Peronosporomycetes (Oomycota) from a Middle Permian
Permineralised Peat within the Bainmedart Coal
Measures, Prince Charles Mountains, Antarctica
Ben J. Slater1*, Stephen McLoughlin2, Jason Hilton1
1 School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham, United Kingdom, 2 Department of Paleobiology, Swedish
Museum of Natural History, Stockholm, Sweden
Abstract
The fossil record of Peronosporomycetes (water moulds) is rather sparse, though their distinctive ornamentation means
they are probably better reported than some true fungal groups. Here we describe a rare Palaeozoic occurrence of this
group from a Guadalupian (Middle Permian) silicified peat deposit in the Bainmedart Coal Measures, Prince Charles
Mountains, Antarctica. Specimens are numerous and comprise two morphologically distinct kinds of ornamented oogonia,
of which some are attached to hyphae by a septum. Combresomyces caespitosus sp. nov. consists of spherical oogonia
bearing densely spaced, long, hollow, slender, conical papillae with multiple sharply pointed, strongly divergent, apical
branches that commonly form a pseudoreticulate pattern under optical microscopy. The oogonia are attached to a parental
hypha by a short truncated stalk with a single septum. Combresomyces rarus sp. nov. consists of spherical oogonia bearing
widely spaced, hollow, broad, conical papillae that terminate in a single bifurcation producing a pair of acutely divergent
sharply pointed branches. The oogonium bears a short truncate extension where it attaches to the parental hypha. We
propose that similarities in oogonium shape, size, spine morphology and hyphal attachment between the Permian forms
from the Prince Charles Mountains and other reported Peronosporomycetes from Devonian to Triassic strata at widely
separated localities elsewhere in the world delimit an extinct but once cosmopolitan Palaeozoic to early Mesozoic branch of
the peronosporomycete clade. We name this order Combresomycetales and note that it played an important role in late
Palaeozoic and early Mesozoic peatland ecosystems worldwide.
Citation: Slater BJ, McLoughlin S, Hilton J (2013) Peronosporomycetes (Oomycota) from a Middle Permian Permineralised Peat within the Bainmedart Coal
Measures, Prince Charles Mountains, Antarctica. PLoS ONE 8(8): e70707. doi:10.1371/journal.pone.0070707
Editor: Carles Lalueza-Fox, Institut de Biologia Evolutiva - Universitat Pompeu Fabra, Spain
Received April 11, 2013; Accepted June 20, 2013; Published August 2, 2013
Copyright: ß 2013 Slater et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The Australian Antarctic Division provided financial and logistical support for collection of the specimens via Antarctic Science Advisory Council Project
509. This research forms part of a doctoral investigation by BJS supported by the Natural Environment Research Council (NE/H5250381/1 to BJS) and the
Synthesys program of the EU to support research on museum collections (SE-TAF-4827 to BJS). SM acknowledges funding support from the Swedish Research
Council (VR) and the Australian Research Council (Linkage) grants. The funders had no role in study design, data collection and analysis, decision to publish, or
preparation of the manuscript. (http://www.nerc.ac.uk/; http://www.synthesys.info/; http://www.vr.se/inenglish.4.12fff4451215cbd83e4800015152.html; http://
www.arc.gov.au/)
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: bxs574@bham.ac.uk
(Phytophthora infestans), sudden oak death (Phytophthora ramorum),
blister rusts and downy mildews [4]. They are currently
responsible for the widespread larch dieback seen in Larix decidua
in the UK and northern Europe [4,7–10], major damage to
tropical commercial plant species [11], and extensive death of
selected plants in temperate forests and heathlands in the Southern
Hemisphere [12,13]. Peronosporomycetes are capable of reproducing both asexually and sexually [4,14]. Asexual reproduction
initiates with the formation of a zoosporangium, from which
primary and secondary bi-flagellated motile zoospores are
released. When reproducing sexually, the male nuclei are injected
directly into the oogonium [14,15]. Zoospores achieve dispersal by
means of flagellar propulsion through water films either in soil
pore water or on the surface of plants and can also spread through
overland flow into fluvial and lacustrine environments. Dispersal
is, therefore, favoured in moist, damp environments where the
zoospores gravitate towards chemical attractants released by plants
such as amino acids, sugars, ethanol and acetaldehyde [16].
Introduction
The Peronosporomycetes (also known as Oomycota or water
moulds) are a class of organisms belonging to the phylum
Heterokontophyta, which also includes autotrophs such as diatoms
and brown algae [1–3]. Due to superficial similarities in their
filamentous morphology, spore-like oogonia (egg-containing sacs)
and life habits, the Peronosporomycetes have in the past been
grouped with the true fungi [4]. However, they can be
distinguished by the morphology of the motile stage of their life
cycle, in which the zoospores possess two differently shaped
flagella used for propulsion; a lateral whip flagellum and a onehaired tinsel flagellum [5]. Peronosporomycetes differ fundamentally from true fungi on a cellular level since their cell walls are
composed of cellulose and hydroxyproline as opposed to chitin
[4,5], and the cell nuclei contained in the hyphae-like filaments are
diploid as opposed to haploid in true fungi [4].
Peronosporomycetes are saprotrophs or parasites [6]. Some are
major plant and animal pathogens in modern ecosystems that are
responsible for well-known plant diseases, such as potato blight
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Krings et al. [5] reviewed the fossil record of the Peronosporomycetes and concluded that all the reported occurrences of this
group older than Devonian are dubious or inconclusive. Confident
Palaeozoic and early Mesozoic records are restricted to a small
number of occurrences in Devonian, Carboniferous and Triassic
permineralised peats and sinter deposits [4,17]. These include the
Devonian Rhynie Chert [18,19], Carboniferous coal balls from
the lower coal measures of the UK [20–22], Upper Mississippian
cherts from France [23], the Upper Pennsylvanian Grand-Croix
cherts of France [24], and Middle Triassic silicified peats from the
Fremouw Peak locality in the Transantarctic Mountains of central
Antarctica [17]. Similar unpublished spinose spore-like bodies are
also known from the Upper Triassic of Hopen, Svalbard
Archipelago, but are attributed to Ascomycetes (C. Strullu and
S. McLoughlin unpublished data). Multilayered oogonium-like
structures possibly attributable to Peronosporomycetes have also
been reported from a Jurassic hot spring deposit in Patagonia,
Argentina [25]. Other possible examples of Peronosporomycetes
have been documented from amber [26–29]. However, it is
difficult to confidently resolve the affinity of those examples. It has
been suggested that outgrowths from a Lower Pennsylvanian
fungal sporocarp from Great Britain could represent an example
of saprotrophic Peronosporomycetes [30]. A possible perononsporomycete affinity has been suggested for some acritarchs [5,31]
based on similarities in their morphology to oogonia of some
extant water moulds.
Their sparse fossil record is unfortunate for understanding the
evolution of feeding guilds and energy flow within terrestrial
communities, since the Peronosporomycetes are important
decomposers and parasites in modern ecosystems, particularly in
damp soils and freshwater habitats [32], and are also present in the
marine realm [33]. Peronosporomycetes are also significant in a
broader evolutionary context since they are possibly among the
earliest differentiated lineages of eukaryotes based on phylogenetic
analyses of molecular data (e.g. [31,34–36]).
The Permian cherts (silicified peats) of the Prince Charles
Mountains contain a range of microbial elements within a
glossopterid- and cordaitalean- (gymnosperm) dominated mire
palaeoecosystem [37,38]. The microbial remains are preserved in
exquisite cellular detail and retain morphological characters that
are not preserved outside of Konservat-Lagerstätten, fossil-bearing
deposits with exceptional fidelity of preservation [39]. Microscopic
remains within the permineralised peat include delicate organs
such as fungal hyphae, spores, and invertebrate exoskeleton parts
[38,40,41]. Some of these fragile organs are even found within
invertebrate coprolites preserved within the peat matrix or inside
plant tissues [42]. Here we describe two new forms of
peronosporomycete oogonia from the Toploje Member chert of
the Prince Charles Mountains that are distinguished from each
other primarily by differences in the length and density of the
branched external spines. The addition of Peronosporomycetes to
the inventory of preserved elements in the fossil community from
the Prince Charles Mountains expands the known biodiversity and
trophic guilds of the high-latitude peat-forming forests of the
Permian.
by numerous cycles of thickly bedded sandstones, siltstones and
coal seams deposited in an alluvial valley dominated by braided
rivers [41,43,45]. The cyclicity of the Bainmedart Coal Measures
sedimentary facies has been attributed to climatically triggered
fluctuations in sediment supply related to Milankovitch cycles [45].
The cause of silicification in the uppermost Toploje Member has
not been resolved but appears to be related to geochemical
changes in the surface layers of the peat during lacustrine
drowning of the mire accompanying deposition of the overlying
sideritic–limonitic Dragons Teeth Member [43,45]. Palynostratigraphic evidence indicates the silicified peat bed is of Roadian to
Wordian age [46]. The coals of the lower Bainmedart Coal
Measures are of sub-bituminous rank but organic remains within
the single layer of silicified peat appear to have been entombed
rapidly and shielded from significant compression or thermal
alteration [38].
The Amery Group was deposited within a series of half-grabens
that constitute the Lambert Graben complex [44,47,48], which
was a southern extension of the Mahanadi Graben of eastern India
before Gondwanan breakup [41,47,49–51]. The Prince Charles
Mountains were situated at a palaeolatitude of 65–70uS during the
Middle Permian [52]. The silicified peats, therefore, provide a
snapshot of a high-latitude mire community that was likely subject
to significant seasonal variation in environmental parameters.
The taphonomy of the silicified peat layer was discussed in
detail by Slater et al. [41]. The peat includes a range of plant
remains dominated by Glossopteris and Noeggerathiopsis (glossopterid
and cordaitalean gymnosperms, respectively), herbaceous lycophytes and ferns. The community likely represents a raised
(ombrotrophic) forest-mire ecosystem based on the substantial
thickness of individual coal seams in the Bainmedart Coal
Measures, together with the occurrence in the coal of significant
quantities of charcoal, fungi and coprolites [42] but minimal
siliciclastic components [41].
Materials and Methods
Ethics
All necessary permits were obtained for the described study
from the Australian Antarctic Division and Australian National
Antarctic Research Expeditions program, which complied with all
relevant regulations. Specimens are held in the palaeobotannical
collections at the Swedish Museum of Natural History (Naturhistoriska riksmuseet), Frescativägen 40, 114 18, Stockholm. Specimen numbers of the material described in this study are; NRM
S097800-01, NRM S087932-01, NRM S087932-01-02, NRM
S088053-01, NRM S088061-01, NRM S088072-01.
Thirty-five thin sections of the chert were prepared for the
analysis of diminutive components of the peats because this
method has been shown to reveal greater optical detail of many
microbial components than obtainable using the acetate peel
technique (see [53]). Images were processed and figures compiled
using Adobe Photoshop and Illustrator CS4 graphics packages.
Peronosporomycetes was reclassified by Dick et al. [54], however
it is important to note that the alternative names for this clade
(Oomycetes and Oomycota) are in common circulation in the
scientific literature [1,17]. Although these organisms are not true
fungi, their morphological features are still described using
mycological terminology. Therefore, this report will describe the
hyphae-like filaments as hyphae for consistency with other current
literature.
Geological Setting and Stratigraphic Age
Samples of silicified peat were obtained from a 3-km-long
outcrop of chert in the northern Prince Charles Mountains, East
Antarctica (see Slater et al. [41] fig. 1 for a map of the sampled
locality). The silicified interval is ca 40 cm thick and caps a coal
seam representing the topmost bed of the Toploje Member within
the Bainmedart Coal Measures, the middle unit of the PermoTriassic Amery Group [43,44]. The Amery Group is characterised
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Figure 1. Combresomyces caespitosus sp. nov. (Peronosporomycetes: Combresomycetales); Oogonium morphotype with dense
coverage of spines. A. NRM S087932-01-02, scale = 50 mm; B. NRM S087800-01, scale = 50 mm; C. NRM S088061-01 oogonium lies within a large
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coprolitic mass, scale = 100 mm; D. S087800-01, scale = 50 mm; E. NRM S088072-01, arrow indicates position of a possible fragment of hypha
extending from oogonium, scale = 100 mm; F. S087800-01, scale = 50 mm; G. S087800-01, scale = 50 mm; H. NRM S087800-01 (holotype specimen),
arrow indicates truncate extension with attached subtending hyphae, scale = 100 mm; I. NRM S087932-01-02, scale = 50 mm; J. NRM S087800-01,
arrow indicates indeterminate spherical internal contents of oogonium, scale = 100 mm; K. NRM S087800-01, enlargement of wall and ornament of
oogonium in image J, scale = 50 mm; L. NRM S087800-01, scale = 100 mm; Arrows in images A–C and G indicate interlocking ornamentation.
doi:10.1371/journal.pone.0070707.g001
Combresomyces caespitosus sp. nov. B. J. Slater, S. McLoughlin et J.
Hilton.
Nomenclature
The electronic version of this article in Portable Document
Format (PDF) in a work with an ISSN or ISBN will represent a
published work according to the International Code of Nomenclature for algae, fungi, and plants, and hence the new names
contained in the electronic publication of a PLOS ONE article are
effectively published under that Code from the electronic edition
alone, so there is no longer any need to provide printed copies. In
addition, new names contained in this work have been submitted
to MycoBank from where they will be made available to the
Global Names Index. The unique MycoBank number can be
resolved and the associated information viewed through any
standard web browser by appending the MycoBank number
contained in this publication to the prefix http://www.mycobank.
org/MycoTaxo.aspx?Link = T&Rec = . The online version of this
work is archived and available from the following digital
repositories: PubMed Central, LOCKSS.
Holotype
NRM S087800-01 (Figure 1, image H).
Type Locality, Stratum and Age
Grid reference 70u499190S, 68u039540E (elevation 162 m),
1.4 km east of Radok Lake, northern Prince Charles Mountains,
Antarctica; uppermost Toploje Member, Bainmedart Coal Measures; Middle Permian (Roadian to Wordian).
Etymology
Latin – tufted or clumped; referring to the tufted branches that
cap papillae.
MycoBank number: 803924.
Diagnosis
Results: Systematic Palaeontology
Spherical oogonia having a main body ,95 mm in diameter,
bearing 6–20 mm long, hollow, slender, conical papillae with at
least two orders of strongly divergent, sharply pointed, apical
branches. Oogonium attached via a short stalk with single septum
to parent hypha 21 mm wide. Papillae spaced 10–20 mm apart.
Kingdom Straminipila M.W. Dick, 2001[a] [4]
Phylum Heterokonta Cavalier-Smith, 1986 [55]
Subphylum Peronosporomycotina M.W. Dick, 2001[a] [4]
Class Peronosporomycetes M.W. Dick, 2001[a] [4]
Order Combresomycetales order nov. B. J. Slater, S.
McLoughlin et J. Hilton, 2013
MycoBank number: 804720
Description
The oogonia are spherical with a surface ornamentation
consisting of hollow, regularly and densely spaced papillae, which
bifurcate at least twice to form a multi-branched terminal crown
(Figure 1; Images A–L). This ornamentation interlocks to give the
impression of a reticulum in light microscopic examination of
some specimens (Figure 1; Images A–C, G). The main body of the
oogonium is 40–95 mm in diameter. The wall is 4–15 mm thick.
Sculptural elements (papillae and their crowns) are 5–7 mm in
basal width and 6–20 mm tall, of which 3–10 mm is the branched
crown. The papillae apices bifurcate twice typically and have
sharp tips. Papillae are spaced 10–20 mm apart.
None of the specimens demonstrates a connection to a
widespread network of aseptate hyphae that is present in the
peat, although one specimen is connected to a 32 mm long solitary
parental hypha. This parental hypha is 21 mm wide and attaches
via a septum to a truncate basal extension of the main oogonium
body (Figure 1; Image H). Other oogonia have truncate extensions
or breaks in the ornament where the parental hypha presumably
attached. It is difficult to discern whether the oogonia have any
preserved contents; some specimens house indistinct structures
that may represent degraded oospores (Figure 1; Image J) but their
identity is inconclusive. Antheridia have not been conclusively
identified.
Diagnosis
Peronosporomycetes with oogonia having robust ancyrate
sculptural elements.
Remarks
The new order differs from other groups of equivalent rank in
the Peronosporomycetes by the thick wall and robust ancyrate
sculptural elements on the oogonia. Oogonia of the Peronosporales and Pythiales may have punctate, papillate, verrucate or
simple spinose ornamentation, but none is known to have complex
branched sculptural elements [56]. The new order contains a
single extinct family diagnosed below.
Family Combresomycetaceae fam. nov. B. J. Slater, S.
McLoughlin et J. Hilton, 2013
MycoBank number: 804721.
Diagnosis
Combresomycetales with oogonia having one to two orders of
terminal branching on the conical sculptural elements.
Etymology for Order and Family
Derived from the type genus Combresomyces.
Genus Combresomyces Dotzler N, Krings M, Agerer R, Galtier J
et Taylor TN 2008 [57].
Remarks
This form occurs dispersed throughout the silicified peat matrix
in approximately 50% of the studied thin-sections. It is particularly
found in association with accumulations of plant debris around
Vertebraria (glossopterid roots) and matted leaf deposits of Glossopteris
and Noeggerathiopsis.
Type Species
Combresomyces cornifer Dotzler N, Krings M, Agerer R, Galtier J et
Taylor TN 2008 [57]; upper Viséan; central France.
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Although known to have a conservative morphology spanning
the Pennsylvanian to Middle Triassic [17], Combresomyces oogonia
show subtle differences in size and ornamentation between
assemblages of different stratigraphic age. Combresomyces caespitosus
sp. nov. differs from Combresomyces cornifer [57] and Combresomyces
williamsonii [58] in several respects including slightly denser
ornamentation, which abuts or interlocks to form a pseudo
reticulum. This feature is not seen in either C. cornifer [57] or C.
williamsonii [58], in which the tips of the ornament remain widely
spaced. The oogonia of C. caespitosus are larger than specimens of
C. cornifer from the Pennsylvanian (,40 mm in diameter: [57]) but
smaller than the large oogonia of C. cornifer known from the Middle
Triassic (up to 110 mm in diameter: [17]). The wall of the
oogonium in C. caespitosus is generally thicker (4–15 mm) than that
of both C. cornifer (described as ca 1 mm [57]) or C. williamsonii
(described as thin-walled [58]), and the truncate attachment to the
parental hypha in Combresomyces caespitosus sp. nov. protrudes
further from the main body of the oogonium.
The dense multi-branched spines of Combresomyces caespitosus
oogonia, though markedly smaller, show remarkable similarities in
basic morphology to the branched ornamentation of some
lycophyte megaspores found in the same beds (see Singhisporites
hystrix [41]). These similarities might be due functional parallels
between these organs as biological dispersive units. The increased
surface area generated by densely ramified appendages might have
conferred improved buoyancy for dispersal of both megaspores
and oogonia in Permian wetland settings [17], or have provided a
favourable mechanism for attachment of these structures to other
materials (e.g., plant debris in the case of the peronosporomycete
saprotroph, or conspecific microspores in the case of the lycophyte
megaspores, or even attachment to arthropod distributers).
Surface sculptures of a broadly similar morphology occur in many
unrelated groups and likely performed an important biological
function in life (e.g. [59]).
Combresomyces rarus sp. nov. B. J. Slater, S. McLoughlin et J.
Hilton.
diameter with a wall 2–5 mm thick. The sculptural elements
(papillae and apical spines) are 12–20 mm in total length, of which
5–8 mm represents the apical branches. Branch apices are sharply
pointed. Papillae are 5–8 mm in basal width and spaced 15–20 mm
apart – their bases being confluent to produce intervening broad
U-shaped transverse sections of the oogonial wall.
None of the specimens demonstrates a connection to a
widespread network of aseptate hyphae found within the peat
matrix although some were found connected to short lengths of
solitary parental hypha (Figure 2; Images C, F, K). The oogonia of
the holotype specimen is connected to a 22 mm long length of
solitary parental hypha. The parental hypha is 35 mm wide and
attaches via a septum to a truncate basal extension of the main
oogonium body (Figure 2; Image F). A truncate extension marked
by a break in ornamentation is evident on some specimens
(Figure 2; Images B and H) and is interpreted to be the attachment
point between the oogonium and the parent hypha. The contents
of the oogonia are difficult to elucidate. Antheridia have not been
identified although it is notable that the length of hypha in one
specimen (Figure 2; Image K) is somewhat morphologically similar
to the outline expected if the antheridium was formed as a collarlike structure at the base of the oogonium in an amphigynous
arrangement. However, the preservation is insufficient to confirm
or refute this and we interpret the structure as a length of parental
hypha.
Remarks
This species is less abundant than Combresomyces caespitosus in the
Toploje Member chert fossil ecosystem, occurring in approximately 25% of the thin sections prepared from the peats. This
form occurs primarily in association with Vertebraria and Australoxylon (respectively, the root and stem wood of glossopterids).
Although of equivalent absolute length, the sculptural elements in
Combresomyces rarus sp. nov. are proportionally longer in relation to
the central body of the oogonium than in C. caespitosus, and the
ornament does not appear to interlink to form a pseudoreticulum.
The ornament of C. rarus is more akin to that of C. williamsonii
[58] than C. caespitosus, although the papillae are much more
widely spaced with the bases merging to form broad U-shaped
transverse sections of the oogonial wall, a feature not seen in C.
williamsonii [58]. The ornament of Combresomyces rarus is also
proportionally larger and less densely distributed than in C.
williamsonii [58].
Holotype
NRM S087932-01-02 (Figure 2, image F).
Type Locality, Stratum and Age
Grid reference 70u499540S, 68u039050E (elevation 166 m),
1.25 km east of Radok Lake, northern Prince Charles Mountains,
Antarctica; uppermost Toploje Member, Bainmedart Coal Measures; Middle Permian (Roadian to Wordian).
Discussion
We refer these fossils to the Peronosporomycetes based on their
morphological similarity to examples of this biological class known
from other late Palaeozoic and early Mesozoic assemblages, in
which oogonia are more confidently associated with hyphae, e.g.,
Combresomyces cornifer [17] and C. williamsonii [58]. Similar isolated
oogonia attributed to this group are also known from the
Pennsylvanian of France [3]. Our confidence in attributing the
fossils to the Peronosporomycetes is enhanced by several
specimens (Figure 1; Image H, Figure 2; Images C, F, K)
possessing a distinctly truncated extension from the main body of
the oogonium that attaches to the parent hypha in the same way as
specimens of Combresomyces cornifer [17]. This truncated extension is
present in some fossil examples of Peronosporomycetes and in
most extant forms, although it is absent in some [19].
Acyrate-conate fossil oogonia attributable to Peronosporomycetes vary significantly over their stratigraphic range. Earlier
forms, e.g., from the Pennsylvanian [57] are generally ,40 mm in
diameter, whereas Middle Triassic forms reach 110 mm in
Etymology
Latin – sparse; referring to the widely spaced papillae.
MycoBank number: 803925.
Diagnosis
Spherical oogonia having a main body ,65 mm in diameter,
bearing 12–20 mm long, hollow, broad, conical papillae that
terminate in at least one bifurcation producing a pair of, generally
acutely divergent, sharply pointed branches. Oogonium wall
locally bearing a short truncate extension marking attachment
point to parent hypha. Papillae spaced 15–20 mm apart.
Description
The oogonia are spherical with sparsely ornamented surfaces.
The ornamentation consists of widely spaced, robust, hollow
papillae with elongate extensions that bifurcate at least once
(Figure 2). The oogonium has a central body 38–65 mm in
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Figure 2. Combresomyces rarus sp. nov. (Peronosporomycetes: Combresomycetales); scale bars = 100 mm unless stated otherwise.
Oogonium morphotype with sparse coverage of spines; some oogonia contain indeterminate contents. A. NRM S087932-01-02; B. NRM S087932-01;
C. NRM S088053-01 arrow indicates attachment point to hyphae; D. S087932-01-02; E. S087932-01-02; F. NRM S087932-01-02 (holotype specimen)
arrow indicates attached subtending hypha; G. NRM S087800-01; H. NRM S087932-01-02; I. NRM S087932-01-02 enlargement of oogonia wall and
ornamentation, arrow indicates the hollow nature of the papillae, scale = 50 mm; J. NRM S087932-01-02 arrows indicate branched crown of
ornamentation, enlargement shown in image I, scale = 50 mm; K. NRM S087932-01-02 arrow indicates attached subtending hypha; L. NRM S08793201-02 oogonium in image K in different focal plane highlighting the nature of the ornamentation covering the oogonium surface.
doi:10.1371/journal.pone.0070707.g002
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diameter [17]. The Prince Charles Mountains examples appear to
be the first recorded Permian representatives of this group of
Peronosporomycetes and possess distinctive ancyrate-conate oogonia of an intermediate size range (38–95 mm). Schopf [60]
figured what was described as; ‘‘the spiny spore with septate
germinal tube, possibly fungal zygospore’’ (illustrated in figure J of
the Schopf paper [60]), which may be a Permian peronosporomycete, though branched ornamentation is not visible on the
original illustration. The apparently sparse fossil record of this
group may in part be attributable to the past prevalence of the
acetate peel technique in studying permineralised plant assemblages. Acetate peels have been shown to be inferior to thin
sections in revealing the microorganisms preserved in silicified
deposits [53]. Thin sections provide a greater depth of section (30–
50 mm) and reveal greater clarity of characters in a range of fungi,
fungi-like organisms and diminutive arthropods with thin-walled
tissues than is obtainable with mounted acetate peels of ca 10 mm
thickness [53,61].
Ovoid structures possibly also representing oogonia have been
reported attached to specimens of Galtierella biscalithecae from the
Upper Pennsylvanian Grand-Croix Cherts from France [3]. These
are also interpreted to be terminally inserted on the hyphae and
but are typically oblong and longer than the oogonia described
herein. Possible oogonia have also been reported from the Jurassic
San Augustı́n hot spring deposit from Patagonia, Argentina [25]
although they lack the forked spines seen in the Prince Charles
Mountains examples.
The oogonia of extant Peronosporomycetes, such as Phytophthora
[62], form terminally and have a range of morphologies from
obpyriform to ellipsoid to ovoid [63]. The two morphologies of
peronosporomycetes evident in the Toploje Member peat are both
covered in ancyrate conate/spinose ornamentation. Fossil examples of this style of ornamentation are numerous [5,17,23,58].
However, the order/family-level affinity of these bodies remains
poorly resolved. Although extant Peronosporomycetes oogonia
bear ornamentation, none appears to have complex branched
crowns on the sculptural elements, a character which is used to
distinguish the new order. Some modern Pythium oogonia have
robust spinose ornamentation [64,65], especially those of P.
oligandrum [66], [67], and P. prolatum Hendrix and Campbell [68],
but the extant forms typically lack forked apices on the spines.
Other extant forms that exhibit broadly similar robust spinose/
conate ornamentation include Aphanomyces stellatus [69], [70,71].
Among extant forms, Pythium prolatum demonstrates particular
similarities with those forms from the Toploje Member peat since
it possesses the most heavily ornamented oogonia and has a similar
truncate extension adjoining the parental hyphae [68]. It seems
likely that the various fossil forms represented by oogonia with
truncate or branched papillae (including Combresomyces, Frankbaronia
and perhaps Hassiella, Galtierella and some members of Zygosporites)
represent a widely distributed extinct late Palaeozoic to early
Mesozoic clade within the Peronosporomycetes and are here
placed in the new order Combresomycetales. This group is
distinguished by its apically branched conate to spinose ornamentation on the surface of the oogonia, but known morphological
characters are as yet insufficient to infer close a phylogenetic
relationship with any one of the extant orders of Peronosporomycetes.
Despite the poor fossil record of this extremely diverse class
(attribution of several fossil examples being equivocal due to the
difficulty in identifying diagnostic characters), the documentation
of the group’s occurrence in palaeocommunities is significant since
they are important shapers of modern ecosystems. Ancient
Peronosporomycetes, like their modern counterparts, probably
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played a significant role in recycling organic matter, via
saprotrophy, and potentially in parasitizing plants and animals
in the Permian high-latitude mire ecosystems. In terms of life habit
and ecology, both Combresomyces caespitosus sp. nov. and Combresomyces rarus sp. nov. appear likely to have occupied a saprotrophic
lifestyle. This is based on the association of the oogonia of both
species with a broad range of adjacent plant tissues. Neither C.
caespitosus nor C. rarus are consistently associated with any one plant
type in the permineralised peats, which suggests they did not have
a well-developed parasitic relationship with a particular host
species.
The recognition of robustly ancyrate-conate Peronosporomycetes oogonia in Middle Permian silicified peats helps bridge the
large (latest Carboniferous to Middle Triassic) gap in the group’s
fossil record noted by Schwendemann et al. [17] and attests to the
broad climatic tolerance of this group, spanning the palaeotropics
to cool palaeotemperate belt; fossil Peronosporomycetes oogonia
are known from palaeolatitudes as divergent as the palaeotropics
of the Viséan of central France [57,72] to the high palaeolatitudes
(ca 65u–70u S) of the Prince Charles Mountains (this study) based
on broadly accepted continental reconstructions [52,73]. Their
broad stratigraphic and palaeoclimatic distribution also suggests
that the group as a whole was not tied to particular plant hosts; the
host floras from the Carboniferous to Triassic variably being
dominated by arborescent lycophytes, glossopterids, corystosperms
and conifers [5,17,57]. This versatility with respect to plant hosts
and their distribution through the late Palaeozoic and into the
Triassic indicates that Combresomycetales were generalist or
opportunistic organisms that were little affected by the endPermian biotic crisis [74] and the disappearance of peat-forming
ecosystems for over 5 million years during the Early Triassic
[75,76].
Conclusions
Oogonia with multi-branched sculptural elements do not
appear to be represented amongst modern Peronosporomycetes
based on our survey of the literature, although published details of
oogonia and oospore morphology are admittedly sparse. Nevertheless, the obvious similarities in oogonium shape, size, process
morphology and hyphal attachment between the Permian
Antarctic forms reported here and fossils documented from the
Devonian to Triassic elsewhere in the world suggest that these
forms represent an extinct but once widespread Palaeozoic to early
Mesozoic branch of the peronosporomycete clade. A new order
and family of fossil Peronosporomycetes, Combresomycetales B. J.
Slater, S. McLoughlin et J. Hilton and Combresomycetaceae B. J.
Slater, S. McLoughlin et J. Hilton, are established on this basis.
Two new species of Combresomyces are distinguished primarily on
subtle differences in oogonium size and ornamentation. These
represent the first examples of this group documented from the
Permian of Antarctica and add to the biodiversity and trophic
levels recognised in high-latitude Permian mire ecosystems of
Gondwana. The lack of a consistent association between the
oogonia and any particular plant fossils in the permineralised peat
or of any reaction tissue in adjacent plant remains suggests that
these Combresomyces species were saprotrophs rather than parasites.
Their complex ornamentation may have been an adaptation for
aquatic dispersal or adhesion to host materials in the extensive
wetlands of the Gondwanan Permian, yet this group of elaborately
sculptured Peronosporomycetes as a whole were sufficiently
generalist in their ecology to survive the demise of peat-forming
ecosystems during the first five million years of the Triassic.
7
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Permian Antarctic Peronosporomycetes
reagents/materials/analysis tools: BJS SM JH. Wrote the paper: BJS SM
JH.
Author Contributions
Conceived and designed the experiments: BJS SM JH. Performed the
experiments: BJS SM JH. Analyzed the data: BJS SM JH. Contributed
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