless, the abundant conidiation and ascomata with
straw-coloured ascospores bearing a single germ pore match
with the circumscription of Microascus, confirming our phylogenetic results.
Microascus longirostris Zukal, Verh. Zool.-Bot. Ges. Wien
35: 33. 1885
= Microascus variabilis Massee & E.S. Salmon, Ann. Bot., Lond. 15: 349.
1901.
Specimens examined. Japan, Tokyo, from soil, 1962, S. Udagawa (CBS
415.64 = NBRC 7554). – USA, Maine, Kittery Point, from a wasp’s nest,
1961, R. Thaxter (neotype designated here CBS H-14440, MBT198046)
culture ex-neotype CBS 196.61 = MUCL 9058.
Notes — Microascus longirostris has been reported from
many sources, mostly from dung of several mammals, soil,
wood, seeds, air, as well from clinical samples in South and
North America, Europe and Australia (Barron et al. 1961). The
protologue of this species was made on the basis of ascomata
on the natural substrata only (dog dung and rotten wood) (Zukal
1885, Barron et al. 1961). No ex-type strain or holotype material of this species was available. Microascus longirostris is the
type of Microascus and, in order to stabilize the nomenclature,
a neotype is here designated. Although none of the cultures
studied here have the same geographical origin or host as the
original specimen, the morphological characteristics of the two
strains studied agree with the fungus described by Zukal in its
original publication (Zukal 1885). The neotype culture selected
here also corresponds with the modern descriptions of M. lon
girostris based on cultural characteristics given by Barron et al.
(1961), Morton & Smith (1963) and von Arx et al. (1988), being
also part of the material revised and considered as authentic
by those authors.
Microascus macrosporus (G.F. Orr) Sandoval-Denis, Gené &
Guarro, comb. & stat. nov. — MycoBank MB809212
Basionym. Microascus trigonosporus C.W. Emmons & B.O. Dodge var.
macrosporus G.F. Orr, Canad. J. Bot. 39: 1617. 1961.
Specimen examined. USA, California, from soil, 1971, G.F. Orr (CBS
662.71 = UAMH 9336).
Notes — This species was originally described from desert
soil as a variety of M. trigonosporus. However, while M. macro-
20
Persoonia – Volume 36, 2016
Fig. 9 Microascus restrictus CBS 138277. a, b. Colonies on OA and PCA, respectively, after 21 d at 25 °C; c, f – h. conidiophores, annellides and conidia;
d, e. solitary conidia. — Scale bars: c, d = 10 µm; all others = 5 µm.
M. Sandoval-Denis et al.: Phylogeny of Microascus and Scopulariopsis
sporus has ascospores measuring 5–6.5 × 5.5–7.5 µm, those of
M. trigonosporus are distinctly smaller (3 – 5 × 3 – 4 µm). Micro
ascus pyramidus is another phylogenetically closely related
and morphologically similar species. However, its ascospores
have distinctly attenuated ends and its conidia are 4.5–5.5 ×
3–4 µm. Microascus macrosporus produces ascospores with
rounded ends and larger conidia (5 –7 × 4 – 5 µm).
Microascus murinus (Samson & Klopotek) Sandoval-Denis,
Gené & Guarro, comb. nov. — MycoBank MB809218
Basionym. Scopulariopsis murina Samson & Klopotek, Arch. Mikrobiol.
85: 175. 1972.
Specimen examined. Germany, Giessen, from composed municipal waste,
1970, A. von Klopotek (ex-type culture CBS 830.70 = IHEM 18567).
Notes — This species was originally isolated from domestic
waste in Germany. Although M. murinus shares morphological features with M. chartarus, M. croci, M. paisii, M. restrictus
and M. verrucosus, it can be differentiated by having smaller
cylindrical conidia, measuring 4 – 6 × 1.5 – 2 µm and slightly
larger annellides, measuring 6.5 –11 × 1.5 – 2.5 µm.
Microascus paisii (Pollacci) Sandoval-Denis, Gené & Guarro,
comb. nov. — MycoBank MB809213
Basionym. Torula paisii Pollacci (as ‘pais’), Atti Ist. Bot. Univ. Pavia, ser.
2, 18: 130. 1921.
≡ Phaeoscopulariopsis paisii (Pollacci) M. Ota, Jap. J. Dermatol. Urol.
28: 5. 1928. nom. inval. (Seifert et al. 2011).
≡ Scopulariopsis paisii (Pollacci) Nannf., Repertorio sistematico dei miceti
dell’uomo e degli animali 4: 259. 1934.
= Scopulariopsis sphaerospora Zach, Oesterr. Bot. Z. 83: 180. 1934.
= Scopulariopsis brumptii Salv.-Duval, Thèse Fac. Pharm. Paris. 23: 58.
1935.
= Scopulariopsis versicolor Salv.-Duval, Thèse Fac. Pharm. Paris. 23:
63. 1935.
= Masoniella grisea (G. Sm.) G. Sm., Trans. Brit. Mycol. Soc. 35: 237.
1952.
≡ Masonia grisea G. Sm., Trans. Brit. Mycol. Soc. 35: 149. 1952, nom.
illeg.
= Scopulariopsis melanospora Udagawa, J. Agric. Sci. (Tokyo) 5: 18.
1959.
Specimens examined. Austria, from unknown substrate, 1934, F. Zach
(S. sphaerospora ex-type culture MUCL 9045 = CBS 402.34). – Germany,
Schleswig-Holstein, Kiel, Kitzeberg, from soil on a Triticum sativum field,
1966, W. Gams (MUCL 8989 = CBS 896.68); Schleswig-Holstein, Kiel,
from soil, 1966, W. Gams (MUCL 8990); from soil on a wheat field, 1966,
W. Gams (MUCL 8993 = CBS 897.68). – Italy, from human, 1927, G. Pol
lacci (T. paisii ex-type culture MUCL 7915 = CBS 213.27). – UK, isolated
as a culture contaminant, 1946, G. Smith (M. grisea ex-type culture MUCL
9003 = CBS 295.52). – USA, from milled Oriza sativa, 1955, S. Udagawa (S.
melanospora ex-type culture MUCL 9040 = CBS 272.60); from bronchoalveolar lavage fluid, 2007, D.A. Sutton (UTHSC 07-639 = FMR 12263); from
bronchoalveolar lavage fluid, 2008, D.A. Sutton (UTHSC 08-1734 = FMR
12248); from sputum, 2009, D.A. Sutton (UTHSC 09- 457 = FMR 12241);
from bronchoalveolar lavage fluid, 2009, D.A. Sutton (UTHSC 09-482 = FMR
12240); from sputum, 2009, D.A. Sutton (UTHSC 09-2391 = FMR 12229);
from bronchoalveolar lavage fluid, 2010, D.A. Sutton (UTHSC 10-2920 = FMR
12215); from sputum, 2011, D.A. Sutton (UTHSC 11-708 = FMR 12210).
Notes — Microascus paisii has had a confusing nomencla
tural history. As Scopulariopsis paisii, it was erroneously con
sidered the asexual morph of M. desmosporus by Morton &
Smith (1963). We have also observed discrepancies concerning T. paisii among fungal databases. In MycoBank, T. paisii is
considered as the asexual morph of M. cirrosus whereas Index
Fungorum lists T. paisii as a synonym of Scytalidium thermo
philum. Our phylogenetic analysis showed that the ex-type of
T. paisii (MUCL 7915) belongs to the Microascus lineage. Within
this lineage, it belongs to a well-supported subclade together
with the ex-type strains of Masoniella grisea, S. melanospora
and S. sphaerospora and several reference strains of S. brumptii.
21
This subclade might represent the rarely opportunist species
S. brumptii. However, since there is no type material of S. brumptii
available, and T. paisii being the oldest type strain included
in this subclade, the latter name has preference according to
the nomenclatural principle that the correct name is the oldest
legitimate one (McNeill et al. 2012). Therefore, according to our
data the new combination Microascus paisii should be adopted.
Regarding data pertaining to S. brumptii, M. paisii has a worldwide distribution, being isolated from multiple substrates, including air, decaying wood or soil and is an opportunistic pathogen
of human and warm-blooded animals (Morton & Smith 1963,
de Hoog et al. 2011, Sandoval-Denis et al. 2013). This species
morphologically resembles M. chartarus and M. croci, but it can
be differentiated by its dark grey or black colonies and its ability
to grow and sporulate well at 37 °C.
Microascus pyramidus G.L. Barron & J.C. Gilman, Canad.
J. Bot. 39: 1618. 1961
Specimen examined. USA, from desert soil, 1957, G.L. Barron (ex-type
culture CBS 212.65).
Notes — This species was originally isolated from desert
soil in North America (Barron et al. 1961). Morphologically, it
is similar to other Microascus species producing triangular ascospores as M. alveolaris, M. campaniformis, M. macrosporus
and M. trigonosporus. However, ascospores of M. pyramidus
are wider (5–6.5 × 5.5–7 µm), have attenuated ends and often acquire a nearly square shape (von Arx et al. 1988). The
asexual morph of M. pyramidus is morphologically similar to
those of M. macrosporus and M. campaniformis. Microascus
macrosporus produces globose to ovoid conidia measuring 5–7
× 4–5 µm, while those of M. pyramidus are markedly narrower
measuring 4.5–5.5 × 3–4 µm, and those of M. campaniformis
are subglobose to broadly ellipsoidal measuring 4–5 × 2.5–3.5
µm.
Microascus restrictus Sandoval-Denis, Gené & Deanna A.
Sutton, sp. nov. — MycoBank MB809420, Fig. 9
Etymology. From the Latin restringere-, restrict, referring to the restricted
growth of the colony.
Colonies on OA at 25 °C growing rather slowly, attaining 23–25
mm diam in 14 d, flat, downy, olive grey (3F2) to brown-grey
(5F2), with an irregular margin; reverse brown-grey (5F2). On
PCA at 25 °C growing restrictedly, attaining 3 – 5 mm diam
after 14 d, membranous, lobulate, with an irregular undulate
margin, olive brown (4E5) to brown (5E5); reverse brown-grey
(5E2). Vegetative hyphae septate, subhyaline becoming dark
brown with age, smooth- and thin-walled, 1.5 – 3 µm wide.
Conidiophores absent or as a basal single cell of 4–6 × 3–5
µm, bearing groups of 2–3 annellides, or slightly branched up
to 20 µm long, subhyaline, smooth-walled. Annellides mostly
sessile borne single and laterally on vegetative hyphae, ampulliform, 7–19 × 2 – 4.5 µm, with a swollen base, tapering
abruptly to a cylindrical and darker annellated zone 1.5–2 µm
wide, subhyaline, becoming darker with age, smooth-walled.
Conidia globose to obovoidal, 4.5–6 × 4–5.5 µm, with truncate
base, dark brown, smooth or finely roughened, thick-walled,
arranged in short chains. Solitary conidia sometimes present,
borne laterally from vegetative hyphae, sessile or on short
stalks, globose or obovate, 5–5.5 × 4.5–5 µm, dark brown,
smooth- and thick-walled. Sexual morph not observed.
Cardinal temperature for growth — Optimum 25 – 30 °C,
maximum 40 °C, minimum 15 °C.
Specimen examined. USA, from human left hallux, 2009, D.A. Sutton
(holotype CBS H-21787, culture ex-type CBS 138277= UTHSC 09-2704 =
FMR 12227).
22
Persoonia – Volume 36, 2016
Fig. 10 Microascus verrucosus CBS 138278. a, b. Colonies on OA and PCA, respectively, after 21 d at 25 °C; c – g. conidiophores, annellides and conidia;
h, i. solitary conidia. — Scale bars: c, h = 10 µm; all others = 5 µm.
23
M. Sandoval-Denis et al.: Phylogeny of Microascus and Scopulariopsis
Notes — Microascus restrictus is morphologically very si
milar to M. verrucosus. However, while M. restrictus shows
larger smooth-walled annellides measuring 7–19 × 2 –4.5 µm,
smaller conidia (4.5–6 × 4–5.5 µm) and is able to grow at 40 °C,
M. verrucosus has annellides measuring 8 –10 × 1– 3 µm, typically warted when mature, larger conidia (5–7 × 4.5–6 µm) and
is unable to growth at 40 °C.
broadly ellipsoidal, 5–6 × 4–5 µm, dark brown, smooth- and
thick-walled. Chlamydospores not observed. Sexual morph not
observed.
Cardinal temperature for growth — Optimum 25 – 30 °C,
maximum 35 °C, minimum 15 °C.
Microascus senegalensis Arx, Persoonia 8: 194. 1975
Notes — Microascus verrucosus can be differentiated from
M. restrictus, its closest morphological relative, by its sparsely
warted annellides and its inability to grow at 40 °C. Microascus
verrucosus is phylogenetically close to M. murinus; however,
this latter species has cylindrical conidia with pointed apices.
Specimen examined. Senegal, Joel, from mangrove soil, J.A. von Arx
(ex-type culture IHEM 18561 = CBS 277.74).
Notes — This species has been reported from soil, seeds
and plant debris as well as from human skin, in Africa, India
and North America (von Arx et al. 1988). The most remarkable
features of M. senegalensis are the presence of large reniform
ascospores (7–9 × 2–3 µm) with a single and often protuberant
germ pore (von Arx et al. 1988, Guarro et al. 2012).
Microascus trigonosporus C.W. Emmons & B.O. Dodge, Mycologia 23: 317. 1931
≡ Scopulariopsis trigonospora C.W. Emmons & B.O. Dodge, Mycologia
23: 317. 1931.
?= Microascus trigonosporus C.W. Emmons & B.O. Dodge var. terreus
Kamyschko, Novosti Sist. Nizsh. Rast. 76: 175. 1966.
?= Microascus trigonosporus C.W. Emmons & B.O. Dodge var. macro
perithecia Sage, Steiman, Seigle-Mur. & Guiraud, Mycotaxon 55: 194. 1995,
nom inval. Art. 40.5 (Melbourne).
Specimens examined. Japan, Burma, from milled rice, 1961, S. Udagawa
(MUCL 9061 = CBS 199.61). – UK, from mushroom bed, 1935, W.M. Ware
(MUCL 9841 = CBS 262.35). – USA, from unknown substrate, 1931, C.W.
Emmons (M. trigonosporus var. trigonosporus ex-type culture CBS 218.31).
Notes — This is a cosmopolitan species, commonly reported
from soil, seeds and dung (Barron et al. 1961). It is also considered as a human pathogen that has been associated with
pneumonia in an immunocompromised patient (Mohammedi et
al. 2004) and endocarditis (Wang et al. 2011). Among the species
producing triangular-shaped ascospores (M. alveolaris, M. cam
paniformis, M. macrosporus and M. pyramidus), M. trigonosporus
produces the smaller ones, measuring 3–5 × 3–4 µm.
Microascus verrucosus Sandoval-Denis, Gené & Cano, sp.
nov. — MycoBank MB809421; Fig. 10
Etymology. From the Latin verruca-, wart, referring to the warted ornamentation of the annellides.
Colonies on OA at 25 °C growing slowly, attaining 19 –22 mm
diam in 14 d, flat, finely granular, olive grey (2 – 3F2), with an
immersed and slightly undulated margin; reverse olive grey (1–
3F2). On PCA at 25 °C growing restrictedly, attaining 1–5 mm
diam in 14 d, adherent, membranous or slightly downy, hemispherical, cerebriform, with lobulated margin, olive (2E3/2E4);
reverse olive (2E2) to olive grey (2E3). Vegetative hyphae septate, subhyaline becoming dark brown with age, smooth- to
rough-walled, thin-walled, 1.5 – 2.5 µm wide. Conidiophores
absent or as a basal single cell of 4 – 5 × 2.5 – 4 µm, bearing
groups of 2 – 3 annellides, rarely slightly branched up to 25 µm
long. Annellides mostly sessile and borne directly on vegetative
hyphae, lageniform, 8 –10 × 1– 3 µm, constricted at the basal
septum, followed by a slightly swollen portion and tapering
to a more or less cylindrical annellated zone 1–1.5 µm wide,
usually sparsely warted. Conidia globose to subglobose, 5–7
× 4.5– 6 µm, often with an inconspicuous truncate base, dark
brown, smooth or finely roughened, thick-walled, arranged in
short chains. Solitary conidia sometimes present, borne laterally
from vegetative hyphae, sessile or on short stalks, globose or
Specimen examined. USA, from bronchoalveolar lavage fluid, 2010, D.A.
Sutton (holotype CBS H-21788, culture ex-type CBS 138278 = UTHSC 102601 = FMR 12219).
Pithoascus Arx, Proc. Kon. Ned. Akad. Wetensch. 76: 295.
1973
Type species. Pithoascus nidicola (Massee & E.S. Salmon) Arx.
Colonies restricted, white, becoming grey or darkening due to
the production of ascomata; usually with scarce aerial mycelium.
Ascomata perithecial, immersed or somewhat superficial, gregarious, often grouped on dense crusts, globose, glabrous, often
with an inconspicuous ostiolar opening or with a short cylindrical
ostiolar neck; peridium black, composed of thick-walled, slightly
flattened cells, textura angularis. Asci unitunicate, 8-spored,
broadly clavate or barrel-shaped, evanescent. Ascospores
1-celled, asymmetrical, navicular, fusiform or falcate, yellow,
straw- or honey-coloured, dextrinoid when young, without germ
pores. Asexual morph present in some species. Conidiogenous
cells annellidic, borne singly and laterally on the vegetative
hyphae, short, ampulliform, hyaline, smooth-walled. Conidia
1-celled, globose to pyriform, with a truncate base, smoothand thin-walled, solitary.
Pithoascus ater (Zach) Sandoval-Denis, Cano & Guarro,
comb. nov. — MycoBank MB809214
Basionym. Scopulariopsis atra Zach, Oesterr. Bot. Z. 83: 184. 1934.
Specimen examined. From human nail, 1934, F. Zach (ex-type culture
IHEM 18608 = CBS 400.34).
Notes — A single strain of this species is available. It was
isolated from a human nail, but its pathogenic role was not
clearly established (Zach 1934). Pithoascus ater is the only
species of the genus for which a sexual morph is unknown and
by contrast shows abundant conidial production. However, the
ex-type strain of P. ater shows similar morphological characteristics to the known asexual morphs of Pithoascus species, such
as P. stoveri and P. intermedius. The main distinctive feature
of P. ater is the abundant production of solitary, globose and
smooth-walled pale brown conidia measuring 4–9 × 4.5–8.5
µm. In contrast, conidia of P. stoveri and P. intermedius are
rarely seen in culture and, when present, are hyaline, obovate
to pyriform (5–8 × 3–4 µm) or globose to subglobose (4–8 ×
4.5–7.5 µm), respectively. Other species, i.e. P. nidicola and
P. exsertus produce only sexual morphs in culture.
Pithoascus exsertus (Skou) Arx, Persoonia 7: 373. 1973
Basionym. Microascus exsertus Skou, Antonie van Leeuwenhoek 39:
533. 1973.
Specimens examined. Denmark, Sjaelland, Bjerge Strand, from Osmia
rufa, 1975, J.P. Skou (CBS 583.75); Tastrup, Hojbakkegard, Experimental
Station, from Megachile willoughbiella, 1970, J.P. Skou (ex-type culture CBS
819.70).
Notes — This fungus is considered as an entomogenous
species, which has been isolated from a leaf-cutting bee (Mega
24
Persoonia – Volume 36, 2016
chile willughbiella) and from a Red Mason-bee (Osmia rufa),
both in northern Europe. Morphologically, P. exsertus can be
differentiated from the other species of the genus by its larger
ascomata (210 – 450 µm diam) and its long, falcate to nearly
cylindrical and yellow ascospores, 6.5 –12 × 1– 2.5 µm.
Pithoascus intermedius (C.W. Emmons & B.O. Dodge) Arx,
Proc. Kon. Ned. Akad. Wetensch. 76: 292. 1973
Basionym. Microascus intermedius C.W. Emmons & B.O. Dodge, Mycologia 23: 324. 1931.
Specimen examined. USA, North Carolina, Chadbourn, from decaying
root of Fragaria vesca, 1932, C.W. Emmons & B.O. Dodge (ex-type culture
CBS 217.32).
Notes — This species has been reported mainly from soil
in North America, Europe and Asia, and also as a potential
pathogenic species isolated from human hair and nails (von
Arx et al. 1988, Guarro et al. 2012). Pithoascus intermedius is
morphologically similar to P. nidicola and P. stoveri. However,
P. intermedius can be identified by its small, fusiform asco
spores, 5 – 6 × 2 – 2.5 µm.
Pithoascus nidicola (Massee & E.S. Salmon) Arx, Proc. Kon.
Ned. Akad. Wetensch. 76: 292. 1973
Basionym. Microascus nidicola Massee & E.S. Salmon, Ann. Bot., Lond.
15: 313. 1901.
Specimen examined. USA, Utah, from Dipodomys merriami, C.W. Em
mons (ex-epitype culture CBS 197.61).
Notes — Pithoascus nidicola was originally isolated from a
wasp’s nest in England and later from soil samples in North
America (Massee & Salmon 1901, Barron et al. 1961). The exepitype culture, however, was isolated from a kangaroo rat in the
USA (von Arx 1973b, Abbott et al. 2002). This species is similar
to P. stoveri; however, P. nidicola can be differentiated by having
larger ascomata (90–160 µm diam) with thicker walls (6–10 µm)
and navicular to nearly lunate straw coloured ascospores. In
contrast, P. stoveri produces ascomata measuring 50 –110 µm
diam, with a wall 4 –7 µm thick, and navicular, golden to brown
coloured ascospores (von Arx 1973b, Abbot et al. 2002, Guarro
et al. 2012). Although conidia had never been reported for
P. nidicola, we observed the development of a reduced asexual
morph on PCA forming globose to ampulliform hyaline conidia,
4–5 × 2.5–3.5 µm, borne on short conidiogenous cells (Fig. 2).
These asexual structures resemble those of P. intermedius, but
the conidia of the latter are globose to subglobose and larger
(4–8 × 4 –7.5 µm).
Pithoascus stoveri Arx, Persoonia 7: 373. 1973
≡ Microascus stoveri (Arx) S.P. Abbott, Mycologia 94: 368. 2002.
Specimen examined. USA, Ohio, from root of Beta vulgaris, W.L. White
(ex-type culture CBS 176.71).
Notes — This species was originally isolated from a root of
sugar beet in the USA. Pithoascus stoveri is morphologically
similar to P. nidicola; however, the former species forms an
asexual morph in culture, has a smaller ascomata (50–110
µm diam) and navicular golden yellow to brown ascospores.
Pithoascus nidicola produces ascomata 90–160 µm diam, and
navicular to nearly lunate straw-coloured ascospores.
Pseudoscopulariopsis Sandoval-Denis, Gené & Guarro, gen.
nov. — MycoBank MB809215
Type species. Pseudoscopulariopsis schumacheri (Curzi) SandovalDenis, Gené & Guarro.
Colonies restricted, greyish, dark olive grey to olivaceous black;
floccose with abundant submerged mycelium, often becoming
crustose and dark. Ascomata black, globose or ovate, glabrous,
with a short cylindrical ostiolar neck and a peridium of textura
epidermoidea. Asci unitunicate, 8-spored, ovoid, evanescent.
Ascospores 1-celled, asymmetrical, navicular to fusiform, subhyaline, pale yellow or brown, without germ pores. Conidio
genous cells short, annellidic, often with a swollen base, mostly
borne on a short and swollen supporting cell forming short
swollen conidiophores, rarely borne singly on aerial hyphae.
Conidia 1-celled, subglobose, obovate to short clavate, with truncate base and rounded apex, smooth- and thin-walled, pale
brown to brown-grey, arranged in short chains.
Pseudoscopulariopsis hibernica (A. Mangan) SandovalDenis, Gené & Cano, comb. nov. — MycoBank MB809216
Basionym. Scopulariopsis hibernica A. Mangan, Trans. Brit. Mycol. Soc.
48: 617. 1965.
Specimen examined. Ireland, from soil, A. Mangan (UAMH 2643 = ATCC
16690).
Notes — This is a species described from soil and only a
few isolates are available, all of them derived from the same
isolation source (Mangan 1965). The isolate studied here, al
though not the ex-type culture, was isolated and considered
authentic by the same authors (Mangan 1965) and matched in
all aspects with the protologue (Mangan 1965). Phylogenetically, P. hibernica clustered close to P. schumacheri, both species being characterised by short cylindrical annellides mostly
formed in small groups on short and swollen supporting cells,
commonly darkening with age. Pseudoscopulariopsis hibernica
can be differentiated mainly by its lack of a sexual morph, the
presence of shorter (9–15 × 3–5 µm) and darker annellides,
and its larger (5 –7 × 5–6 µm) subglobose conidia.
Pseudoscopulariopsis schumacheri (E.C. Hansen) SandovalDenis, Gené & Guarro, comb. nov. — MycoBank MB809549
Basionym. Sphaerella schumacheri E.C. Hansen, Vidensk. Meddel.
Dansk Naturhist. Foren. Kjøbenhavn: 16. 1876.
≡ Rosellinia schumacheri (E.C. Hansen) Sacc., Syll. Fung. 1: 276. 1882.
≡ Microascus schumacheri (E.C. Hansen) Curzi, Boll. Staz. Patol. Veg.
Roma, N.S. 23: 8. 1931.
≡ Pithoascus schumacheri (E.C. Hansen) Arx, Proc. Kon. Ned. Akad.
Wetensch. 76: 292. 1973.
= Melanospora stysanophora Mattir., Nuovo Giorn. Bot. Ital. 18: 121.
1886.
≡ Microascus stysanophorus (Mattir.) Curzi, Boll. Staz. Patol. Veg. Roma,
N.S. 10: 391. 1930.
≡ Microascus stysanophorus (Mattir.) G.L. Barron, Cain & J.C. Gilman,
Canad. J. Bot. 39: 1621. 1961.
≡ Pithoascus stysanophorus (Mattir.) Valmaseda, A.T. Martínez & Barrasa, Canad. J. Bot. 65: 1805. 1987.
Specimen examined. Spain, Puerto de la Quesera, from soil, 1986, A.T.
Martínez (neotype designated here MA-Fungi 16319, MBT178643), culture
ex-neotype CBS 435.86.
Notes — This species was originally described from dung of
rodents, in Denmark, but no ex-type strain was preserved nor
herbarium material listed in the protologue. The modern descriptions of the species by Barron et al. (1961), Valmaseda et al.
(1986), von Arx et al. (1988) and Guarro et al. (2012) are based
on the same isolate studied here; however, a type specimen
has never been designated. We agree with the observations of
all these authors in that morphological features of CBS 435.86
match with those of the protologue of the species (Hansen
1876). Therefore, due to the scant live material available and
the inexistence of ex-type cultures, we have selected this strain
as neotype in order to fix the application of the name. Although
neither the substrate nor the geographic origin correspond to
M. Sandoval-Denis et al.: Phylogeny of Microascus and Scopulariopsis
that indicated in the protologue of the species, this strain clearly
represents P. schumacheri according to concepts maintained
by subsequent authors (Valmaseda et al. 1986, von Arx 1988,
Guarro et al. 2012).
Morphologically, P. schumacheri resembles Pithoascus species
by its navicular to fusiform ascospores lacking germ pores, thus
being included in that genus by von Arx (1973a). Nevertheless,
P. schumacheri can be differentiated by its restricted growth
and the textura epidermoidea of the ascoma wall. Phylogenetically, P. schumacheri is related to P. hibernica; however, the
former can be differentiated by the presence of ascomata and
the production of obovate to short-clavate conidia, measuring
4.5–6 × 2.5–4 µm, on mostly hyaline annellides which measure
3.5–22.5 × 1.5 – 2.5 µm.
Scopulariopsis Bainier, Bull. Soc. Mycol. France 23: 98. 1907
?= Acaulium Sopp, Skr. Vidensk.-Selsk. Christiana, Math.-Naturvidensk.
Kl. I, 11: 42. 1912.
= Phaeoscopulariopsis M. Ota, Jap. J. Dermatol. Urol. 28: 405. 1928,
nom. inval. Art 34 (Seifert et al. 2011).
Type species. Scopulariopsis brevicaulis (Sacc.) Bainier.
Colonies spreading fast, velvety, funiculose or granular, varying
from white and grey-white to several shades of buff, brown or
dark brown, but never in shades of green or black. Ascomata
perithecial, immersed or superficial, developing slowly, scattered; globose to subglobose or pyriform, glabrous, ostiolate,
papillate or with a cylindrical neck; peridium black, composed
of thick-walled, slightly flattened cells of textura angularis.
Asci unitunicate, 8-spored, subglobose, irregularly ovoidal or
ellipsoidal, evanescent. Ascospores 1-celled, asymmetrical,
short, broadly reniform or lunate, dextrinoid when young, with
or without an inconspicuous germ pore. Conidiogenous cells
annellidic, borne on branched penicillate conidiophores, occasionally singly on vegetative hyphae or in groups of 2–3
on short stalks, cylindrical, often with a slightly swollen base
followed by a cylindrical annellated portion that ends in a flat
and wide conidiogenous opening, hyaline, smooth- or roughwalled. Conidia 1-celled, hyaline, avellaneous or brown, globose
to ovate, with a rounded or pointed apex and a conspicuously
protuberant and truncate base, smooth- or rough- and thickwalled, arranged in long basipetal dry chains.
Scopulariopsis asperula (Sacc.) S. Hughes, Canad. J. Bot.
36: 803. 1958
Basionym. Torula asperula Sacc., Michelia 2: 560. 1882.
= Acaulium nigrum Sopp, Skr. Vidensk.-Selsk. Christiana, Math.-Natur
vidensk. Kl. I 11: 47. 1912.
≡ Penicillium nigrum (Sopp) Biourge, Cellule 33: 1043. 1923.
≡ Microascus niger (Sopp) Curzi, Boll. Staz. Patol. Veg. Roma, N.S. 11:
8. 1931.
= Scopulariopsis repens Bainier, Bull. Soc. Mycol. France 23: 125. 1907.
≡ Penicillium repens (Bainier) Biourge, Cellule 33: 225. 1923.
= Monilia arnoldii L. Mangin & Pat., Bull. Soc. Mycol. France 24: 164.
1908.
≡ Scopulariopsis arnoldii (L. Mangin & Pat.) Vuill., Bull. Soc. Mycol.
France 27: 148. 1911.
= Scopulariopsis ivorensis H. Boucher, Bull. Soc. Pathol. Exot. 11: 312.
1918.
= Torula bestae Pollacci, Rivista Biol. 4: 317. 1922.
≡ Phaeoscopulariopsis bestae (Pollacci) M. Ota, Jap. J. Dermatol. Urol.
28: 405. 1928, nom. inval. (Seifert et al. 2011).
≡ Scopulariopsis bestae (Pollacci) Nannf., Repertorio sistematico dei
miceti dell’uomo e degli animale 4: 254. 1934.
= Scopulariopsis fusca Zach, Oesterr. Bot. Z. 83: 174. 1934.
= Acaulium nigrum Sopp var. glabrum Salv.-Duval, Thèse Fac. Pharm.
Paris. 23: 55. 1935.
= Scopulariopsis roseola N. Inagaki, Trans. Mycol. Soc. Japan 4: 1. 1962.
25
Specimens examined. Austria, from a carcass of rabbit, 1934, F. Zach
(Scopulariopsis fusca ex-type culture MUCL 9032 = CBS 401.34). – Canada,
Alberta, Girouxville, from indoor air ex RCS strip, Apis mellifera overwintering facility, Jan. 1994, S.P. Abbott (MUCL 40729 = UAMH 7879); Alberta, 10
km south of Leduc, from dung of Mephitis mephitis, June 1997, S.P. Abbott
(MUCL 40746 = UAMH 9029). – Germany, from compost soil, 1958, K.H.
Domsch (CBS 853.68). – Italy, from human, 1938, G. Pollacci (Torula bestae
ex-type culture MUCL 9012 = CBS 289.38). – USA, from toenail, 2010, D.A.
Sutton (UTHSC 10-3405 = FMR 12212).
Notes — This species has been mostly recovered from en
vironmental samples such as soil, air, mouldy indoor environments, food such as cheese and butter, as well as from human
clinical specimens, mainly skin and nails (Ropars et al. 2012,
Sandoval-Denis et al. 2013).
Torula bestae was considered by Morton & Smith (1963) to
be conspecific with S. koningii. However, although both species show smooth conidia, T. bestae typically exhibits darker
fuscous-black colonies and conidia. Later, Abbott & Sigler
(2001), using mating experiments, established that S. arnoldii,
S. asperula, S. bestae, S. fusca and S. roseola were all synonyms of the heterothallic species Microascus niger. The same
authors also selected neotype and epitype cultures for M. niger
(UAMH 9489) and S. asperula (UAMH 9037), respectively,
which unfortunately were not available for our study. However,
all the reference strains studied here were genetically related
with the type cultures of S. fusca and S. bestae, both species
regarded as synonyms of S. asperula. Recently, Ropars et al.
(2012) confirmed the synonymy of these species using a multilocus analysis based on D1/D2, TUB and EF-1α sequences
which results are confirmed by our phylogenetic analysis.
Morphologically, S. asperula is close to S. brevicaulis and
S. flava; however, S. asperula can be differentiated by having
dark brown to fuscous or violaceus colonies, and globose to
ovate, coarsely verrucose or smooth walled, fuscous to sepia
coloured conidia, mostly with a pointed apex and measuring
5–8 × 4–6.5 µm. In contrast, S. brevicaulis shows tan colonies,
globose and verrucose pale brown conidia, 6–9 × 5.5–9 µm,
while S. flava exhibits white colonies and obovoidal, verrucose
and hyaline conidia, 6 –9.5 × 5–8.5 µm.
Scopulariopsis brevicaulis (Sacc.) Bainier, Bull. Soc. Mycol.
France 23: 99. 1907
Basionym. Penicillium brevicaule Sacc., Fungi Ital. 893: 1881.
= Monilia penicillioides Delacr., Bull. Soc. Mycol. France 13: 114. 1897.
≡ Penicillium penicillioides (Delacr.) Vuill., Bull. Soc. Mycol. France 27:
75. 1911.
≡ Scopulariopsis penicillioides (Delacr.) Smith & Ramsb., Trans. Brit.
Mycol. Soc. 5: 164. 1915.
= Monilia koningii Oudem., Arch. Neerl. Sci., sér. 2: 287. 1902.
≡ Scopulariopsis koningii (Oudem.) Vuill., Bull. Soc. Mycol. France 27:
143. 1911.
= Penicillium coccophilum Sacc., Ann. Mycol. Berl. 5: 178. 1907.
= Scopulariopsis rufulus Bainier, Bull. Soc. Mycol. France 23: 105. 1907.
≡ Penicillium rufulum (Bainier) Sacc., Syll. Fung. 22: 1275. 1913.
= Penicillium brevicaule Sacc. var. hominis Brumpt & Langeron in Brumpt,
E. Précis de parasitologie, Ed. 1: 838. 1910.
≡ Scopulariopsis brevicaulis (Sacc.) Bainier var. hominis (Brumpt &
Langeron) Brumpt & Langeron in Brumpt, E. Précis de parasitologie, Ed 2:
902. 1913.
= Scopulariopsis hominis (Brumpt & Langeron) Sartory, Champ. Parasit.
Fasc. 8: 612. 1922.
= Acaulium insectivorum Sopp, Skr. Vidensk.-Selsk. Christiana, Math.Naturvidensk. Kl. I, 11: 60. 1912.
≡ Penicillium insectivorum (Sopp) Biourge, Cellule 33: 103. 1923.
≡ Scopulariopsis insectivora (Sopp) Thom, The Penicillia: 532. 1930.
= Acaulium anomalum Sopp, Skr. Vidensk.-Selsk. Christiana, Math.Naturvidensk. Kl. I, 11: 65. 1912.
= Penicillium brevicaule Sacc.var. intermedium Cagnetto, Sperimentale
67, Suppl. to Fasc. 4: 210. 1913.
= Sporotrichum stercorarium Ehrenb., Jahrb. Gewächsk. 1: 178. 1818.
≡ Scopulariopsis stercoraria (Ehrenb.) S. Hughes, Canad. J. Bot. 36:
803. 1958.
26
Persoonia – Volume 36, 2016
Fig. 11 Scopulariopsis cordiae CBS 138129. a, b. Colonies on OA and PCA, respectively, after 21 d at 25 °C; c. ascoma; d. peridium; e, f. asci and ascospores;
g – i. conidiophores, annellides and conidia; j, k. conidial chains. — Scale bars: c = 50 µm; all others = 5 µm.
M. Sandoval-Denis et al.: Phylogeny of Microascus and Scopulariopsis
= Scopulariopsis alboflavescens Zach, Oesterr. Bot. Z. 83: 177. 1934.
= Microascus brevicaulis S.P. Abbott. Mycologia 90: 298. 1998.
Specimens examined. Austria, from human diseased skin, 1934, F. Zach
(S. alboflavescens ex-type culture CBS 339.34). – Belgium, Heverlee, from
soil, J. Meyer (as S. stercoraria MUCL 14213). – Canada, Alberta, from indoor
air, March 1994, S.P. Abbott (M. brevicaulis ex-type culture UAMH 7770 =
MUCL 40726). – The Netherlands, Wageningen, from pupa of Pteronus pini,
1935, J. Rozsypal (as S. insectivora CBS 335.35 = MUCL 9035). – Unknown
geographical origin, Elephant, 1951, I.M. Scott (as S. koningii CBS 208.61).
– USA, from hair, 2006, D.A. Sutton (UTHSC 06-277 = FMR 12273); from
toenail, 2006, D.A. Sutton (UTHSC 06-619 = FMR 12271); from toenail,
2007, D.A. Sutton (UTHSC 07-1812 = FMR 12257); from human spine, 2007,
D.A. Sutton (UTHSC 07-1888 = FMR 12255); from maxillary sinus, 2008,
D.A. Sutton (UTHSC 08-1920 = FMR 12247); from toe, 2009, D.A. Sutton
(UTHSC 09-1092 = FMR 12236); from sputum, 2009, D.A. Sutton (UTHSC
09-1373 = FMR 12233); from sputum, 2011, D.A. Sutton (UTHSC 11-427 =
FMR 12211); from lung mass, 2011, D.A. Sutton (UTHSC 11-1240 = FMR
12206); from bronchoalveolar lavage fluid, 2011, D.A. Sutton (UTHSC 111563 = FMR 12204).
Notes — This is a species with a worldwide distribution. It
has been isolated from a wide range of substrates and locations and also recognised as an important human opportunistic
pathogen (de Hoog et al. 2011, Sandoval-Denis et al. 2013). The
history of this taxon was reviewed by Morton & Smith (1963).
These authors synonymised S. insectivora and S. brevicaulis,
but regarded S. stercoraria and S. koningii as different species
since the latter two taxa exhibited smooth conidia. Later, Abbott
& Sigler (2001) based on mating studies demonstrated that
S. brevicaulis and S. koningii were conspecific. The present
data confirmed the synonymy of the four mentioned species. In
contrast, our results showed that the ex-type strain of S. albofla
vescens (CBS 339.34), a species currently considered a synonym of S. candida, is conspecific with S. brevicaulis. Scopulari
opsis alboflavescens was described as having smooth conidia
and colonies at first white becoming pale yellowish, features that
distinguished it from S. brevicaulis (Zach 1934). However, our
morphological study of the ex-type strain of S. alboflavescens
revealed that despite the fact that it forms whitish to pale yellow colonies, it also produces some finely roughened conidia.
Ropars et al. (2012) already suggested a relationship between
the two species using a phylogenetic analysis based in LSU,
TUB and EF-1α sequences, showing that the ex-type strain of
S. alboflavescens nested in a clade closely related to S. brevicaulis and far from the S. candida clade. However, those
authors concluded that S. candida was a polyphyletic species.
Abbott & Sigler (2001) reported the formation of fertile ascomata
when crossing the ex-type strain of S. alboflavescens (CBS
339.34) with several strains of S. candida and the ex-types of
S. candida (MUCL 40743) and Nephrospora manginii (basionym of M. manginii CBS 170.27), thus supporting the synonymy
of S. alboflavescens and S. candida already proposed by
Morton & Smith (1963). However, considering that strains of
M. manginii (CBS 170.27 and MUCL 12598), the ex-epitype of
S. candida (MUCL 40743) and S. alboflavescens (CBS 399.34)
were all self-fertile in our study, the phylogenetic results and the
placement of S. alboflavescens as a synonym of S. brevicaulis,
including strains showing smooth conidia and whitish to pale
yellow colonies, is supported.
27
= Scopulariopsis brevicaulis (Sacc.) Bainier var. glabra (Thom) Thom
sensu Raper & Thom, Manual of the Penicillia: 699. 1949.
= Chrysosporium keratinophilum (Frey) Carmich. var. denticola C. Moreau,
Mycopathol. Mycol. Appl. 37: 37. 1969.
≡ Basipetospora denticola (C. Moreau) C. Moreau, Bull. Soc. Mycol.
France 87: 43, 1971.
Specimens examined. Canada, British Columbia, Chilliwak, from indoor
air, March 1997, S.P. Abbott (S. candida ex-type culture MUCL 40743 =
UAMH 9004). – France, from unknown origin, 1927, L. Mangin (N. manginii
ex-type culture CBS 170.27); from unknown substrate, 1927, L. Mangin (as
S. candelabrum MUCL 9026 = CBS 205.27); from cheese ‘tome de Savoie’,
Aug. 1998, C. Decock (as M. manginii MUCL 41467). – Unknown origin, 1966
(as S. alboflavescens MUCL 9007). – USA, from sputum, 2009, D.A. Sutton
(UTHSC 09-2576 = FMR 12228); from scalp, 2009, D.A. Sutton (UTHSC
09-3241 = FMR 12226).
Notes — This species has been reported from environmental
samples (air, dust and soil) generally from the Northern Hemisphere, especially in Europe and North America; and also from
clinical samples, mainly from superficial tissue of humans and
animals (de Hoog et al. 2011). It is morphologically close to
S. brevicaulis, S. asperula and S. flava. However, S. candida has
subglobose to broadly ovate, hyaline, smooth-walled conidia
and white colonies. In contrast, S. brevicaulis and S. asperula
produce tan or fuscous brown colonies, respectively, while
S. flava produces white colonies and obovoidal rough-walled
conidia. When the sexual morph is present, it is characterised
by globose perithecia, 100–170 µm diam, and reniform to heartshaped ascospores which are somewhat wider (4–6 × 5–6 µm)
than those of its closest relatives such as S. brevicaulis (5–6
× 3.5–4.5 µm), S. cordiae (4.5–5.5 × 3.5–4 µm) and S. soppii
(6–7 × 2.5–3 µm).
Scopulariopsis cordiae Sandoval-Denis, Gené & Cano, sp.
nov. — MycoBank MB809217, Fig. 11
Etymology. From the Latin cordiae-, heart, referring to the heart-shaped
ascospores.
Colonies on OA and PCA at 25 °C attaining 35–36 and 48–50
mm diam, respectively, after 14 d, flat, with scarce aerial mycelium, white to light grey (4B1) and granular due to the abundant
production of ascomata, regular margin with abundant submerged mycelium; reverse whitish. Vegetative hyphae septate,
hyaline, smooth- and thin-walled, 1.5–3.5 µm wide. Ascomata
abundant, superficial or immersed, globose or subglobose,
100–150 µm diam, with a long cylindrical ostiolar neck up to
390 µm, black, glabrous; peridium with a textura angularis.
Asci irregularly ellipsoidal, 9–15.5 × 7.5–10 µm. Ascospores
broadly lunate to reniform, 4.5–5.5 × 3.5–4 µm, straw coloured,
bright yellow in mass, with a single and inconspicuous germ
pore. Conidiophores absent. Annellides sessile, borne single
and laterally on vegetative hyphae, hyaline, smooth and thinwalled, cylindrical, 8–15 × 1.5–3.5 µm, tapering gradually to
a cylindrical annellated zone 1–1.5 µm wide. Conidia broadly
ellipsoidal to obovoidal, 2.5–6 × 2–5 µm, with truncate base,
hyaline, white in mass, smooth- and thick-walled, arranged in
chains. Chlamydospores and solitary conidia not observed.
Cardinal temperature for growth — Optimum 25 – 30 °C,
maximum 40 °C, minimum 15 °C.
Scopulariopsis candida (Guég.) Vuill., Bull. Soc. Mycol.
France 27: 143. 1911
Specimens examined. USA, from a human J.P Drain, 2005, D.A. Sutton
(UTHSC 05-3453 = FMR 12349); from human finger, 2009, D.A. Sutton
(holotype CBS H-21789, culture ex-type CBS 138129 = UTHSC 09-866 =
FMR 12338).
Basionym. Monilia candida Guég., Bull. Soc. Mycol. France 15: 271.
1899.
= Nephrospora manginii Loubière, Compt. Rend. Hebd. Séances Acad.
Sci. 177: 209. 1923.
≡ Microascus manginii (Loubière) Curzi, Boll. Staz. Patol. Veg. Roma 2:
60. 1931.
= Monilia candida auct. non Pers.: Loubière in Compt. Rend. Hebd.
Séances Acad. Sci. 177: 209. 1923.
Notes — Scopulariopsis cordiae morphologically resembles
the sexual morph of S. candida in the shape and size of the
ascomata, asci and ascospores. Scopulariopsis cordiae can
be differentiated by its faster growth rate, the sparkled appearance of the colonies, the presence of long cylindrical necks in
numerous submerged ascomata, and the slightly reduced size
and shape of its ascospores and conidia.
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Persoonia – Volume 36, 2016
Scopulariopsis flava (Sopp) F.J. Morton & G. Sm., Mycol.
Pap. 86: 43. 1963
Basionym. Acaulium flavum Sopp, Skr. Vidensk.-Selsk. Christiana, Math.Naturvidensk. Kl. I 11: 53. 1912.
= Penicillium brevicaule Sacc. var. album Thom, Bull. U.S. Bur. Anim.
Ind. 118: 47. 1910.
≡ Scopulariopsis brevicaulis (Sacc.) Bainier var. alba (Thom) Thom, The
Penicillia: 520. 1930.
= Scopulariopsis aurea Sartory, Champ. Parasit. Fasc. 9: 650. 1922.
= Scopulariopsis casei Loubière, Thèse Fac. Sci. Paris, Sér. 4: 62. 1924.
= Scopulariopsis grylli Sartory, Ann. Mycol., Berl., 30: 469. 1932.
Specimen examined. UK, from cheese, 1948, G. Smith (neotype designated here CBS H-21939, MBT198047) culture ex-neotype CBS 207.61 =
MUCL 9031).
Notes — This species is commonly isolated from cheese
and soil in Europe and North America (Ropars et al. 2012).
However, Sopp’s original description of A. flavum is based on
an isolate obtained from an insect larva. There are also reports
of this species as human opportunistic pathogen (de Hoog et al.
2011). Scopulariopsis flava is morphologically close to S. brevi
caulis. However, while S. brevicaulis produces tan, powdery to
granular colonies, and globose to ovoid conidia with rounded
or pointed apices, becoming verrucose and pale brown when
mature, S. flava produces white floccose to fasciculate colonies,
and hyaline globose to obovoidal conidia, with rounded apices
and a coarsely roughened wall.
We only could study a single strain of S. flava (MUCL 9031),
which is morphologically identical to the asexual morph of
A. flavum and fits with the modern concept of S. flava by Morton
& Smith (1963). Abbott et al. (2002) considered this strain a
probable poorly pigmented variant of S. brevicaulis. However,
our analyses show that MUCL 9031 is phylogenetically and
morphologically distant from S. brevicaulis. Considering that
Morton & Smith (1963) regarded MUCL 9031 as an authentic
strain of S. brevicaulis var. alba, the epithet alba would take
priority over the younger one flava, however the former epithet
was already used in Scopulariopsis (S. alba, currently Dorato
myces albus according to Dominik & Majchrowicz (1970)). Thus
to avoid nomenclatural confusion we prefer to maintain the
epithet flava for the present species. Phylogenetically S. flava
is related to S. soppii, but the latter differs morphologically in
producing larger conidia (5.5 – 9 × 5 – 8 µm vs 6.5 –7 × 5.5–6.5
µm in S. flava), and falcate to lunate ascospores measuring 6–7
× 2.5–3 µm. It is noteworthy that a short description of a sexual
morph was included in the protologue of A. flavum having ‘ovalround’ ascospores measuring 6 –7 µm (Sopp 1912). However,
we were not able to induce the production of ascomata in the
above-mentioned strain and according to Abbott et al. (2002) no
sexual morph has been reported since the original description
of the species (Sopp 1912).
Scopulariopsis soppii S.P. Abbott, Mycologia 94: 364. 2002
≡ Microascus soppii S.P. Abbott, Mycologia 94: 364. 2002.
Specimen examined. Canada, Alberta, Elk Island National Park, from dry,
rotten wood of Populus tremuloides, T. Lumley (ex-type culture UAMH 9169).
Notes — This species has been isolated from decayed wood
and sandy loam (Abbott et al. 2002). It is phylogenetically and
morphologically close to S. flava from which it can be differentiated based on the size of the conidia and the size and shape
of its ascospores (see S. flava).
IDENTIFICATION KEYS
According to the morphological features, identification keys were
constructed for the different genera including all the phylo
genetic species recognised in this study.
Key to Microascus, Scopulariopsis and allied genera
1. Colonies white, tan or brown coloured; conidiogenous cells
cylindrical, hyaline or pale brown; conidia thick-walled with
a protruding flat base . . . . . . . . . . . . . . . . Scopulariopsis
1. Colonies grey-white, olive-green or black; conidiogenous cells
ampulliform or lageniform, subhyaline or brown-green;
conidia otherwise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Asexual morph absent; if present conidiophores simple,
short; ascospores without germ pores . . . . . . . . . . . . . . 3
2. Asexual morph always present, conidiophores often branched up to 80 µm long; ascospores with a germ pore . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Microascus
3. Ascomata peridium of textura angularis; asexual morph
when present forming short, hyaline and single annellides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pithoascus
3. Ascomata peridium of textura epidermoidea; asexual
morph usually abundant, forming long annellides from short
swollen conidiophores, darkening with time . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . Pseudoscopulariopsis
Key to Microascus species
1. Ascomata present in culture . . . . . . . . . . . . . . . . . . . . . . 2
1. Ascomata absent in culture . . . . . . . . . . . . . . . . . . . . . 14
2. Growth at 40 °C . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
2. No growth at 40 °C . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
3. Peridium with textura angularis . . . . . . . . . . . . . . . . . . . 4
3. Peridium with textura intricata . . . . . . . . . . . M. intricatus
4. Ascospores always triangular or quadrangular . . . . . . . . 5
4. Ascospores reniform to broadly lunate, rarely triangular . 8
5. Ascospores with rounded ends . . . . . . . . . . . . . . . . . . . . 6
5. Ascospores with attenuated (pointed) ends M. pyramidus
6. Ascospores 5 –6.5 × 5.5–7.5 µm . . . . . . M. macrosporus
6. Ascospores narrower . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
7. Ascospores 4 –6 × 3–5 µm, yellow in mass . M. alveolaris
7. Ascospores 6–7 × 4–4.5 µm elongated to one side, yellow
to orange in mass . . . . . . . . . . . . . . . . . M. campaniformis
8. Colonies dull to olive-green; ascospores lunate 4.5–6.5 ×
2–4 µm; conidiophores irregularly branched . . M. gracilis
8. Colonies light to brown-grey; ascospores reniform to
broadly lunate 4 – 6 × 2.5 – 4 µm; conidiophores usually
simple . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
9. Ascomata up to 300 µm diam; ascospores pale red-brown
in mass; conidia 2 –3 µm wide . . . . . . . . . . . M. cinereus
9. Ascomata less than 230 µm diam; ascospores straw colour
ed; conidia 4 –6 µm wide . . . . . . . . . . . . . . . . M. cirrosus
10. Ascospores triangular 4 –5 × 3–4 µm . M. trigonosporus
10. Ascospores otherwise . . . . . . . . . . . . . . . . . . . . . . . . . 11
11. Ascospores reniform . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
11. Ascospores broadly ovoid to ellipsoidal . . . . . . . . . . . . 13
12. Ascospores 7–9 × 2–3 µm, straw coloured, yellow in mass,
with a protuberant germ pore . . . . . . . . M. senegalensis
12. Ascospores 3–4 × 2–3.5 µm, hyaline to subhyaline with
an indistinct germ pore . . . . . . . . . . . . . . . . M. longirostris
13. Ascospores ellipsoidal 5–7 × 2–3 µm, light brown to brown
in mass . . . . . . . . . . . . . . . . . . . . . . . . M. brunneosporus
13. Ascospores broadly ovoid 3.5–5 × 2–3.5 µm, pale yellow
in mass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . M. hyalinus
14. Growth at 35 °C . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
14. No growth at 35 °C . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
15. Colonies fast growing (> 60 mm in 14 d); conidia bulletshaped to broadly clavate, finely roughened 4–8 × 2.5–3.5
µm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . M. expansus
15. Colonies growing restrictedly; conidia otherwise . . . . . 16
29
M. Sandoval-Denis et al.: Phylogeny of Microascus and Scopulariopsis
16. Colonies finely granular, olive-grey; conidiophores sparsely
warted . . . . . . . . . . . . . . . . . . . . . . . . . . . . M. verrucosus
16. Colonies downy to velvety, dark brown-grey; conidiophores
smooth-walled . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
17. Growth at 40 °C; conidia globose to obovoidal 4.5 –6 × 4–
5.5 µm, thick- and rough-walled . . . . . . . . . . M. restrictus
17. No growth at 40 °C; conidia smooth-walled . . . . . . . . . 18
18. Conidia broadly ellipsoidal to short clavate 4 – 6 × 2–4.5
µm with rounded apex . . . . . . . . . . . . . . . . . . . . M. paisii
18. Conidia cylindrical, 4–6 × 1.5–2 µm, usually with a pointed
apex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . M. murinus
19. Conidia globose, 3.5 – 5 × 3 – 4 µm, brown coloured; slow
growth at 5 °C . . . . . . . . . . . . . . . . . . . . . . . . . . . M. croci
19. Conidia ovate, usually with a pointed apex, 4 – 5.5 × 3–4
µm, green-brown; no growth at 5 °C . . . . . . . M. chartarus
Key to Pithoascus species
1. Colonies black, velvety or powdery; sexual morph not
formed in culture; asexual morph abundant showing conidia
globose to pyriform, 4 – 9 × 4.5 – 8.5 µm . . . . . . . . . P. ater
1. Colonies light grey to black, becoming crustose by the
formation of ascomata; asexual morph scarce or absent
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Ascomata 210 – 450 µm diam; ascospores falcate with
attenuated ends, up to 12 µm long . . . . . . . . . P. exsertus
2. Ascomata less than 170 µm diam; ascospores otherwise
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3. Ascomata 50 –110 µm diam; ascospores navicular, 6–7.5
× 2 – 3 µm, golden yellow to brown coloured . . P. stoveri
3. Ascomata 90 –160 µm diam; ascospores fusiform . . . . 4
4. Ascospores fusiform 5–6 µm long, honey coloured; asexual
morph when present forming globose to subglobose hyaline
conidia 4 – 8 × 4 –7.5 µm . . . . . . . . . . . . . . P. intermedius
4. Ascospores fusiform, nearly lunate 6–8 µm long, subhyaline
to straw coloured; asexual morph when present forming globose to ampulliform hyaline conidia 4 – 5 × 2.5 – 3.5 µm on
short stalks . . . . . . . . . . . . . . . . . . . . . . . . . . . . P. nidicola
Key to Pseudoscopulariopsis species
1. Colonies grey-white; conidia obovate or short clavate,
4.5 – 6 × 2.5 – 4 µm; sexual morph present in culture, with
pale brown fusiform or navicular ascospores, measuring
8 –13 × 2.5 – 4 µm . . . . . . . . . . . . . . . . . . . P. schumacheri
1. Colonies olive-grey; conidia subglobose 5 –7 × 5–6 µm;
sexual morph absent . . . . . . . . . . . . . . . . . . P. hibernica
Key to Scopulariopsis species
1. Colonies white, tending to light grey when ascomata are present . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
1. Colonies tan, pale brown to fuscous brown . . . . . . . . . . 5
2. Conidia smooth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
2. Conidia rough at maturity . . . . . . . . . . . . . . . . . . . . . . . . 4
3. Conidiophores abundant; conidia 6–9.5 × 5–8.5 µm; asco
spores when present hyaline, heart shaped . . S. candida
3. Conidiophores scarce; conidia 2.5 – 6 × 2 – 5 µm; asco
spores straw coloured, reniform to broadly lunate . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . S. cordiae
4. Conidia pale yellow in mass, globose to subglobose, 5.5–9
× 5 – 8 µm; sexual morph present; ascospores falcate to
lunate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . S. soppii
4. Conidia white in mass, globose to obovoidal, 6.5 –7 ×
5.5 – 6.5 µm; sexual morph not observed . . . . . . S. flava
5. Conidia brown in mass, verrucose at maturity, globose to
ovoid; 6 – 9 × 5.5 – 9 µm . . . . . . . . . . . . . . . . S. brevicaulis
5. Conidia dark brown to fuscous, smooth or verrucose, globose to ovate usually with a pointed apex, 5–8 × 4–6.5
µm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . S. asperula
EXCLUDED OR DOUBTFUL SPECIES
Microascus albonigrescens (Sopp) Curzi, Boll. Staz. Patol.
Veg. Roma 11: 60. 1931
Specimen examined. Japan, Hokkaido, from litter, treated with urea, 1967,
S. Udagawa (IHEM 18560 = CBS 109.69).
Notes — Our phylogenetic study demonstrates that this
taxon does not belong to Microascus s.str. It nested in a clade
related to the genera Cephalotrichum, Gamsia and Wardomy
ces, and might represent the former genus Acaulium, which
was typified by Sopp (1912) with Scopulariopsis albonigrescens
(sexual morph M. albonigrescens). Given the absence of type
material, however, we prefer not to introduce any taxonomic
changes until a more accurate study of the available reference
material can be carried out.
Microascus caviariformis Malloch & Hubart, Canad. J. Bot.
65: 2384. 1987
Specimen examined. Belgium, Prov. de Liège, Flemalle, Cave de Ramioul,
from decaying meat, 1985, J.M. Hubart (ex-type culture CBS 536.87).
Notes — As in the case of M. albonigrescens, our phylo
genetic data revealed that this taxon shows affinity with members of Cephalotrichum, Gamsia and Wardomyces rather than
Microascus. It could represent another species of the former
genus Acaulium.
Microascus decorticatus C. Ram, Nova Hedwigia 21: 226.
1972
Notes — The original description stated a close morphological relationship of this species with M. cinereus and M. gracilis.
Microascus decorticatus was described having slightly larger
ascomata, while the asci and ascospores are nearly identical
in size and shape to those of M. cinereus. Because the extype culture (IMUFPe 2194) was not available for study, the
taxonomy of this species remains unclear.
Microascus desmosporus (Lechmere) Curzi, Boll. Staz. Patol.
Veg. Roma 11: 60. 1931
≡ Peristomium desmosporum Lechmere, Compt. Rend. Hebd. Séances
Acad. Sci. 155: 178. 1912.
?= Peristomium desmosporum Lechmere var. verticillium Lechmere, Bull.
Trimestriel Soc. Mycol. France: 178. 1913.
= Microascus desmosporus (Lechmere) Curzi var. macroperithecia Sage,
Steiman, Seigle-Mur. & Guiraud, Mycotaxon 55: 191. 1995, nom inval. Art.
40.5 (Melbourne).
Notes — This species has a controversial taxonomy. Barron
et al. (1961) recognize M. desmosporus as a species distinct
from M. cirrosus while Morton & Smith (1963) regarded both
species as conspecific. However, the ex-type strain of M. cir
rosus was not examined by the latter authors. Von Arx (1975)
and von Arx et al. (1988) regarded M. desmosporus as a doubtful species considering that Peristomium desmosporum and
M. desmosporus are based on two different fungi. In the absence of type cultures the taxonomy of these fungi remains
unknown.
Microascus dimonatus Sage, Steiman, Seigle-Mur. & Guiraud,
Mycotaxon 55: 195. 1995
Notes — This name is currently considered as invalid in
fungal databases (Index Fungorum, MycoBank) following the
30
Persoonia – Volume 36, 2016
Art. 40.5 of the International Code of Nomenclature for algae,
fungi, and plants (Melbourne Code). As stated in the original
description, an ex-type culture of this fungus exists (CMPG
1274); however, it was not available for examination. Therefore,
according to Guarro et al. (2012) further studies are necessary
to clarify the taxonomy of this species.
Microascus singularis (Sacc.) Malloch & Cain, Canad. J. Bot.
49: 859. 1971
Microascus giganteus Malloch, Mycologia 62: 731. 1970
Notes — The morphological features of the asexual morph,
with conidia showing longitudinal bands, and the analysis of the
LSU and ITS sequences of a reference isolate (CBS 414.64)
showed that this taxon formed a phylogenetic lineage related to
Wardomyces and Wardomycopsis. However, given the absence
of an ex-type strain, a deeper phylogenetic analysis is required.
Specimen examined. Canada, Ontario, from insect frass in dead log, 1968,
D.W. Malloch (ex-type culture CBS 746.69 = UAMH 9425).
Notes — This is a coprophilous species, originally isolated
from insect dung (Malloch 1970), which resembles Microascus
species in many morphological characteristics, particularly in
those of the sexual state. However, it shows large (up to 750
µm) and hairy ascomata, the asci are formed irregularly at
the centre of the perithecia and it has a Wardomyces asexual
morph. The genus Wardomyces, typified by W. anomalus, is
characterised by having swollen conidiogenous cells forming
conidia in lateral or basipetal succession, the conidia are subglobose, ovoid or ellipsoid, brown to blackish and present a
single longitudinal germ-slit (Brooks & Hansford 1923, Hennerbert 1962). According to our combined LSU and ITS sequence
analysis (Fig. 1), M. giganteus is closely related to W. inflatus,
thus the morphological features and phylogenetic evidence
seem to demonstrate that M. giganteus is a Wardomyces species. However, sequence comparison with the type species of
Wardomyces is required for taxonomical changes.
Microascus inopinatus Udagawa & Furuya, Mycotaxon 7: 91.
1978
≡ Wardomycopsis inopinata Udagawa & Furuya, Mycotaxon 7: 92. 1978.
Specimen examined. Myanmar, from soil, 2008, C. Hartung (FMR 10305).
Notes — This taxon was described as unusual among the
genus Microascus since its asexual morph exhibits annellated
conidiogenous cells producing short catenate and globose
conidia with a prominent longitudinal germ-slit. Thus, the
genus Wardomycopsis was established to accommodate its
asexual state. Although the ex-type culture was not available,
the reference strain included in our study fits clearly with the
protologue of the species. The phylogenetic analysis of the
LSU and ITS sequences showed that this taxon was located
far from the Microascus clade forming a highly supported clade
with the ex-type strain of Wardomycopsis humicola (basionym
Scopulariopsis humicola CBS 487.66).
Microascus microcordiformis Matsush., Matsush. Mycol. Mem.
9: 16. 1996
Notes — The original description correlates with a Micro
ascus species; being morphologically close to M. longirostris.
However, in absence of live type material, the status of this
name remains unknown.
Microascus pilosus Valldos. & Guarro, Nova Hedwigia 57:
123. 1993
Basionym. Fairmania singularis Sacc., Ann. Mycol. 4: 276. 1906.
= Microascus doguetii Moreau, Rev. Mycol. 18: 177.1953.
Specimen examined. Japan, Tokyo, laboratory contaminant, 1962, S. Udagawa (CBS 414.64).
Microascus tardifaciens Y. Horie & Udagawa, Mycotaxon 17:
331. 1983
≡ Scopulariopsis tardifaciens Y. Horie & Udagawa, Mycotaxon 17: 331.
1983.
Notes — According to the protologue, this species is similar morphologically in colony features and its asexual morph
to M. albonigrescens and S. acremonium. In this sense, our
phylogenetic analysis (Fig. 1) showed that these species could
probably correspond to a species of the former genus Acaulium.
However, the ex-type culture (NHL 2912) of M. tardifaciens was
not available for study.
Pithoascus platysporus Arx & Veenb.-Rijks, Persoonia 7: 374.
1973
Specimen examined. The Netherlands, Wageningen, from agricultural
soil, date unknown, J.W. Veenbaas-Rijks (ex-type culture CBS 419.73).
Notes — This species was described showing reddish
brown, broadly cylindrical ascospores that differs from the main
characteristics of the genus Pithoascus. According to Abbott et
al. (2002), the ascospore morphology suggests a closer affinity
to Kernia or Lophotrichus. Although we were unable to obtain
sporulation from the ex-type strain (CBS 419.73), the analysis
of the LSU and ITS sequences showed that this taxon was
phylogenetically far from the Microascales and was closely
related with the Hypocreales.
Scopulariopsis acremonium (Delacr.) Vuill., Bull. Soc. Mycol.
France 27: 148. 1911
Basionym. Monilia acremonium Delacr., Soc. Mycol. Fr. 13: 114. 1897.
= Scopulariopsis communis Bainier, Bull. Soc. Mycol. France 23:
125.1907.
= Penicillium scopulariopsis Sacc., Syll. Fung. 22: 1275. 1913.
= Oospora glabra Hanzawa, J. Coll. Agric. Tohuko Imper. Univ. 4: 1912.
= Scopulariopsis candelabrum Loubière, Rech. Struct. Mucor. (Thesis),
Paris: 63. 1924.
= Penicillium brevicaule Sacc. var. glabrum Thom, Bull. U.S. Bur. Anim.
Ind. 118: 48. 1910.
≡ Scopulariopsis brevicaulis (Sacc.) Bainier var. glabra (Thom) Thom in
The Penicillia: 250. 1930.
= Scopulariopsis danica J.F.H. Beyma, Zentralbl. Bakteriol., 2 Abt. 99:
390. 1939.
Specimen examined. Spain, Burgos, from rabbit dung, 1986, M. Hernandez
(ex-isotype FMR 2604).
Specimens examined. Denmark, from horse skin infected with Tricho
phyton sp., 1938, C. Werdelin (Scopulariopsis danica ex-type culture MUCL
9028). – Germany, from wheat field soil, 1963, W. Gams (MUCL 8274); from
soil, collector unknown (MUCL 8409).
Notes — No live ex-type material is available for phylogenetic analyses. An isotype specimen (FMR 2604) is preserved
at the Universitat Rovira i Virgili. The morphological examination of this specimen corresponded with the original description
showing that this species clearly belongs to Microascus (Guarro
et al. 2012).
Notes — This species was transferred to Scopulariopsis from
Monilia acremonium by Vuillemin (1911). No ex-type strain of
M. acremonium exists. This taxon was later considered con
specific with Scopulariopsis danica by Morton & Smith (1963),
from which an ex-type culture (MUCL 9028) was available. Our
phylogenetic and morphological studies seem to confirm this
M. Sandoval-Denis et al.: Phylogeny of Microascus and Scopulariopsis
31
synonymy; however, this species is phylogenetically distant
from Scopulariopsis and related to the genera Cephalotrichum,
Gamsia, Trichurus and Wardomyces, clustering with a reference
strain of S. albonigrescens and probably corresponding to a
species of the former genus Acaulium (see M. albonigrescens).
acteristics with Scopulariopsis baarnensis, both species being
included in different series of Scopulariopsis (Morton & Smith
1963). The latter species was transferred to the genus Gliomas
tix, as G. murorum var. polychroma by Dickinson (1968), currently named Gliomastix polychromum (Bionectriaceae, Hypocreales) (Summerbell et al. 2011).
Scopulariopsis argentea Szilvinyi, Zentralbl. Bakteriol., 2 Abt.
103: 173. 1941
Although no ex-type culture of S. coprophila is available, two
reference strains were included in this study, one of them
(MUCL 9641) was reidentified here as M. trigonosporus. Interestingly, the second strain (CBS 206.61), according to its LSU
and ITS sequences it is phylogenetically related with members
of Bionectriaceae.
Notes — Type material was studied by Morton & Smith
(1963) and considered as ‘unidentifiable’. The protologue suggest a species of Paecilomyces. No living ex-type material is
available.
Scopulariopsis bertaccini Redaelli, Giorn. Ital. Derm. Syph.
75: 825. 1934
Notes — Type material was studied by Morton & Smith (1963),
and considered not to be a Scopulariopsis species. No living
type material is available.
Scopulariopsis canadensis F.J. Morton & G. Sm., Mycol. Pap.
86: 55. 1963
Specimen examined. Canada, British Columbia, from seed of Beta vulgaris,
1958, S.J. Hughes (ex-type culture CBS 204.61).
Notes — Our phylogenetic data showed that the ex-type
culture (CBS 204.61) is related to the Xylariales.
Scopulariopsis carbonaria F.J. Morton & G. Sm., Mycol. Pap.
86: 59. 1963
Specimen examined. Panama, from soil, 1961, R. Coghill (ex-type culture
MUCL 9027 = CBS 205.61).
Notes — Our phylogenetic data on LSU, ITS, EF-1α and
TUB showed that the ex-type strain (MUCL 9027) formed an
isolated lineage basal to the Microascus and Pithoascus clades.
However, the ex-type culture was sterile, impeding further com
parisons.
Scopulariopsis castellanii M. Ota & Komaya, Dermatol. Wo
chenschrift 78: 163. 1924
Notes — Morton & Smith (1963) considered its original description as ‘unidentifiable’. Since no living type material exists,
the identity of this taxon remains unknown.
Scopulariopsis coprophila (Cooke & Massee) W. Gams,
Cephalosporium-artige Schimmelpilze (Stuttgart): 207. 1971
Basionym. Monosporium coprophilum Cooke & Massee, Grevillea 16:
10. 1887.
= Monilia fimicola Costantin & Matr., Rev. Gén. Bot. 6: 292. 1894.
≡ Oospora fimicola (Costantin & Matr.) Cub. & Megliola, C. R. Accad.
Lincei: 440. 1903.
≡ Scopulariopsis fimicola (Costantin & Matr.) Vuill., Bull. Soc. Mycol.
France 27: 143. 1911.
Specimen examined. UK, from mushroom bed, 1946, C.J. La Touche (as
Scopulariopsis fimicola MUCL 9030 = CBS 206.61).
Notes — Originally described as Monosporium coprophilum,
this species was transferred to Scopulariopsis by Gams (1971)
who also considered it to be conspecific with Monilia fimicola.
The latter taxon had been previously transferred to Scopulari
opsis by Vuillemin (1911) as Scopulariopsis fimicola, a species
that was regarded as valid by Morton & Smith (1963); however,
these authors did not consider M. coprophilum, whose oldest
epithet has priority over fimicola. According to their observations, S. fimicola shares colonial and micromorphological char-
Scopulariopsis finkii Sartory & R. Sartory ex Vuill., Encycl.
Mycol. 2: 65. 1931
Notes — Original description of this fungus is too vague
and inadequate for recognition of the species (Morton & Smith
1963). Type material does not exist.
Scopulariopsis halophilica Tubaki, Trans. Mycol. Soc. Japan
14: 367. 1973
Specimen examined. Japan, Osaka, from Undaria pinnatifida, 1974, K.
Tubaki (ex-type culture CBS 380.74).
Notes — This name was considered by Pitt & Hocking (1985)
to be a synonym of Basipetospora halophila, a fungus formerly
described as Oospora halophila by van Beyma (1933). Recently,
Samson et al. (2014) transferred this species to the genus As
pergillus under the new name A. baarnensis. Our phylogenetic
data on LSU and ITS confirmed those results, showing its relationships with the Eurotiales.
Scopulariopsis hanii Moustafa & Abdul-Wahid, Nova Hedwigia
51: 476. 1990
Notes — According to the protologue, this fungus is morphologically compatible with the asexual morph of Microascus
and should be considered as member of this genus. In many
aspects, this species resembles M. restrictus and M. verruco
sus from which it can be differentiated by having annellides,
conidia and solitary sessile conidia at least two times larger.
The protologue indicates that holotype material was deposited
in the Herbarium of the Royal Botanic Gardens (IMI 326933).
However, this accession number corresponds to an isolate of
Scopulariopsis croci. No living culture of S. hanii was available
for study.
Scopulariopsis lanosa J.F.H. Beyma, Zentralbl. Bakteriol., 2 Abt.
99: 423. 1937
Notes — This species was excluded from the genus by
Morton & Smith (1963). No ex-type strain is available.
Scopulariopsis lilacea Szilvinyi, Zentralbl. Bakteriol., 2 Abt.
103: 174. 1941
Notes — Morton & Smith (1963) regarded the species as
‘unidentifiable’. The illustrations included in the protologue seem
to represent a conidial apparatus similar to Fusarium, while
none of the described structures fits with those of Scopulari
opsis. No live cultures were available.
Scopulariopsis lingualis Neto bis & C. Martins, Compt. Rend.
Seanc. Soc. Biol. 106: 1179. 1931
Notes — Morton & Smith (1963) regarded the species as
‘unidentifiable’. No living type material was available.
32
Persoonia – Volume 36, 2016
Scopulariopsis longipes H.Q. Pan & T.Y. Zhang, Mycosystema 33: 2. 2014
Scopulariopsis parva (A.H.S. Br. & G. Sm.) Samson, Stud. Mycol.
6: 102. 1974
Notes — This species was recently described based only on
morphological features but no phylogenetic study was carried
out. Unfortunately, the type material listed in the protologue
(holotype HMAS 196252, dried culture HSAUP II 074334) is not
available for comparison. According to the authors, S. longipes
morphologically resembles S. fusca (syn. S. asperula), but differs in having smaller conidia (3.5 – 5 µm wide vs 5 – 8 µm in
S. fusca).
Basionym. Paecilomyces parvus A.H.S. Br. & G. Sm., Trans. Brit. Mycol.
Soc. 40: 58. 1957.
Scopulariopsis maduramycosis Q.T. Chen, Chin. Med. J. 99:
378. 1986
Notes — This name has been invalidated since it was published without an adequate description or holotype information.
Scopulariopsis mencieri C.W. Dodge, Medical Mycology.
Fungous diseases of men and other mammals: 648. 1935
Notes — According to Morton & Smith (1963) the description
is inadequate. No living type material is available.
Scopulariopsis minima Sartory, Hufschm. & J. Mey., Bull.
Acad. Méd. Paris, sér. 3, 103: 606. 1930
Notes — This species is not a Scopulariopsis according to
Morton & Smith (1963). No living material is available.
Scopulariopsis mottai Vuill., Encycl. Mycol. 2: 62. 1931
Notes — Considered as a doubtful species by Dodge (1935),
and probably not a Scopulariopsis according to Morton & Smith
(1963). No living material is available.
Scopulariopsis musae Matsush., Matsush. Mycol. Mem. 5: 27.
1987
Notes — The protologue of this species has morphological
features that could correspond with an asexual state of Micro
ascus. However, it shows asymmetrical, curved and extremely
large conidia, features that do not match with the typical characteristics of the genus. No living culture is available for study.
Scopulariopsis nicotianae J.F.H. Beyma, Zentralbl. Bakteriol.,
2 Abt. 91: 354. 1933
Notes — According to Morton & Smith (1963) the fungus
probably belongs to a fungal genus different from Scopulari
opsis. No living material is available.
Specimen examined. Canada, Alberta, from soil, 1961, J.W. Carmichael
(Scopulariopsis parvula ex-type culture MUCL 9041 = CBS 209.61).
Notes — This species was originally described as Scopula
riopsis parvula by Morton & Smith (1963). Samson (1974) considered this taxon as synonym of the older species Paecilo
myces parvus, transferred to Scopulariopsis since it produces
conidia with a truncate base, thus the new combination S. parva
was established. However, the analysis of the LSU and ITS
sequences of the ex-type culture (basionym Scopulariopsis
parvula MUCL 9041) showed that this fungus is related with
the Eurotiomycetes.
Scopulariopsis penicillioides H.Q. Pan, Y.L. Jiang, H.F. Wang
& T.Y. Zhang, Mycosystema 33: 3. 2014
Notes — This name is an illegitimate later homonym of Scopulariopsis penicillioides (Delacroix) Smith & Ramsbottom
(1915), a species considered a synonym of S. brevicaulis in
Morton & Smith (1963), but not listed in the repositories for fungal names such as Index Fungorum or MycoBank. Comparing
the original descriptions of these two fungi we conclude that
they are different species. While S. penicillioides (Delacroix)
Smith & Ramsbottom, a species based on Monilia penicillioides
Delacroix (1897), shows pale-yellow, oval and echinulate conidia, the fungus described by Pan et al. (2014) has pale-brown,
ellipsoidal to broadly obovoid and smooth-walled conidia. The
latter fungus resembles Pseudoscopulariopsis hibernica but
mainly differs in having narrower conidia (3–4.5 µm vs 5–6 µm
in P. hibernica). The molecular study of these fungi has not been
carried out because the type material listed in the protologue of
S. penicillioides (holotype HMAS 196253, dried culture HSAUP
II 074299) is not available for comparison.
Scopulariopsis polychromica Szilvinyi, Zentralbl. Bakteriol.,
2 Abt. 103: 175. 1941
Notes — According to Morton & Smith (1963) the fungus
is unrecognisable from the original description. The original
illustrations seem to represent a ‘degenerated’ strain. A type
does not exist.
Scopulariopsis rosacea Szilvinyi, Zentralbl. Bakteriol., 2 Abt.
103: 175. 1941
Notes — ‘Unidentifiable’ according to Morton & Smith (1963).
No living material is available.
Scopulariopsis nivea Demelius, Verh. Zool.-Bot. Ges. Wien
66: 490. 1916
Scopulariopsis rubellus Bainier, Bull. Soc. Mycol. France 23:
104. 1907
Notes — According to the original description the fungus
might represent a Scopulariopsis species; however, the description is too vague. No living specimen is available.
Notes — Inadequately described according to Morton &
Smith (1963). An ex-type strain does not exist.
Scopulariopsis olivacea Szilvinyi, Zentralbl. Bakteriol., 2 Abt.
103: 174. 1941
Notes — Description and illustrations of the protologue seem
to indicate that this is a Penicillium species. No living cultures
are available.
Scopulariopsis sehnsuchta Mello, Bull. Soc. Pathol. Exot.
25: 296. 1932
Notes — This fungus was poorly described according to
Morton & Smith (1963). No living material is available.
Scopulariopsis silvatica (Oudem.) Apinis, Nova Hedwigia 5:
73. 1963
Basionym. Spicaria silvatica Oudem., Arch. Néerl. Sci., sér. 2, 7: 291. 1902.
33
M. Sandoval-Denis et al.: Phylogeny of Microascus and Scopulariopsis
Notes — The description of S. silvatica (Apinis 1962) and
the illustrations of the basionym Spicaria silvatica, seem to
represent a fungus not belonging to Scopulariopsis, showing
a phialidic conidiogenesis with abundant intercalary phialides.
No living material is available for examination.
Scopulariopsis spinosa E. Müll. & Pacha-Aue, Nova Hedwigia
18: 161. 1970
Notes — The original illustrations of the fungus suggest the
conidial apparatus typical of a Penicillium species. No living
culture is available.
Scopulariopsis sputicola (Galippe) C.W. Dodge, Medical
Mycology. Fungous diseases of men and other mammals:
648. 1935
Basionym. Monilia sputicola Galippe, J. Anatomie 21: 538. 1885.
Notes — ‘Unidentifiable’ according to Morton & Smith (1963).
No living material is available.
Scopulariopsis tritici K.B. Deshp. & K.S. Deshp., Curr. Sci.
34: 222. 1965
Notes — The original description and illustration seem to
belong to a species of Stachybotrys or related taxa. According to
the authors of the species, the holotype and an ex-type culture
were deposited in the Herbarium Cryptogamae India Orientalia
(New Delhi) and in the Herbarium of the Botany Department,
Marathwada University (Aurangabad) from India. However, no
records of this species were found in the respective catalogues.
Scopulariopsis venerei Greco, Origine des Tumeurs (Etiologie
du Cancer, etc.) et Observations de Mycoses (Blastomycoses, etc.) Argentines (Buenos Aires): 716. 1916
Notes — Morton & Smith (1963) considered this fungus as
a possible species of Botrytis. No living material is available.
Scopulariopsis verticillioides Kamyschko, Notul. Syst. Sect.
Cryptog. Inst. Bot. Acad. Sci. U.S.S.R. 14: 225. 1961
Notes — Living material of this species is not available.
Scopulariopsis verrucaria (‘verrucifera’ ) H.F. Wang & T.Y.
Zhang, Mycosystema 33: 4. 2014
Notes — This species was recently described based only on
morphological features. This has not been included in our phylogenetic study because the type material listed in the protologue
(holotype HMAS 196254, dried culture HSAUP II 064334) is not
available for comparison. According to the original description
and illustration of the species, it is similar to Microascus ver
rucosus. However, S. verrucaria differs in having dark brown
colonies, and conidia of 3 – 5 µm wide covered by a gelatinous
membrane, while M. verrucosus has olive grey colonies and
rough, somewhat wider conidia (5 –7 µm).
Scopulariopsis vignolo-lutatii (Matr.) C.W. Dodge, Medical
Mycology. Fungous diseases of men and other mammals:
650. 1935
Basionym. Acaulium vignolo-lutatii Matr. (as Vignoli-Lutatii), in VignoloLutati, Arch. Derm. Syph., Berlin 118: 690. 1913.
Notes — Dodge (1935), although with no strong conviction
due to its inadequate description, transferred Acaulium vignolilutatii to Scopulariopsis. Morton & Smith (1963) considered this
species as a possible member of the Scopulariopsis brumptii
series, but with an inadequate description for recognition of the
fungus. The original description and illustration seem to refer to
a fungus morphologically close to M. paisii. No living cultures
are available for study.
Scopulariopsis yunnanensis Q.T. Chen & C.L. Jiang, Acta
Mycol. Sin. 4: 167. 1985
Notes — The original description seems to refer to a Scopu
lariopsis species. However, it was described forming bifurcate
chains of conidia. In addition, the conidia are smaller than those
of the currently known Scopulariopsis species. According to
the authors (Jiang et al. 1985), S. yunnanensis is similar to
S. parva, a species that according to our results is phylogenetically related with the Eurotiomycetes. The ex-type strain of this
species is not available.
DISCUSSION
In this study we have reviewed the taxonomic circumscription
of Microascus and Scopulariopsis, traditionally referred to as
sexual and asexual morphs, respectively, and related genera
using a polyphasic approach based on the evaluation of molecular, physiological and morphological data. These results
show that Microascus and Scopulariopsis constitute two phylogenetically distant lineages, which are clearly different from
Pithoascus, a genus revalidated in the present work, and from
the lineage proposed here as the novel genus Pseudoscopu
lariopsis. Furthermore, combining the results of a multilocus
sequence analysis and phenotypic data, we were able to delineate the accepted species of the four genera, proposing
several new ones.
One of the first attempts to clarify phylogenetically the relationships among the different genera of the Microascales by the use
of partial LSU sequences was that of Issakainen et al. (2003).
That study demonstrated polyphyly of several genera of Micro
ascaceae and raised questions concerning correct positions of
several members of the family and their generic circumscriptions, suggesting a possible subdivision of Microascus and
Scopulariopsis into several smaller genera. However, the LSU
fragments used were too small and poorly informative, thus no
final conclusions were made. Nevertheless, our phylogenetic
analysis based on combined, longer LSU and ITS sequences
proved to be useful to resolve topology of the different genera
in the Microascacae. Confirming the findings of Issakainen et al.
(2003), we demonstrated that Microascus and Scopulariopsis
are clearly polyphyletic and that their currently accepted species
are grouped in at least seven different lineages. In addition, the
combined LSU and ITS phylogeny showed that the dry-spored
synnematous genera Cephalotrichum, Doratomyces, Stysanus,
and Trichurus are conspecific, which agrees with Abbott (2000)
who synonymised and integrated these four genera under the
name Cephalotrichum. However, given the lack of ex-type
strains for most of the species, no formal decision is made at the
moment. The genus Cephalotrichum, as well as several other
genera of the Microascaceae, such as Kernia, Wardomyces and
Wardomycopsis, have been considered in the past as probably
congeneric with Scopulariopsis or Microascus (Morton & Smith
1963, Abbott 2000). Our phylogeny demonstrates that, although
these genera share similar morphological and ecological traits,
they are in fact genetically distant. The phylogenetic data is
supported by relevant morphological differences, such as the
presence of germ slits, synnemata or conspicuously hairy
ascomata (Abbott 2000, Issakainen et al. 2003).
The recognition of Pithoascus as a valid genus has always
been a matter of discussion. Probably one of the strongest
reasons to synonymise the genus with Microascus was the
obovate
–
–
+
+
+
+
+
–
+
–
dark grey
white to olive grey
grey-black to brown-black
grey opaque
pale to dark grey
grey to violaceus grey
+
+
125–250
5– 6.5 × 5.5–7
+
dull to olive green
grey-brown grey-black
–
+
4 – 6 × 2 – 4.5
–
olive to grey-brown
olive to brown-grey
pale brown
grey
olive grey
M. expansus
M. gracilis
M. hyalinus
M. intricatus
M. longirostris
M. macrosporus
M. murinus
M. paisii
M. pyramidus
M. restrictus
M. senegalensis
M. trigonosporus
M. verrucosus
+
+
white to light grey
light to dark grey
P. nidicola
P. stoveri 2
+
+
+
+
–
+
tan
white
white to light grey
white
white
S. candida
S. cordiae
S. flava
S. soppii
Asexual morph data obtained from Roberts (1985).
2
Asexual morph data obtained from von Arx et al. (1988).
3
Sexual morph data obtained from von Arx et al. (1988).
4
Sexual morph data obtained from Abbott & Sigler (2001).
1
+
130 –250
180–300
140–200
50–180
130–300
5–6.5 × 5.5–7.5
3– 4 × 2–3.5
5 –6 × 2.5–3.5
3.5–5 × 2–3.5
4.5–6.5 × 2–4
triangular
reniform
fusiform
broadly ovoid
lunate
+
+
+
+
+
+
130–250
180 –250
3– 5 × 3–4
7–9 × 2–3
triangular
reniform
+
+
+
+
+
+
triangular or quadrangular
with attenuated ends
+
+
+
+
+
+
+
5 –7 × 4.5 – 6
2.5 – 3.5 × 3.5 – 5.5
4.5 – 5.5 × 3.5 – 4
4.5 – 6 × 4 – 5.5
4.5 – 5.5 × 3 – 4
4 – 6 × 1.5 – 2
5 –7 × 4 – 5
4–6 × 3–4
4 – 5 × 3 – 3.5
3.5 – 5 × 2 – 3.5
3.5 – 5.5 × 2 – 3.5
4 – 8 × 2.5 – 3.5
3.5 – 5 × 3 – 4
4 – 6.5 × 4 – 6
globose to subglobose
globose to ovoid
obovate
globose to obovoidal
cylindrical
globose to ovoid
obovate
globose to broadly ellipsoidal
ovoid
subglobose or ellipsoidal
bullet shaped to broadly clavate
globose
subglobose to obovate
–
–
–
–
–
–
–
–
–
–
–
–
+
+
–
–
–
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
–
+
+
+
30
+
+
+
+
+
+
+
+
–
+
+
+
+
–
+
+
–
+
+
+
35
–
–
–
+
+
–
–
+
–
+
–
+
+
–
+
+
–
+
–
+
40
–
+
+
+
210–450
50–110
90–160
95 –150
6.5–12 × 1–2.5
6–7.5 × 2–3
6 –8 × 2–2.5
5–6 × 2–2.5
falcate
navicular
fusiform, nearly lunate
fusiform
–
–
5–8 × 3–4
4 – 5 × 2.5 – 3.5
4 – 8 × 4 –7.5
obovate to pyriform
globose to ampulliform
globose to subglobose
–
–
–
–
–
–
+
+
+
+
+
+
+
+
+
–
+
+
+
–
+
–
+
140–190
8–13 × 2.5–4
fusiform or navicular
–
4.5 – 6 × 2.5 – 4
obovate, short clavate
–
+
–
–
–
100 –150
100–170
70 –150
4.5 –5.5 × 3.5–4
4 –6 × 5–6
5– 6 × 3.5–4.5
reniform
reniform, heart shaped
broadly reniform
+
+
+
+
130–200
6 –7 × 2.5–3
lunate
+
+
+
+
+
5.5 – 9 × 5 – 8
6.5 – 7 × 5.5 – 6.5
2.5 – 6 × 2 – 5
6 – 9.5 × 5 – 8.5
6 – 9 × 5.5 – 9
globose to subglobose
globose to obovoidal
broadly ellipsoidal to obovoidal
subglobose to broadly ovate
globose to ovate
–
–
–
–
–
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
–
–
+
–
+
dark brown
+
+
130–190
4.5–6.5 × 3.5–4
broadly reniform
5 – 8 × 4 – 6.5
globose to ovate
–
+
+
+
–
grey-white
S. brevicaulis
Scopulariopsis
S. asperula 4
P. schumacheri 3
5–6 × 3–4
obovate or clavate
ovate
+
+
+
25
olive grey
–
+
5 –7 × 5 – 6
subglobose
–
+
–
–
–
+
+
white
white to light grey
P. intermedius1
Pseudoscopulariopsis
P. hibernica
140 –230
+
+
3–5 × 2–3
4 – 5.5 × 3 – 4
–
–
–
5
Growth at (º C)
brown-black
–
+
4 – 9 × 4.5 – 8.5
globose to pyriform
+
+
+
+
–
P. exsertus
Pithoascus
P. ater
broadly ellipsoidal to
short clavate
broadly reniform
+
+
+
subglobose to broadly
ellipsoidal
subglobose to navicular
grey to mouse grey
ellipsoidal to bullet shaped
brown-grey
4 – 5 × 2.5 – 5
M. croci
3 – 5 × 2 – 3.5
M. cirrosus
–
+
reniform, broadly lunate,
rarely triangular
+
triangular with an
+
4 – 5 × 2.5 – 3.5
elongated side
ellipsoidal
light to dark grey
+
+
95–300
4–5.5 × 2.5–4
broadly triangular
grey to smoke grey
5–7 × 2–3
M. cinereus
4 –6 × 3–5
M. chartarus
110–205
dull green
+
+
150– 220
6–7 × 4–4.5
110– 290
M. campaniformis
+
+
dull green to olive brown
+
+
white to grey
M. brunneosporus
Microascus
M. alveolaris
Sexual
Asexual
Ascomata
Ascospore
Ascospore
Germ pore
Conidial
Conidial
morph
morph
diam (µm)
size (µm)
shape
size (µm)
shape
Colony
Species
Table 2 Relevant phenotypic features of members of Microascus, Pithoascus, Pseudoscopulariopsis and Scopulariopsis.
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Persoonia – Volume 36, 2016
35
M. Sandoval-Denis et al.: Phylogeny of Microascus and Scopulariopsis
publication of the species M. caviariformis by Malloch & Hubart (1987), a fungus exhibiting intermediate characteristics
between Microascus and Pithoascus. Microascus caviariformis
showed the typical ascospores of Pithoascus, although with
an inconspicuous germ pore, and produced abundant conidia.
Our study demonstrated that both genera were clearly separated, thus confirming the original observations made by Skou
(1973) and von Arx (1973a, b). Moreover, our data showed that
M. caviariformis was located outside the main clades, which
represent the genera Microascus, Pithoascus, Scopulariopsis
and Pseudoscopulariopsis, forming a distant and strongly
supported clade with S. acremonium and a reference strain of
M. albonigrescens. The latter fungus was described as the sexual morph of the type species of Acaulium (Sopp 1912), and this
genus was considered as congeneric with Microascus (Curzi
1930, Barron et al. 1961, Morton & Smith 1963). However, our
phylogenetic analysis suggests that the old genus Acaulium
might be revalidated. Considering that neither original cultures
of Sopp, nor an ex-type strain of M. albonigrescens were
available for analysis, we think it is best to not propose further
taxonomic changes at the moment. Furthermore, M. singularis
proved to be related to the putative Acaulium clade, which also
constituted a new lineage among the Microascaceae. More
study is needed on members of these clades and their closest
phylogenetic relatives.
Although the morphological differences distinguishing the genera treated here are subtle, they correlate with the phylogenetic
data, shape, size and colour of annellides and conidia, shape
of ascospores and presence of germ pores being the most
informative morphological characters (Table 2). Other features,
such as shape and size of ascomata and number and shape
of ostiolar necks, are frequently associated with environmental
changes related to incubation conditions (Barron et al. 1961).
On the basis of our data, we recommend using PCA or OA
culture media to achieve the best growth and sporulation ratio.
On PCA these fungi produce fast and abundant sporulation
but some species, particularly those with little growth of their
asexual morphs, might sporulate better on OA. It is most likely
that variable morphological differences observed in the past
might have led to incorrect identification of strains due to overlapping characteristics between closely related species. For
example, two strains (MUCL 9048 and MUCL 9049) that were
received as M. cinereus were finally reidentified as belonging
to the undescribed sexual morph of M. gracilis, a species morphologically close to M. cinereus but differentiated by size and
complexity of conidiophores and shape of ascospores (Table 2).
Barron et al. (1961) and Udagawa (1962) mentioned a wide
variation in size and shape of ascospores of isolates identified
as M. trigonosporus, i.e. from triangular to nearly quadrangular, with some isolates showing spores distinctly longer at one
side, but judging from our data this ascospore shape variation
might correspond to different phylogenetic species. Most of the
species of Microascus newly described here showed triangular
ascospores of variable size. The new species M. campaniformis
produced inequilateral spores with the longer side towards the
germ pore, although the measurements do not coincide with
those previously described by the authors mentioned above.
One of the main objectives of the present work was to assess
the phylogenetic relationships among members of Microascus
and Scopulariopsis in order to comply with the requirements of
the new International Code of Nomenclature for fungi, algae
and plants (Hawksworth et al. 2011). As has been discussed
extensively by Hawksworth (2012), for this particular dual-name
combination an option might be to retain the most ‘widely-used’
name. Accordingly, Scopulariopsis should have priority over
Microascus, primarily because of the abundant medical literature on this genus (Hawksworth 2012, Sandoval-Denis et al.
2013). Our proposal to separate both genera is an alternative
approach that maintains the names of the most relevant species
of each genus, including those of the species that are significant
in medicine as well as some important plant pathogens.
Acknowledgements We thank Chantal Planard and Marijke Hendrickx
(Belgian Coordinated Collections of Microorganisms, BCCM/IHEM), Lynne
Sigler and Connie F.C. Gibas (University of Alberta Microfungus Collection
and Herbarium, UAMH) for providing cultures. This study was in part supported by the Spanish Ministerio de Economía y Competitividad, grant CGL
2011-27185.
REFERENCES
Abbott SP. 2000. Holomorph studies of the Microascaceae (PhD dissertation).
Edmonton, Alberta, University Alberta.
Abbott SP, Lumley TC, Sigler L. 2002. Use of holomorph characters to delimit Microascus nidicola and M. soppii sp. nov., with notes on the genus
Pithoascus. Mycologia 94: 362 – 369.
Abbott SP, Sigler L. 2001. Heterothallism in the Microascaceae demonstrated
by three species in the Scopulariopsis brevicaulis series. Mycologia 93:
1211–1220.
Abbott SP, Sigler L, Currah RS. 1998. Microascus brevicaulis sp. nov., the
teleomorph of Scopulariopsis brevicaulis, supports placement of Scopulariopsis with the Microascaceae. Mycologia 90: 297– 302.
Apinis AE. 1962. Occurrence of thermophilous microfungi in certain alluvial
soils near Nottingham. Nova Hedwigia 5: 57–78.
Arx JA von. 1973a. Ostiolate and nonostiolate pyrenomycetes. Koninklijke
Nederlandse Akademie van Wetenschappen, Amsterdam.
Arx JA von. 1973b. The genera Petriellidium and Pithoascus (Microasca
ceae). Persoonia 7: 367– 375.
Arx JA von. 1975. Revision of Microascus with the description of a new species. Persoonia 8: 191–197.
Arx JA von. 1978. Notes on Microascaceae with the description of two new
species. Persoonia 10: 23 – 31.
Arx JA von, Figueras MJ, Guarro J. 1988. Sordariaceous ascomycetes without ascospore ejaculation. Beihefte zur Nova Hedwigia 94: 1–104.
Baddley JW, Moser SA, Sutton DA, et al. 2000. Microascus cinereus (ana
morph Scopulariopsis) brain abscess in a bone marrow transplant recipient.
Journal of Clinical Microbiology 38: 395 – 397.
Bainier G. 1907. Mycothèque de l’École de Pharmacie, XIV. Scopulariopsis
(Penicillium pro parte) genre nouveau de mucédinées. Bulletin Trimestriel
de la Société Mycologique de France 23: 98 –105.
Barron GL, Cain RF, Gilman JC. 1961. The genus Microascus. Canadian
Journal of Botany 39: 1609 –1631.
Beyma FH van. 1933. Beschreibung einiger neuer Pilzarten aus dem Cen
traalbureau voor Schimmelcultures - Baarn (Holland). Zentralblatt für
Bakteriologie und Parasitenkunde Abteilung 2, 88: 132–141.
Biourge P. 1923. Les moisissures du groupe Penicillium Link: etude mono
graphique. La Cellule 33: 7–331.
Brooks FT, Hansford CG. 1923. Mould growths upon cold-store meat. Transactions of the British Mycological Society 8: 113 –142.
Crous PW, Gams W, Stalpers JA, et al. 2004. MycoBank: an online initiative
to launch mycology into the 21st century. Studies in Mycology 50: 19 – 22.
Curzi M. 1930. Una nuova specie di Microascus. Bolletino della Stazione di
Patologia Vegetale di Roma 10: 302 – 309.
Curzi M. 1931. Rapporti fra i generi Microascus Zukal e Scopulariopsis
Bainier. Bolletino della Stazione di Patologia Vegetale di Roma 11: 55 – 60.
Delacroix EG. 1897. Quelques espéces nouvelles. Bulletin de la Société
Mycologique de France 13: 114 –127.
Dickinson CH. 1968. Gliomastix Guéguen. Mycological Papers 115: 1– 24.
Dodge CW. 1935. Medical mycology; fungous diseases of men and other
mammals. St. Louis, The C.V. Mosby Company.
Dominik T, Majchrowicz I. 1970. Further contribution to the knowledge of
keratinolytic and keratinophilic fungi of the region of Szczecin. Keratinolytic and keratinophilic fungi in the excrements of farm animals. Ekologia
Polska 18: 571– 611.
Domsch KH, Gams W, Anderson TH. 2007. Compendium of soil fungi ed 2.
Eching, IHW Verlag.
Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy
and high throughput. Nucleic Acids Research 32: 1792 –1797.
Émile-Weil P, Gaudin L. 1919. Contribution a l’étude des onychomycoses.
Archives de Médecine Expérimentale et d’Anatomie Pathologique 28:
452 – 467.
Felsenstein J. 1985. Confidence limits on phylogenies: an approach using
the bootstrap. Evolution 39: 783 –791.
36
Gams W. 1971. Cephalosporium-artige Schimmelpilze (Hyphomycetes).
Fischer Verlag, Stuttgart.
Giraldo A, Gené J, Sutton DA, et al. 2014. Phylogenetic circumscription
of Arthrographis (Eremomycetaceae, Dothideomycetes). Persoonia 32:
102 –114.
Glass NL, Donaldson GC. 1995. Development of primer sets designed for use
with the PCR to amplify conserved genes from filamentous ascomycetes.
Applied and Environmental Microbiology 61: 1323 –1330.
Guarro J, Gené J, Stchigel AM, et al. 2012. Atlas of soil ascomycetes. CBS
Biodiversity Series. CBS-KNAW Fungal Biodiversity Centre, Utrecht, The
Netherlands.
Hansen EC. 1876. De Danske Gjøningssvampe (Fungi fimicoli Danici). Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening i Kjøbenhavn.
38: 207–354.
Hansford CG. 1944. Contribution towards the fungus flora of Uganda. VI.
New records. Proceedings of the Linnean Society London 156: 102 –124.
Hawksworth DL. 2012. Managing and coping with names of pleomorphic
fungi in a period of transition. IMA Fungus 3: 15 – 24.
Hawksworth DL, Crous PW, Redhead SA, et al. 2011. The Amsterdam declaration on fungal nomenclature. IMA Fungus 2: 105 –112.
Hennebert GL. 1962. Wardomyces and Asteromyces. Canadian Journal of
Botany 40: 1203–1216.
Hibbett DS, Taylor JW. 2013. Fungal systematics: is a new age of enlightenment at hand? Nature Reviews Microbiology 11: 129 –133.
Hoog GS de, Guarro J, Gené J, et al. 2011. Atlas of clinical fungi. CD-ROM
version 3.1. CBS-KNAW Fungal Biodiversity Centre, Utrecht.
Huelsenbeck JP, Ronquist F. 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754 –755.
Issakainen J, Jalava J, Hyvönen J, et al. 2003. Relationships of Scopulariopsis based on LSU rDNA sequences. Medical Mycology 41: 31– 42.
Iwen P, Schutte SD, Florescu DF, et al. 2012. Invasive Scopulariopsis
brevicaulis infection in an immunocompromised patient and review of
prior cases caused by Scopulariopsis and Microascus species. Medical
Mycology 50: 561–569.
Jiang CI, Xu LH, Chen QT. 1985. A new species of Scopulariopsis Bainier.
Acta Mycologica Sinica 4: 167–170.
Kornerup A, Wanscher JH. 1978. Methuen handbook of colour, 3rd edition.
London, Methuen.
Lackner M, Hoog GS de. 2011. Parascedosporium and its relatives: phylo
geny and ecological trends. IMA Fungus 21: 39 – 48.
Lackner M, Hoog GS de, Yang L, et al. 2014. Proposed nomenclature for
Pseudallescheria, Scedosporium and related genera. Fungal Diversity
67: 1–10.
Lumbsch HT, Huhndorf SM. 2007. Outline of Ascomycota – 2007. Myconet
13: 1–58.
Malloch D. 1970. New concepts in the Microascaceae illustrated by two new
species. Mycologia 62: 727–740.
Malloch D, Cain RF. 1971. The genus Kernia. Canadian Journal of Botany
49: 855–867.
Malloch D, Hubart JM. 1987. An undescribed species of Microascus from the
Cave of Ramioul. Canadian Journal of Botany 65: 2384 – 2388.
Malloch D, Sigler L. 1988. The Eremomycetaceae (Ascomycotina). Canadian
Journal of Botany 66: 1929 –1932.
Mangan A. 1965. Scopulariopsis hibernica sp. nov. Transactions of the British
Mycological Society 48: 617– 620.
Massee GE, Salmon ES. 1901. Researches on coprophilous fungi. Annals
of Botany 15: 313–357.
McNeill J, Barrie FR, Buck WR, et al. (eds). 2012. International Code of
Nomenclature for algae, fungi, and plants (Melbourne Code). Regnum
Vegetabile 146. Gantner Verlag, Ruggell.
Mohammedi I, Piens M, Audigier-Valette C, et al. 2004. Fatal Microascus
trigonosporus (anamorph Scopulariopsis) pneumonia in a bone marrow
transplant recipient. European Journal of Clinical Microbiology & Infectious
Diseases 23: 215–217.
Morton FJ, Smith G. 1963. The genera Scopulariopsis Bainier, Microascus
Zukal, and Doratomyces Corda. Mycological Papers 86: 1– 96.
Nylander JA. 2004. MrModeltest v2. Program distributed by the author.
Evolutionary Biology Centre, Uppsala University.
O’Donnell K. 1993. Fusarium and its near relatives. In: Reynolds DR, Taylor
JW (eds), The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics: 225 – 233. CAB International, Wallingford.
Pan HQ, Wang HF, Jiang YL, et al. 2014. Scopulariopsis: three new species
and a key to species from soils in China. Mycosystema 33: 1– 6.
Pitt JI, Hocking AD. 1985. New species of fungi from Indonesian dried fish.
Mycotaxon 22: 197–208.
View publication stats
Persoonia – Volume 36, 2016
Rehner SA, Buckley E. 2005. A Beauveria phylogeny inferred from nuclear
ITS and EF1-α sequences: evidence for cryptic diversification and links to
Cordyceps teleomorphs. Mycologia 97: 84 – 98.
Roberts RG. 1985. The anamorph of Microascus intermedius Emmons &
Dodge (abstract). Mycological Society of America Newsletter 36: 37.
Ropars J, Cruaud C, Lacoste S, et al. 2012. A taxonomic and ecological
overview of cheese fungi. International Journal of Food Microbiology 155:
199 – 210.
Saccardo PA. 1882. Fungi veneti novi vel critici vel mycologiae venetae
addendi. Series 13. Michelia 2: 528 – 563.
Samson RA. 1974. Paecilomyces and some allied Hyphomycetes. Studies
in Mycology 6: 1–119.
Samson RA, Houbraken J, Thrane U, et al. 2010. Food and indoor fungi.
CBS Laboratory Manual Series 2. CBS-Fungal Biodiversity Centre, Utrecht.
Samson RA, Klopotek A von. 1972. Scopulariopsis murina, a new fungus
from self-heated compost. Archiv für Mikrobiologie 85: 175 –180.
Samson RA, Visagie CM, Houbraken J, et al. 2014. Phylogeny, identification
and nomenclature of the genus Aspergillus. Studies in Mycology 78: 141–
173.
Sandoval-Denis M, Sutton DA, Fothergill AW, et al. 2013. Scopulariopsis, a
poorly known opportunistic fungus: spectrum of species in clinical samples
and in vitro responses to antifungal drugs. Journal of Clinical Microbiology
51: 3937– 3943.
Seifert KA, Morgan-Jones GA, Gams W, et al. (eds). 2011. The genera of
Hyphomycetes. CBS Biodiversity Series 9, CBS Fungal Diversity Centre,
Utrecht, The Netherlands.
Skou JP. 1973. Microascus exsertus sp. nov. associated with a leaf-cutting
bee, with considerations on relationships of species in the genus Microascus
Zukal. Antonie van Leeuwenhoek 39: 529 – 538.
Smith AL, Ramsbottom J. 1915. New or rare microfungi. Transactions of the
British Mycological Society 5: 156 –168.
Smith G. 1952a. Masonia, a new genus of Hyphomycetes. Transactions of
the British Mycological Society 35: 149 –151.
Smith G. 1952b. Masoniella nom. nov. Transactions of the British Mycological Society 35: 237.
Sopp OJ. 1912. Monographie der Pilzgruppe Penicillium mit besonderer
Berücksichtigung der in Norwegen gefunden Arten. Videnskaps Selskapets
Skrifter 1. Matematisk-Naturvidenskabelig Klasse 11: 1– 207.
Summerbell RC, Gueidan C, Schroers HJ, et al. 2011. Acremonium phylogenetic overview and revision of Gliomastix, Sarocladium, and Trichothecium.
Studies in Mycology 68: 139 –162.
Tamura K, Peterson D, Peterson N, et al. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance
and maximum parsimony methods. Molecular Biology and Evolution 28:
2731– 2739.
Taylor JW, Jacobson DJ, Kroken S, et al. 2000. Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology 31: 21–32.
Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the
sensitivity of progressive multiple sequence alignment through sequence
weighting, position-specific gap penalties and weight matrix choice. Nucleic
Acids Research 22: 4673 – 4680.
Udagawa S. 1959. Taxonomic studies of fungi on stored rice grains. III. Penicillium group (penicillia and related genera) 2. Journal of Agricultural
Science Tokyo Nogyo Daigaku 5: 5 – 21.
Udagawa S. 1962. Microascus species new to mycoflora of Japan. Journal
of General and Applied Microbiology 8: 39 – 51.
Udagawa S, Furuya K. 1978. A new species of Microascus and its peculiar
conidial state. Mycotaxon 7: 91– 96.
Valmaseda M, Martínez T, Barrasa JM. 1986. Annellidic conidiogenesis in
Pithoascus schumacheri and redefinition of Pithoascus and related fungi.
Canadian Journal of Botany 65: 1802 –1805.
Vuillemin P. 1911. Différence fondamentale entre le genre Monilia et les
genres Scopulariopsis, Acmosporium et Catenularia. Bulletin de la Société
Mycologique de France 27: 137–152.
Wang P, Wang H, Zhao Y, et al. 2011. A case of endocarditis caused by Microascus trigonosporus. Chinese Journal of Mycology 6: 162 –165.
White TJ, Bruns T, Lee S, et al. 1990. Amplification and direct sequencing
of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand
DH, Sninsky JJ, et al. (eds), PCR protocols: a guide to methods and applications: 315 – 322. Academic Press, New York.
Zach F. 1934. Untersuchungen über einige neue Arten der Gattung Scopulariopsis Bainier. Österreichische Botanische Zeitschrift 83: 173–186.
Zukal H. 1885. Ueber einige neue Pilze, Myxomyceten und Bakterien. Verhandlungen der Zoologisch-Botanischen Gesellschaft Wien 35: 333 – 342.