Pseudobactrodesmium (Dactylosporaceae, Eurotiomycetes, Fungi) a Novel Lignicolous Genus

During our ongoing surveys of fungi on submerged wood in the Greater Mekong Subregion, we collected two new species similar to Bactrodesmium longisporum. Pseudobactrodesmium gen. nov. is introduced to accommodate the new species, P. aquaticum, P. chiangmaiensis and B. longisporum is transferred to this genus. Fasciculate conidiophores, enteroblastic conidiogenous cells and subulate to fusiform, phragmoseptate conidia with a tapering apical cell and sheath characterize the genus. Pseudobactrodesmium aquaticum has longer conidia than P. chiangmaiensis. The placement of Pseudobactrodesmium in Dactylosporaceae (Eurotiomycetes) is a novel finding based on analyses of combined LSU, SSU, ITS and RPB2 sequence data. Our study reveals that Pseudobactrodesmium is likely to be a speciose genus with different species in streams around the world.

Introduction

Dactylosporaceae accommodates ecologically and morphologically diverse genera, and was reinstated by Diederich et al. (2018) to replace Sclerococcaceae (Réblová et al., 2016). For example, the freshwater genus Cylindroconidiis has holoblastic conidiogenous cells (Yu et al., 2018), while the terrestrial genera Pseudosclerococcum and Rhopalophora are apothecial ascomycetes and dematiaceous phialidic hyphomycetes, respectively (Réblová et al., 2016; Olariaga et al., 2019). The terrestrial and marine genus Sclerococcum (= Dactylospora) has loose sporodochia with catenate conidia or apothecia-like ascomata often growing on lichens or decaying wood (Hawksworth, 1975; Jones et al., 1999; Pang et al., 2014; Pino-Bodas et al., 2017). Additionally, Fusichalara minuta, which is a dematiaceous phialidic hyphomycete, and some beetle-associated strains also cluster in this family (Vargasasensio et al., 2014; Tedersoo et al., 2017).

Aquatic hyphomycetes are a morphologically diverse and polyphyletic group (Shenoy et al., 2006; Baschien et al., 2013; Su et al., 2016). Species with similar morphological characters are difficult to identify without molecular data. Previously, identification was mostly carried out based on morphology and only a few asexual taxa have been subjected to phylogenetic studies (Goh and Hyde, 1996; Cai et al., 2002; Cai and Hyde, 2007). With more molecular data becoming available for phylogenetic analyses, numerous new combinations have been proposed to accommodate poorly documented hyphomycetous species (Lu et al., 2018; Yang et al., 2018a, b). Molecular data also demonstrated that some previously known congeneric species are now distributed in different families, e.g., Monodictys arctica in Leptosphaeriaceae (Day et al., 2006), M. capensis in Pleomonodictydaceae (Hernández-Restrepo et al., 2017), and some other Monodictys species in Parabambusicolaceae (Tanaka et al., 2015). Although the polyphyletic nature of some hyphomycetous genera were partially resolved, e.g., Dendryphion, Sporidesmium and torula-like species (Su et al., 2016), fresh collections with molecular data are still needed to obtain a natural classification of hyphomycetes.

Invalidly established by Berkeley and Broome (1865) with Sporidesmium abruptum as the type, the hyphomycetous genus Bactrodesmium was segregated from Sporidesmium, with B. abruptum as the lectotype (Hughes, 1958). Bactrodesmium is distributed worldwide with more than 48 species (Wijayawardene et al., 2017a; Index Fungorum database¹). It was regarded as a member of Dothideomycetes based on the sexual-asexual morph connection between Bactrodesmium obliquum and Stuartella suttonii (Funk and Shoemaker, 1983; Wijayawardene et al., 2017b). However, with molecular evidence, Bactrodesmium was shown to be polyphyletic, as B. gabretae clustered within Helotiales, Leotiomycetes (Koukol and Kolárová, 2010), B. cubense had affinities to Morosphaeriaceae, Dothideomycetes (Hernández-Restrepo et al., 2017) and B. pallidum clustered in Savoryellaceae, Sordariomycetes (Hernández-Restrepo et al., 2017). Recently, Bactrodesmium fasciculare was transferred to a newly established genus Pleotrichocladium in Melanommataceae (Dothideomycetes) based on molecular data and morphology (Hernández-Restrepo et al., 2017). Moreover, the generic type B. abruptum was tentatively placed in Dothideomycetes based on morphological evidence but molecular data is still lacking (Pem et al., 2019). The phylogenetic position of other species still needs to be investigated.

We are studying the freshwater fungi on submerged wood along a north–south latitudinal gradient in the Asian/Australian region (Hyde et al., 2016) and have published several papers on the Greater Mekong Subregion ([citeskum]BR90,BR88,BR87,BR89,BR85,BR86[citeekum]Zhang et al., 2011, 2012, 2013, 2014, 2016, 2017; Dong et al., 2018; Wei et al., 2018; Yu et al., 2018; Wang et al., 2019). In this study, two taxa morphologically similar to Bactrodesmium longisporum were collected from submerged wood. To clarify the classification of the two new collections, we analyzed a combined LSU, SSU, ITS and RPB2 sequence dataset and compared their morphological characters. Pseudobactrodesmium, a new genus with two new species, and one new combination are introduced. Morphologically similar genera are compared with Pseudobactrodesmium and the taxonomic placements of Bactrodesmium species are discussed.

Materials and Methods

Isolation and Morphology

The decaying wood samples were collected from freshwater streams in Chiang Mai Province, Thailand and Yunnan Province, China. Specimens were placed in zip-lock plastic bags with moist cotton or tissue paper and taken to the laboratory. Morphological observations were carried out after incubation at room temperature for 1–2 weeks. Colonies were examined using a Nikon SMZ-171 dissecting microscope. Photomicrographs were made with a Nikon ECLIPSE Ni compound microscope fitted with a Canon EOS 600D digital camera. Measurements were made with the Tarosoft (R) Image Frame Work program. Images used for figures were processed with Adobe Photoshop CS5 software (Adobe Systems, United States). Single spore isolations were made from conidia onto potato dextrose agar (PDA) at room temperature, as detailed in Chomnunti et al. (2014) and cultured as outlined by Vijaykrishna et al. (2004) and Liu et al. (2010). Herbarium specimens (dry wood with fungal material) were deposited in the herbarium of Mae Fah Luang University (MFLU), Chiang Rai, Thailand and herbarium of Cryptogams, Kunming Institute of Botany Academia Sinica (HKAS), Kunming, China. Living cultures were deposited in Mae Fah Luang University Culture Collection (MFLUCC) and Kunming Institute of Botany Culture Collection (KUMCC). Facesoffungi and Index Fungorum numbers were registered as in Jayasiri et al. (2015) and Index Fungorum (2020), respectively.

DNA Extraction, PCR Amplification and Sequencing

Fungi were grown on PDA for 20–30 days at 25°C. A Biospin Fungus Genomic DNA Extraction Kit (Bioer Technology Co., Hangzhou, China) was used to extract total genomic DNA from fresh mycelia according to the manufacturer’s instructions. DNA amplification was performed by polymerase chain reaction (PCR). LSU, SSU, ITS and RPB2 gene regions were amplified using the primer pairs LR0R/LR5, NS1/NS4, ITS5/ITS4 and RPB2-5F/RPB2-7cR, respectively (Vilgalys and Hester, 1990; White et al., 1990; Rehner and Samuels, 1994; Liu et al., 1999). The amplifications were carried out in a 25 μL reaction volume containing 9.5 μL ddH₂O, 12.5 μL 2 × PCR Master Mix, 1 μL DNA template, 1 μL each primer (10 μM). The PCR thermal cycles for the amplification of the gene regions followed the methods in Jeewon et al. (2004); Réblová et al. (2011), and Su et al. (2015). PCR products were checked on 1% agarose electrophoresis gels stained with Gel Red. The sequencing reactions were carried out by Shanghai Sangon Biological Engineering Technology and Services Co., Shanghai, China.

Phylogenetic Analyses

The qualities of raw sequences generated in this study were checked with Finch TV version 1.4.0. Based on nucleotide BLAST² and previous publications (Raja et al., 2008; Koukol and Kolárová, 2010; Réblová et al., 2012, 2016; Diederich et al., 2013; Pang et al., 2014; Boonmee et al., 2016; Su et al., 2016; Yang et al., 2016; Hernández-Restrepo et al., 2017; Pino-Bodas et al., 2017; Yu et al., 2018; Dayarathne et al., 2019; Ekanayaka et al., 2019; Olariaga et al., 2019), related sequences together with newly generated ones were selected for constructing a phylogenetic tree. All sequences used in this study are listed in Table 1. The individual datasets of LSU, SSU, ITS and RPB2 were aligned using MAFFT v. 7.409 online version (Kazutaka and Standley, 2016) and manually verified with BioEdit v.7.2.5 Biological Sequence Alignment Editor (Ibis BioSciences, CA). Phylogenetic analyses of the combined dataset (LSU, SSU, ITS and RPB2) were inferred with maximum likelihood (ML) and Bayesian inference (BI) analyses.

TABLE 1

Table 1. Taxa used in the phylogenetic analysis and their corresponding GenBank accession numbers.

A ML analysis was performed with RAxML-HPC v.8 on XSEDE in CIPRES Science Gateway (Miller et al., 2010, 2015) with 1000 rapid bootstrap replicates. The model selected for ML was GTRGAMMA. Maximum likelihood bootstrap values equal to or greater than 60% are given above or below the nodes (first value, Figure 1). Bayesian inference was conducted with MrBayes v. 3.1.2 (Huelsenbeck and Ronquist, 2001) to evaluate posterior probabilities (BPP) (Rannala and Yang, 1996) by Markov chain Monte Carlo (MCMC) sampling. The best-fit model was GTR + I + G for LSU, SSU and RPB2, and SYM + I + G for ITS. Six simultaneous Markov chains were run for one million generations and trees were sampled every 100 generation (resulting in 10000 trees). The first 2500 trees, representing the burn-in phase of the analyses, were discarded and the remaining 7500 trees were used for calculating posterior probabilities (PP) in the majority rule consensus tree (Larget and Simon, 1999). Bayesian posterior probabilities (BPP) equal to or greater than 0.95 are given above or below the nodes (second value, Figure 1).

FIGURE 1

Figure 1. RAxML tree generated from combined LSU, SSU, ITS, and RPB2 sequence data. Bootstrap support values for maximum likelihood (the first value) equal to or greater than 60% and Bayesian posterior probabilities (the second value) equal to or greater than 0.95 are given above or below the nodes. The tree is rooted to Cheilymenia stercorea (AFTOL 148) (Pezizomycetes). The ex-type strains are indicated in bold and newly generated sequences are indicated in blue. Four bactrodesmium-like species are highlighted in gray background. Symbols after generic names in Eurotiomycetes indicate the habitats of taxa as explained in the phylogram.

Phylogenetic trees were viewed with FigTree v1.4.0³,⁴ and edited using Microsoft Office PowerPoint 2007 (Microsoft Corporation, WA, United States). The new sequences were deposited in GenBank (Table 1).

Results

Phylogenetic Analyses

Combined LSU, SSU, ITS, and RPB2 gene regions were employed to explore the taxonomy of new collections. The alignment comprised 79 strains (including two new strains) with an alignment length of 4381 total characters. The RAxML analysis resulted in a best scoring likelihood tree selected with a final value for the combined dataset ln L = −39819.188166. The matrix has 2564 distinct alignment patterns, with 62% of undetermined characters or gaps. Estimated base frequencies are as follows: A = 0.256432, C = 0.229269, G = 0.279558, T = 0.234740; substitution rates AC = 1.300864, AG = 2.616909, AT = 1.328213, CG = 1.028043, CT = 6.168383, GT = 1.000000; gamma distribution shape parameter α = 0.360140.

In the phylogenetic tree (Figure 1), the two new isolates are shown in Eurotiomycetes and distantly related to Bactrodesmium cubense (Dothideomycetes), B. gabretae (Leotiomycetes), and B. obovatum and B. pallidum (Sordariomycetes). The morphologically similar genera, e.g., Bactrodesmiastrum, Dictyosporium, Digitodesmium, Distoseptispora, and Sporidesmium, have phylogenetically unrelated relationships with our new strains (Figure 1). Pseudobactrodesmium aquaticum and P. chiangmaiensis constitute a distinct clade in the family Dactylosporaceae (Figure 1).

Taxonomy

Pseudobactrodesmium H. Zhang, W. Dong & K. D. Hyde, gen. nov.

Index Fungorum number: IF557247; Facesoffungi number: FoF07525

Etymology: in reference to bactrodesmium-like morphology

Saprobic on submerged wood in freshwater or decaying wood in terrestrial habitats. Sexual morph: Undetermined. Asexual morph: Hyphomycetous. Colonies sporodochial, superficial, effuse, gregarious or scattered, brown, punctiform. Mycelium mostly immersed, composed of septate, branched, hyaline hyphae. Conidiophores macronematous, mononematous, fasciculate, compact, erect, subcylindrical, septate, usually unbranched, brown, smooth. Conidiogenous cells enteroblastic, with inconspicuous proliferations, integrated, terminal, subcylindrical, pale brown. Conidia acrogenous, solitary, dry, thin-walled, smooth-walled, clavate, subcylindrical, narrowly fusiform or subulate, euseptate, phragmoseptate, brown, often enveloped by a hyaline, spherical sheath at the apex. Apical cells elongated, tapering gradually toward the apex, with globose tuberculate apex.

Type species: Pseudobactrodesmium aquaticum W. Dong, H. Zhang & K.D. Hyde

Notes: Pseudobactrodesmium is characterized by enteroblastic conidiogenous cells and subulate or fusiform, evenly pigmented conidia with a tapering apical cell. In contrast, Bactrodesmium as typified by B. abruptum is quite distinct in producing holoblastic conidiogenous cells and clavate to fusiform, unevenly colored conidia which are mid or dark brown at the upper part and becoming paler toward the basal cell, 3- to multi-transversely septate, with very dark bands at the septa, the upper one thick and black, unequal cells, the penultimate cell much longer than any of the others (Ellis, 1971). Pseudobactrodesmium nests well within the family Dactylosporaceae in our phylogenetic tree of the combined sequence dataset (Figure 1). The unique combination of morphological characters of Pseudobactrodesmium stands apart from other existing genera in this family (Hawksworth, 1975; Ellis, 1976; Jones et al., 1999; Réblová et al., 2016; Yu et al., 2018; Olariaga et al., 2019). Pseudobactrodesmium is morphologically similar to a few dematiaceous hyphomycetous genera with long or short, septate conidia, e.g., Bactrodesmiastrum (Holubová-Jechová, 1984), Bactrodesmium (Ellis, 1971, 1976), Digitodesmium (Boonmee et al., 2016), Distoseptispora (Su et al., 2016), Scolecostigmina (Braun et al., 1999), and Sporidesmium (Su et al., 2016), but they are separated by molecular evidence (Figure 1).

Pseudobactrodesmium aquaticum W. Dong, H. Zhang & K.D. Hyde, sp. nov., Figure 2

FIGURE 2

Figure 2. Pseudobactrodesmium aquaticum (MFLU 18-1171, holotype). (a,b) Colonies on submerged wood. (c,d) Conidiophores bearing conidia. (e) Enteroblastic conidiogenous cells (arrow). (f) Conidiophore. (g–i) Conidia. (j) Conidial tips with sheaths. (k) Germinated conidium. (l) Colony on PDA (front view). (m) Colony on PDA (bottom view). Scale bars: (a) 200 μm, (b) 100 μm, (c,d,h,k) 20 μm, (e,g,i,j) 10 μm, (f) 5 μm.

Index Fungorum number: IF557248; Facesoffungi number: FoF07526

Etymology: aquaticum in reference to the aquatic habitat

Holotype: MFLU 18-1171

Saprobic on submerged wood in freshwater. Sexual morph: Undetermined. Asexual morph: Hyphomycetous. Colonies sporodochial, superficial, effuse, gregarious or scattered, brown, punctiform. Mycelium mostly immersed, composed of septate, branched, hyaline hyphae. Conidiophores 26–38 × 3–4.5 μm ($\overline{x}$ = 34 × 3.8 μm, n = 10), macronematous, mononematous, fasciculate, compact, erect, subcylindrical, the apex slightly wider than the base, septate, slightly constricted at septa, usually unbranched, brown, smooth. Conidiogenous cells enteroblastic, with inconspicuous proliferations, integrated, terminal, subcylindrical, pale brown. Conidia (80–)90–105 × 6–8.5 μm ($\overline{x}$ = 95 × 7.5 μm, n = 20), acrogenous, solitary, dry, thin-walled, smooth-walled, clavate when young, subcylindrical to narrowly fusiform, or subulate when mature, straight or slightly curved, euseptate, (15–)16–19-phragmoseptate, slightly constricted and darker at septa, pale brown to brown, obscurely guttulate, wedge-shaped at basal cell, with tapering apical cells, often enveloped by a hyaline, spherical, thin, gelatinous sheath at the apex, 13–20 μm diam. Apical cells elongated, up to 6 μm long, tapering gradually toward the apex, easily becoming senescent, subhyaline, with obscured, subglobose tuberculate ends.

Culture characteristics: On PDA, colony circular, slow growing, reaching 10 mm in 50 days at 25°C, gray to brown from above, dark gray from below, surface rough, dry, raised, entire at edge.

Material examined: CHINA, Yunnan Province, Pingbian City, on submerged wood in a stream, 20 September 2017, W. Dong, WF-24A-1 (MFLU 18-1171, holotype), ex-type living culture MFLUCC 18-1015; ibid. WF-24A-2 (HKAS 101707, isotype), ex-isotype living culture KUMCC 18-0056.

Notes: Pseudobactrodesmium aquaticum is introduced as the type species of Pseudobactrodesmium having the typical euseptate, phragmoseptate conidia with apical sheath. The enteroblastic conidiogenous cells are particularly obvious in Figure 2e.

Pseudobactrodesmium chiangmaiensis X. D. Yu, W. Dong & K. D. Hyde, sp. nov., Figure 3

FIGURE 3

Figure 3. Pseudobactrodesmium chiangmaiensis (MFLU 18-0994, holotype). (a) Colonies on submerged wood. (b,c) Conidiophores bearing conidia. (d) Conidial tips with sheaths (arrow). (e) Apex of conidiophores. (f–h) Conidia. (i) Colony on PDA (front view). (j) Colony on PDA (bottom view). Scale bars: (a) 500 μm, (b,g,h) 20 μm, (c,d) 30 μm, (e) 10 μm, (f) 50 μm.

Index Fungorum number: IF557249; Facesoffungi number: FoF07527

Etymology: name reflects Chiang Mai, from where the species was collected

Holotype: MFLU 18-0994

Saprobic on submerged wood in freshwater. Sexual morph: Undetermined. Asexual morph: Hyphomycetous. Colonies sporodochial, superficial, effuse, gregarious or scattered, dark brown to black, punctiform. Mycelium mostly immersed, composed of septate, branched, hyaline hyphae. Conidiophores 15–23 × 2.5–4 μm ($\overline{x}$ = 21.5 × 3.5 μm, n = 10), macronematous, mononematous, fasciculate, compact, erect, subcylindrical, septate, slightly constricted at the septa, usually unbranched, brown, smooth. Conidiogenous cells enteroblastic, with inconspicuous proliferations, integrated, terminal, subcylindrical, pale brown. Conidia 40–90 × 5.5–8.5 μm ($\overline{x}$ = 70 × 7 μm, n = 50), acrogenous, solitary, dry, thin-walled, smooth-walled, clavate when young, subcylindrical to narrowly fusiform, or subulate when mature, straight or slightly curved, euseptate, 6–19-phragmoseptate, slightly constricted and darker at septa, pale brown to brown, obscurely guttulate, wedge-shaped at basal cell, with tapering apical cells, often enveloped by a hyaline, spherical, thin, gelatinous sheath at the apex, 17–21 μm diam. Apical cells elongated, up to but rarely 16 μm long, tapering gradually toward apex, subhyaline, with subglobose tuberculate ends.

Culture characteristics: On PDA, colony circular, reaching 15 mm in 20 days at 25°C, dark gray to dark brown from above, dark gray to black from below, surface rough, dry, raised, margin entire.

Material examined: Thailand, Chiang Mai Province, on submerged wood in a stream, 9 February 2018, X.D. Yu, Y11 (MFLU 18-0994, holotype), ex-type living culture MFLUCC 18-0982.

Notes: Pseudobactrodesmium chiangmaiensis differs from P. aquaticum in having shorter conidia (40–90 × 5.5–8.5 μm vs. (80–)90–105 × 6–8.5 μm), longer apical cells (up to 16 μm vs. up to 6 μm), as well as darker colonies on the host (dark brown to black vs. brown). The conidial sheaths are obscure in P. chiangmaiensis when mounted in water, while they are easily observed in P. aquaticum. This is probably because the specimens were senescent which led the sheaths to deliquesce. In our phylogenetic tree, P. chiangmaiensis groups with P. aquaticum with strong bootstrap support (100% MLBS, 1.00 PP, Figure 1). However, a comparison of sequence data between P. chiangmaiensis and P. aquaticum shows a difference of 6, 7, 20, and 32 nucleotides in LSU, SSU, ITS, and TEF gene regions, respectively. This indicates that they are distinct species according to guidelines of Jeewon and Hyde (2016).

Pseudobactrodesmium longisporum (M.B. Ellis) W. Dong & K.D. Hyde, comb. nov.

Index Fungorum number: IF557250; Facesoffungi number: FoF07466

≡ Bactrodesmium longisporum M.B. Ellis, More Dematiaceous Hyphomycetes (Kew): 68 (1976)

≡ Stigmina longispora (M.B. Ellis) S. Hughes, N. Z. Jl Bot. 16(3): 353 (1978)

= Bactrodesmium stilboideum R. F. Castañeda & G. R. W. Arnold, Revta Jardín bot. Nac., Univ. Habana 6(1): 48 (1985)

≡ Stigmina longispora var. stilboidea (R. F. Castañeda & G. R. W. Arnold) J. Mena & Mercado, Reporte de Investigacion del Instituto de Ecología y Sistemática, Academia de Ciencias de Cuba, Ser. Bot. 17: 10 (1987)

Holotype: On dead wood of Alnus sp. in Great Britain (IMI 63746 B)

Known distribution: New Zealand (Hughes, 1978), Australia (Vijaykrishna and Hyde, 2006), Brazil (Barbosa and Gusmão, 2011; Barbosa et al., 2013; Santa Izabel and Gusmão, 2016, 2018), Cuba (Castañeda Ruiz and Arnold, 1985), Great Britain (Ellis, 1976), Hong Kong, China (Wong and Hyde, 2001), India (Prabhugaonkar, 2011), Venezuela (Castañeda Ruiz et al., 2009), México (Heredia et al., 2018), Peru (Shearer et al., 2015), Philippines (Cai et al., 2003), South Africa (Hyde et al., 1998), Thailand (Hu et al., 2010; this study), United States (Raja et al., 2007).

Notes: Bactrodesmium longisporum was described by Ellis (1976) with a line-drawing. It was subsequently synonymized with Stigmina longispora by Hughes (1978) who observed percurrently proliferating conidiophores in old specimens from New Zealand. Bactrodesmium stilboideum is another synonym listed in Index Fungorum database. However, they can be distinguished by the aggregation of conidiophores (synnematous in B. stilboideum vs. mononematous, fasciculate conidiophores in B. longisporum) (Ellis, 1976; Castañeda Ruiz and Arnold, 1985).

A Thai strain of B. longisporum (NBRC 104945) clustered with Pseudobactrodesmium chiangmaiensis (MFLUCC 18-0982) in our phylogenetic tree (Figure 1). A comparison of sequence data between NBRC 104945 and MFLUCC 18-0982 shows a difference of 2, 281, 5 nucleotides in LSU, SSU and ITS gene regions, respectively (NBRC 104945 has 3 major insertions spanning over 281 nucleotides in SSU gene). In this study, we name NBRC 104945 as Pseudobactrodesmium sp. until its morphological characters are established to formally name this isolate. Five additional strains with only ITS2 sequence data are named as Bactrodesmium longisporum in GenBank. However, their status should be treated with caution as they represent OTUS from a metagenomic study of a heap leaching system (Hu et al., 2015) and further evidence of conspecificity is needed.

Unfortunately, the holotype specimen of B. longisporum (IMI 63746 B), does not exist in herbarium IMI.⁵ According to protologue description of the holotype (Ellis, 1976), B. longisporum (IMI 63746 B) has similar conidial size to P. chiangmaiensis (MFLU 18-0994) (50–80 × 7–8 μm in former vs. 40–90 × 5.5–8.5 μm in latter). However, P. chiangmaiensis has elongated apical cells (up to 16 μm long) with subglobose tuberculate ends, which were not described and drawn in protologue of B. longisporum (Ellis, 1976). The conidiophores of B. longisporum are up to 50 μm long, but only 15–23 μm long in P. chiangmaiensis. The size of apical sheath of B. longisporum is also unclear. Thus, we treat them as different species and synonymize B. longisporum under Pseudobactrodesmium as the third species in the genus. Epitypification of Pseudobactrodesmium longisporum is needed using a collection from its type locality.

Discussion

Bactrodesmium longisporum has been recorded as having a worldwide distribution, however these records have not been verified with molecular data. The type of B. longisporum also appears to be lost and therefore its identity cannot be verified. We therefore designate our new species of Pseudobactrodesmium from China as the generic type, describe a second species from Thailand and transfer Bactrodesmium longisporum to the new genus. However, it is likely that many collections of this species have been misidentified and as more collections are made from different countries, we would expect Pseudobactrodesmium to become speciose.

Bactrodesmium is a complex genus in need of extensive taxonomic reassessment. Pem et al. (2019) reviewed the holotype material of Bactrodesmium abruptum (≡ Sporidesmium abruptum) and tentatively placed the generic type in Dothideomycetes incertae sedis based on morphology. Both B. cubense and B. obovatum produce clavate or obovate conidia with darker septa and unequal cells, similar to the type species B. abruptum (Ellis, 1971; Zucconi and Lunghini, 1997). However, our phylogenetic study shows that they belong to different classes, Dothideomycetes and Sordariomycetes, respectively (Figure 1). Bactrodesmium gabretae differs from B. abruptum by its transversely or occasionally oblique, distoseptate conidia, and phylogenetically clustered in Leotiomycetes (Figure 1). Bactrodesmium pallidum is different from B. abruptum but similar to our new genus Pseudobactrodesmium in conidial shape (Ellis, 1959), and phylogeny places this species in Sordariomycetes (Figure 1). Our phylogenetic study is in agreement with the studies of Koukol and Kolárová (2010) and Hernández-Restrepo et al. (2017).

Although molecular data of B. abruptum is still missing, the working hypothesis of Bactrodesmium sensu stricto in Dothideomycetes provides further evidence for the introduction of Pseudobactrodesmium. Pseudobactrodesmium shares some morphological characters with Digitodesmium in having acrogenous, long, transversely septate conidia with a hyaline sheath at the apex (Kirk, 1981; Boonmee et al., 2016). However, the semi-macronematous, moniliform conidiophores and digitate conidia of Digitodesmium are clearly distinguishable from the macronematous, subcylindrical conidiophores and subcylindrical to narrowly fusiform, or subulate conidia of Pseudobactrodesmium. Phylogeny also segregates them into different classes, viz. Pseudobactrodesmium in Eurotiomycetes, and Digitodesmium in Dothideomycetes (Tsui et al., 2006; Boonmee et al., 2016; this study). The conidia of Scolecostigmina are superficially similar to those of Pseudobactrodesmium, but the former is characterized by conspicuously annellate conidiogenous cells, thick-walled, smooth to verrucose conidia occasionally with a few longitudinal or oblique septa or a few intermixed distosepta, contrasting with inconspicuously proliferating conidiogenous cells and thin-walled, smooth, transversely phragmoseptate conidia with a hyaline, spherical sheath at the apex in Pseudobactrodesmium (Braun et al., 1999; Crous et al., 2013). Scolecostigmina, typified by S. mangiferae, clustered in Capnodiales (Dothideomycetes) (Crous et al., 2013), while Pseudobactrodesmium clustered in Dactylosporaceae (Eurotiomycetes). Pseudobactrodesmium longisporum is superficially similar to Gangliostilbe malabarica in the conidial shape and apical sheath, but the synnemata and apically rounded conidia of the latter can easily be separated from the former (Xia et al., 2015). These characters of G. malabarica are also distinguished from those in the collection of Castañeda Ruiz and Arnold (1985) bearing the name Bactrodesmium stilboideum.

It is challenging to reconstruct the phylogeny of Bactrodesmium considering lack of living cultures of B. abruptum. The species having clavate or obovate, long or short, transversely septate conidia with or without apical sheath are common and scattered in different groups (Ellis, 1976; Hughes, 1978; Holubová-Jechová, 1984; Braun et al., 1999; Koukol and Kolárová, 2010; Crous et al., 2013; Xia et al., 2015; Boonmee et al., 2016; Su et al., 2016; Hernández-Restrepo et al., 2017; Videira et al., 2017). These groups of fungi are morphologically similar and therefore molecular characters are of crucial importance to clarify their taxonomy. The sequence data of B. abruptum is needed in the future to clarify the natural classification of Bactrodesmium.

Data Availability Statement

The datasets generated for this study can be found in the NCBI GenBank: MN335230, MN335226, MN335228, MN335229, MN335225, and MN335227.

Author Contributions

WD conducted the experiments, analyzed the data, and wrote the manuscript. KH planned the experiments. MD analyzed the data. X-DY conducted the experiments. DB and RJ revised the manuscript. SB funded the experiments. G-NW conducted the experiments. SN planned the experiments. HZ planned the experiments, analyzed the data, and wrote the manuscript. All authors revised the manuscript.

Funding

This work was mainly supported by National Natural Science Foundation of China (Project ID: NSF 31500017 to HZ), Yunnan young and middle aged academic and technical leaders reserve talents (Project ID: 2018HB008). KH thanks the Foreign Experts Bureau of Yunnan Province, Foreign Talents Program (2018; grant no. YNZ2018002), Thailand Research grants entitled Biodiversity, phylogeny and role of fungal endophytes on above parts of Rhizophora apiculata and Nypa fruticans (grant no: RSA5980068), the future of specialist fungi in a changing climate: baseline data for generalist and specialist fungi associated with ants, Rhododendron species and Dracaena species (grant no: DBG6080013), Impact of climate change on fungal diversity and biogeography in the Greater Mekong Subregion (grant no: RDG6130001). KH also thanks Chiang Mai University for the award of visiting Professor. MD would like to thank the 5th batch of Postdoctoral Orientation Training Personnel in Yunnan Province (grant no: Y934283261) and the 64th batch of China Postdoctoral Science Foundation (grant no: Y913082271). SB would like to thank the National Research Council of Thailand (No. 61215320023).

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

WD would like to thank Prof. Eric H. C. McKenzie for correcting English on manuscript. RJ thanks Mae Fah Luang University and University of Mauritius for support.

Footnotes

1. ^ http://www.indexfungorum.org/names/Names.asp
2. ^ http://www.ncbi.nlm.nih.gov/
3. ^ http://tree.bio.ed.ac.uk/
4. ^ http://jebl.sourceforge.net/
5. ^ http://www.herbimi.info/herbimi/results.htm?name=Bactrodesmium%20longisporum

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