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Research Article
Thyridium revised: Synonymisation of Phialemoniopsis under Thyridium and establishment of a new order, Thyridiales
expand article infoRyosuke Sugita§, Kazuaki Tanaka§
‡ Iwate University, Morioka, Japan
§ Hirosaki University, Hirosaki, Japan
Open Access

Abstract

The genus Thyridium, previously known as a saprobic or hemibiotrophic ascomycete on various plants, was revised taxonomically and phylogenetically. Sequences of the following six regions, that is, the nuclear ribosomal internal transcribed spacer (ITS) region, the large subunit (LSU) of rDNA, the second largest RNA polymerase II subunit (rpb2) gene, translation elongation factor 1-alpha (tef1) gene, the actin (act) gene, and the beta-tubulin (tub2) gene, were generated for molecular phylogenetic analyses of species of this genus. Phialemoniopsis, a genus encompassing medically important species, is synonymised with Thyridium based on molecular evidence and morphological similarities in their asexual characters. The generic concept for Thyridium is expanded to include species possessing both coelomycetous and hyphomycetous complex asexual morphs. In addition to type species of Thyridium, T. vestitum, nine species were accepted in Thyridium upon morphological comparison and molecular phylogenetic analyses in this study. All seven species of Phialemoniopsis were treated as members of the genus Thyridium and new combinations were proposed. A bambusicolous fungus, Pleospora punctulata, was transferred to Thyridium, and an epitype is designated for this species. A new species, T. flavostromatum, was described from Phyllostachys pubescens. The family Phialemoniopsidaceae, proposed as a familial placement for Phialemoniopsis, was regarded as a synonym of Thyridiaceae. A new order, Thyridiales, was established to accommodate Thyridiaceae; it forms a well-supported, monophyletic clade in Sordariomycetes.

Keywords

Ascomycota, Phialemoniopsidaceae, phylogeny, Sordariomycetes, taxonomy, Thyridiaceae

Introduction

Thyridium was originally established to accommodate species with cylindrical, uniseriate, 8-spored asci and muriform, dark-coloured, ascospores (Nitschke 1867). Species of this genus occur on various plants as saprobic or hemibiotrophic fungi (Eriksson and Yue 1989; Taylor et al. 1997; Checa et al. 2013). Currently, Thyridium includes 33 species and is placed in Thyridiaceae (family incertae sedis, Sordariomycetes; Yue and Eriksson 1987; Index Fungorum, http://www.indexfungorum.org, 2021). The type species T. vestitum has been verified to produce both coelomycetous and hyphomycetous asexual morphs, which have phialidic conidiogenous cells with collarette and ellipsoidal to allantoid hyaline conidia (Leuchtmann and Müller 1986).

Molecular information on Thyridium species is available only for two non-type strains (CBS 113027, CBS 125582) of the type species T. vestitum (Lutzoni et al. 2004; Spatafora et al. 2006; Vu et al. 2019); however, the phylogenetic relationships among species of this genus are unclear. A recent study on the phylogeny of Sordariomycetes has shown that T. vestitum is closely related to two Phialemoniopsis spp. (P. endophytica and P. ocularis), but their phylogenetic and taxonomic relationships have not been clarified (Dong et al. 2021; Hyde et al. 2021).

The genus Phialemoniopsis was placed in Phialemoniopsidaceae (Diaporthomycetidae family incertae sedis, Sordariomycetes; Hyde et al. 2021). Species of this genus are widely distributed in various environments and substrates, including industrial water, plant materials, raw sewage, and soil (Gams and McGinnis 1983; Halleen et al. 2007; Su et al. 2016). Several species have been reported from parts of the human body, such as blood, eye, toenail, skin, and sinus (Perdomo et al. 2013; Tsang et al. 2014), and some of them have also been isolated from patients with keratomycosis and phaeohyphomycosis (Perdomo et al. 2013; Desoubeaux et al. 2014). All species in this genus are known to be asexual.

In our ongoing taxonomic study of sordariomycetous fungi in Japan, several new specimens of Thyridium-like sexual morphs were collected. Single ascospore isolates from these specimens formed typical Phialemoniopsis-like asexual morphs in culture, suggesting that both genera are closely related. This study aims to reveal the taxonomic and phylogenetic relationships between Thyridium and Phialemoniopsis, and to clarify their ordinal position in Sordariomycetes.

Material and method

Isolation and morphological observation

All materials were obtained from Japan. Morphological characteristics were observed in preparations mounted in distilled water by differential interference and phase contrast microscopy (Olympus BX53) using images captured with an Olympus digital camera (DP21). All specimens were deposited in the herbarium at Hirosaki University (HHUF), Hirosaki, Japan. Single spore isolations were performed from all specimens. Colony characteristics were recorded from growth on potato dextrose agar (PDA), malt extract agar (MEA), and oatmeal agar (OA) from Becton, Dickinson and Company (MD, USA), after a week at 25 °C in the dark. Colony colours were recorded according to Rayner (1970). To observe the asexual morphs in culture, 5 mm squares of mycelial agar were placed on water agar containing sterilised plant substrates such as rice straws and banana leaves. Then these plates were incubated at 25 °C for 2 weeks in the dark. When the substrates were colonised, the plates were incubated at 25 °C under black light blue illumination for 1–2 weeks to observe sporulation.

Phylogenetic analyses

DNA was extracted from four isolates using the ISOPLANT II kit (Nippon Gene, Tokyo, Japan) following the manufacturer’s instructions. The following loci were amplified and sequenced: the internal transcribed spacer (ITS) region with primers ITS1 and ITS4 (White et al. 1990), the large subunit nuclear ribosomal DNA (LSU) with primers LR0R (Rehner and Samuels 1994) and LR5 or LR7 (Vilgalys and Hester 1990), the second largest RNA polymerase II subunit (rpb2) gene with primers fRPB2-5F and fRPB2-7cR (Liu et al. 1999), the translation elongation factor 1-alpha (tef1) gene with primers 983F and 2218R (Rehner and Buckley 2005), the actin (act) gene with primers Act-1 and Act-5ra (Voigt and Wöstemeyer 2000) and the beta-tubulin (tub2) gene with primers TUB-F and TUB-R (Cruse et al. 2002). PCR products were purified using the FastGene Gel/PCR Extraction Kit (Nippon Gene, Tokyo, Japan) following the manufacturer’s instructions and sequenced at SolGent (South Korea). Newly generated sequences were deposited in GenBank (Table 1).

Table 1.

Isolates and GenBank accessions of sequences used in the phylogenetic analyses of Sordariomycetes (Fig. 1).

Taxon Isolatea Statusb GenBank accession numbersa Ref.c
LSU rpb2 tef1
Acrodictys aquatica MFLUCC 18-0356 HT MG835712 47
Acrodictys bambusicola HSAUP myr9510 KX033564 44
Annulatascus velatisporus A70 18 AY316354 3
Annulusmagnus triseptatus CBS 128831 GQ996540 JQ429258 25, 29
Ascitendus austriascus CBS 131685 GQ996539 JQ429257 25, 29
Atractospora reticulata CBS 127884 HT KT991660 KT991649 41
Atractospora thailandensis KUMCC 16-0067 HT MF374362 MF370951 MF370962 45
Barbatosphaeria arboricola CBS 127689 HT KM492862 KM492901 38
Barbatosphaeria barbirostris CBS 121149 EF577059 KM492903 18, 38
Barbatosphaeria varioseptata CBS 137797 HT KM492869 KM492907 38
Barrmaelia rhamnicola CBS 142772 ET MF488990 MF488999 MF489009 52
Bombardia bombarda AFTOL-ID 967 DQ470970 DQ470923 DQ471095 14
Calosphaeria pulchella CBS 115999 IT AY761075 GU180661 FJ238421 8, 27
Camarops microspora CBS 649.92 AY083821 DQ470937 13, 14
Camarotella costaricensis MM-149 KX430484 KX451954 KX451982 43
Cancellidium cinereum MFLUCC 18-0424 HT MT370363 MT370486 MT370488 57
Cancellidium griseonigrum MFLUCC 17-2117 HT MT370364 MT370487 57
Ceratolenta caudata CBS 125234 HT JX066704 JX066699 33
PRM 899855 JX066705 33
Chaetosphaeria ciliata ICMP 18253 GU180637 GU180659 27
Chaetosphaeria curvispora ICMP 18255 GU180636 GU180655 27
Cryptadelphia groenendalensis SH12 EU528007 20
SMH3767 EU528001 20
Diaporthe phaseolorum NRRL 13736 U47830 1
Distoseptispora obpyriformis MFLUCC 17-1694 HT MG979764 MG988415 MG988422 48
Distoseptispora rostrata MFLUCC 16-096 HT MG979766 MG988417 MG988424 48
Endoxyla operculata UAMH 11085 JX460992 KY931927 34, 49
Entosordaria perfidiosa CBS 142773 ET MF488993 MF489003 MF489012 52
Fluminicola aquatica MFLUCC 15-0962 HT MF374366 MF370960 45
Fluminicola saprotrophitica MFLUCC 15-0976 HT MF374367 MF370954 MF370956 45
Gnomonia gnomon CBS 199.53 AF408361 DQ470922 DQ471094 2, 14
Jobellisia fraterna SMH2863 AY346285 4
Jobellisia luteola SMH2753 AY346286 4
Lanspora coronata AFTOL-ID 736 U46889 DQ470899 14
Lasiosphaeria ovina SMH4605 AY436413 AY600284 DQ836908 6, 7, 16
Lentomitella cirrhosa ICMP 15131 ET AY761085 KM492911 11, 38
Lentomitella crinigera CBS 138678 KY931811 49
Linocarpon livistonae HKUM 6520 DQ810205 DQ810248 10
Magnaporthe salvinii M 21 JF414887 JF710406 28
Magnaporthiopsis agrostidis CBS 142740 HT KT364754 KT364756 37
Melanconis stilbostoma CBS 109778 AF408374 EU219299 EU221886 2
Myrmecridium montsegurinum JF 13180 HT KT991664 KT991654 41
Myrmecridium schulzeri CBS 100.54 EU041826 17
Myrmecridium thailandicum CBS 136551 HT KF777222 30
Neolinocarpon enshiense HKUCC 2983 DQ810221 DQ810244 10
Neolinocarpon globosicarpum HKUCC 1959 DQ810224 DQ810245 10
Ophiostoma piliferum CBS 158.74 DQ470955 DQ470905 DQ471074 14
Ophiostoma stenoceras CBS 139.51 DQ836904 DQ836891 DQ836912 16
Papulosa amerospora AFTOL-ID 748 DQ470950 DQ470901 DQ471069 14
Pararamichloridium caricicola CBS 145069 HT MK047488 46
Pararamichloridium livistonae CBS 143166 HT MG386084 54
Pararamichloridium verrucosum CBS 128.86 HT MH873621 56
Phaeoacremonium fraxinopennsylvanica M.R. 3064 HQ878595 HQ878609 26
Phaeoacremonium novae-zealandiae CBS 110156 HT AY761081 8
Phomatospora bellaminuta AFTOL-ID 766 FJ176857 FJ238345 23
Phomatospora biseriata MFLUCC 14-0832A KX549448 51
Phyllachora graminis TH-544 KX430508 43
Pleurostoma ootheca CBS 115329 IT AY761079 HQ878606 FJ238420 8, 23, 26
Pseudostanjehughesia aquitropica MFLUCC 16-0569 HT MF077559 MF135655 53
Pseudostanjehughesia lignicola MFLUCC 15-0352 HT MK849787 MN124534 MN194047 55
Pyricularia borealis CBS 461.65 DQ341511 24
Pyricularia bothriochloae CBS 136427 HT KF777238 30
Rhamphoria delicatula CBS 132724 FJ617561 JX066702 22, 33
Rhamphoria pyriformis CBS 139024 MG600397 MG600401 50
Rubellisphaeria abscondita CBS 132078 HT KT991666 KT991657 41
Sordaria fimicola CBS 723.96 AY780079 DQ368647 9, 19
Spadicoides bina CBS 137794 KY931824 KY931851 49
Sporidesmium minigelatinosa NN 47497 DQ408567 DQ435090 12
Sporidesmium parvum HKUCC 10836 DQ408558 12
Thyridium cornearis CBS 131711 HT KJ573450 LC382144 36
Thyridium curvatum CBS 490.82 HT AB189156 LC382142 15
Thyridium endophyticum ACCC 38980 HT KT799560 42
Thyridium flavostromatum KT 3891 = MAFF 247509 HT LC655963 LC655967 LC655971 This study
Thyridium hongkongense HKU39 HT KJ573447 36
Thyridium limonesiae CBS 146752 HT MW050976 58
Thyridium oculorum CBS 110031 HT KJ573449 LC382145 36
Thyridium pluriloculosum CBS 131712 HT HE599271 LC382141 32
KT 3803 = MAFF 247508 LC655964 LC655968 LC655972 This study
Thyridium punctulatum KT 1015 = MAFF 239669 LC655965 LC655969 LC655973 This study
KT 3905 = MAFF 247510 ET LC655966 LC655970 LC655974 This study
Thyridium vestitum CBS 113027 AY544671 DQ470890 DQ471058 d 5, 14
CBS 125582 MH875182 56
Tirisporella beccariana BCC 36737 JQ655450 39
Tirisporella bisetulosus BCC 00018 EF622230 21
Wongia griffinii BRIP 60377 KU850470 KU850466 40
Woswasia atropurpurea CBS 133167 HT JX233658 JX233659 31
Xylochrysis lucida CBS 135996 HT KF539911 KF539913 35
Xylolentia brunneola PRA-13611 HT MG600398 MG600402 50

Primary analysis of LSU-rpb2-tef1 sequences from 88 strains of Sordariomycetes (Table 1) was conducted to clarify the ordinal/familial placement of Thyridium (or Phialemoniopsis) species. Barrmaelia rhamnicola and Entosordaria perfidiosa (Xylariomycetidae) were used as outgroups. As a secondary analysis, single gene trees of ITS, act and tub2, and a combined tree of these three loci were generated to assess the species boundaries of 17 strains within Thyridium/Phialemoniopsis (Table 2). All sequence alignments (LSU, ITS, rpb2, tef1, act and tub2) were produced using the server version of MAFFT (http://www.ebi.ac.uk/Tools/msa/mafft), checked and refined using MEGA v. 7.0 (Kumar et al. 2016).

Table 2.

Isolates and GenBank accessions of sequences used in the phylogenetic analyses of Thyridium species (Fig. 2).

Taxon Isolatea Substrate/Host Statusb GenBank accession numbersa Ref.c
ITS act tub2
Thyridium cornearis CBS 131711 human corneal fluid HT KJ573445 HE599252 HE599301 1, 2
UTHSC 06-1465 shin aspirate HE599285 HE599253 HE599302 2
Thyridium curvatum CBS 490.82 skin lesion HT AB278180 HE599258 HE599307 2
UTHSC R-3447 human eye HE599291 HE599259 HE599308 2
Thyridium endophyticum ACCC 38979 lower stem of Luffa cylindrica (endophyte) KT799556 KT799553 KT799562 4
ACCC 38980 lower stem of Luffa cylindrica (endophyte) HT KT799557 KT799554 KT799563 4
Thyridium flavostromatum KT 3891 = MAFF 247509 dead twigs of Phyllostachys pubescens HT LC655959 LC655979 LC655975 This study
Thyridium hongkongense HKU39 the right forearm nodule biopsy of a human HT KJ573442 KJ573452 KJ573457 3
Thyridium limonesiae CBS 146752 Skin nodule HT MW050977 MW349126 MW048608 6
Thyridium oculorum CBS 110031 human keratitis HT KJ573444 HE599247 HE599296 2, 3
UTHSC 05-2527 peritoneal dialysis catheter HE599281 HE599249 HE599298 2
Thyridium pluriloculosum CBS 131712 human toe nail HT HE599286 HE599254 HE599303 2
KT 3803 = MAFF 247508 dead wood of Betula maximowicziana HT LC655960 LC655980 LC655976 This study
UTHSC 09-3589 synovial fluid HE599287 HE599255 HE599304 2
Thyridium punctulatum KT 1015 = MAFF 239669 dead culms of Phyllostachys pubescens LC655961 LC655981 LC655977 This study
KT 3905 = MAFF 247510 dead twigs of Phyllostachys nigra var. nigra ET LC655962 LC655982 LC655978 This study
Thyridium vestitum CBS 125582 MH863721 5

Phylogenetic analyses were conducted using maximum-likelihood (ML) and Bayesian methods. The optimum substitution models for each dataset were estimated using Kakusan4 software (Tanabe 2011) based on the Akaike information criterion (AIC; Akaike 1974) for ML analysis and the Bayesian information criterion (BIC; Schwarz 1978) for Bayesian analysis. ML analyses were performed using the TreeFinder Mar 2011 program (http://www.treefinder.de) based on the models selected with the AICc4 parameter (used sequence length as sample size). ML bootstrap support (ML BS) values were obtained using 1000 bootstrap replicates. Bayesian analyses were performed using MrBayes v. 3.2.6 (Ronquist et al. 2012), with substitution models selected based on the BIC4 parameter (used sequence length as sample size). Two simultaneous and independent Metropolis-coupled Markov chain Monte Carlo (MCMC) runs were performed for 9,000,000 generations for primary analysis and 1,000,000 generations for secondary analyses (except for the ITS dataset for 1,500,000 generations) with the tree sampled every 1,000 generations. Convergence of the MCMC procedure was assessed from the effective sample size scores (all > 100) using MrBayes and Tracer v. 1.6 (Rambaut et al. 2014). First 25% of the trees were discarded as burn-in, and the remainder were used to calculate the 50% majority-rule trees and to determine the posterior probabilities (PPs) for individual branches. These alignments were submitted to TreeBASE under study number S28934.

Result

Phylogeny

For primary analysis, ML and Bayesian phylogenetic trees were generated using an aligned sequence dataset comprising of LSU (1,205 base pairs), rpb2 (1,059 bp) and tef1 (954 bp). Of the 3,218 characters included in the alignment, 1,478 were variable and 1,686 were conserved. This combined dataset provided higher confidence values for ordinal and familial classification than those of individual gene trees, with 25 orders and three families (order unknown) being reconstructed in Sordariomycetes (Fig. 1). ML analysis of the combined dataset was conducted based on the selected substitution model for each partition (GTR+G for LSU, J2+G for the first and third codon positions of rpb2, J1+G for the second codon positions of rpb2, F81+G for the first codon positions of tef1, JC69+G for the second codon positions of tef1, and J2+G for the third codon position of tef1). The ML tree with the highest log likelihood (–43687.562) is shown in Fig. 1. Topology recovered by Bayesian analysis was almost identical to that of the ML tree. All species previously described as Phialemoniopsis (marked with blue circle in Fig. 1), one species of “Linocarpon”, two species of “Neolinocarpon” and four strains newly obtained in this study formed a monophyletic clade with the type species of Thyridium (T. vestitum). Their monophyly was completely supported (100% ML BS/1.0 Bayesian PP; Fig. 1). The family Thyridiaceae was found to be related to Annulatascales and Myrmecridiales but did not cluster with any existing order in Sordariomycetes.

Figure 1. 

Maximum-likelihood tree of Sordariomycetes based on combined LSU, rpb2 and tef1 sequence. ML bootstrap proportion (BP) greater than 70% and Bayesian posterior probabilities (PP) above 0.95 are presented at the nodes as ML BP/Bayesian PP and a node not present in the Bayesian analysis is shown with ‘x’. A hyphen (‘-’) indicates values lower than 70% BP or 0.95 PP. Ex-holotype, isotype, paratype and epitype strains are shown in bold and the newly obtained sequences are shown in red. Strains previously described as Phialemoniopsis species are marked with a blue circle. The scale bar represents nucleotide substitutions per site.

For secondary analysis, ML and Bayesian phylogenetic trees were generated using sequences of ITS (483 bp), act (646 bp), tub2 (375 bp), and a combined dataset of these three regions (1,504 bp). The selected substitution models for each region were as follows: J2ef+G for ITS, F81+H for the first and second codon positions of act, J2+G for the third codon position of act, K80+H for the first codon positions of tub2, JC69+H for the second codon position of tub2 and TN93+H for the third codon position of tub2. The ML trees with the highest log likelihood (–1172.0198 in ITS, –1196.6012 in act, –859.37115 in tub2 and –3315.7254 in ITS-act-tub2) are shown in Fig. 2. Our results confirmed close phylogenetic relationships between Thyridium and Phialemoniopsis (Fig. 2A–D). Except for act (Fig. 2B) and tub2 (Fig. 2C), where sequence data of T. vestitum were unavailable, the existence of ten distinct species was suggested (Fig. 2A, D). The following three lineages were found in our four strains (Fig. 2A–D): 1) a bambusicolous lineage (KT 3891) close to T. curvatum and T. limonesiae, 2) a fungus on Betula maximowicziana (KT 3803) nested with T. pluriloculosum, which was previously reported from clinical sources (Perdomo et al. 2013), and 3) another bambusicolous lineage represented by two strains (KT 1015 and KT 3905).

Figure 2. 

Maximum-likelihood tree of Thyridium species based on each ITS (A), act (B), tub2 (C) and combined sequences (ITS-act-tub2; D). ML bootstrap proportion (BP) greater than 70% and Bayesian posterior probabilities (PP) above 0.95 are presented at the nodes as ML BP/Bayesian PP. A hyphen (‘-’) indicates values lower than 70% BP or 0.95 PP and a node not present in the Bayesian analysis is shown with ‘x’. Ex-holotype and epitype strains are shown in bold and the newly obtained sequences are shown in red. Strains previously as Phialemoniopsis species are marked with a blue circle. The scale bars represent nucleotide substitutions per site.

Taxonomy

A new order, Thyridiales, is introduced to accommodate Thyridiaceae because its lineage is phylogenetically and morphologically distinct from any known orders in Sordariomycetes. We concluded Thyridium and Phialemoniopsis to be congeneric based on their morphological similarities and phylogenetic relatedness. An expanded generic circumscription of Thyridium that integrates the generic concept of Phialemoniopsis is provided below. One new species and eight new combinations of Thyridium are proposed.

Thyridiales R. Sugita & Kaz. Tanaka, ord. nov.

MycoBank No: 841916

Type family

Thyridiaceae J.Z. Yue & O.E. Erikss., Syst. Ascom. 6(2): 233 (1987).

Sexual morph

Stromata scattered to grouped. Ascomata perithecial, subglobose to ampulliform. Ostiolar neck cylindrical, periphysate. Paraphyses numerous, unbranched, cylindrical, hyaline. Asci unitunicate, cylindrical, with an apical annulus, pedicellate. Ascospores obovoid to ellipsoid, muriform, hyaline to brown.

Asexual morph

Coelomycetous asexual morph: Conidiomata pycnidial, globose to subglobose. Conidiogenous cells phialidic. Conidia ellipsoidal to obovoid, aseptate, hyaline. Hyphomycetous synasexual morph: Colonies effuse or sporodochial. Conidiophores micronematous, mononematous, simple or branched, hyaline, thin-walled. Conidiogenous cells phialidic. Conidia ellipsoidal to allantoid, aseptate, hyaline.

Notes

Thyridiaceae has been treated as incertae sedis in Sordariomycetes (Yue and Eriksson 1987). Members of Thyridiaceae differ from Myrmecridiales by having pycnidial conidiomata, becoming cup-shaped in the coelomycetous state and micronematous conidiophores with monophialidic conidiogenous cells in the hyphomycetous state. Myrmecridiales have brown thick-walled conidiophores with polyblastic conidiogenous cells (Crous et al. 2015a). Annulatascales have relatively massive refractive, well-developed, conspicuous apical annulus in asci (Wong et al. 1999; Campbell and Shearer 2004; Dong et al. 2021). In contrast, those of members of Thyridiaceae are compact and inconspicuous. Therefore, a new order, Thyridiales, is introduced for this lineage.

Thyridiaceae J.Z. Yue & O.E. Erikss., Syst. Ascom. 6(2): 233 (1987).

Phialemoniopsidaceae K.D. Hyde & Hongsanan, [as Phialemoniopsaceae] Fungal Divers. 107: 95 (2021).

Type genus

Thyridium Nitschke, Pyrenomyc. Germ. 1: 110 (1867).

Notes

Phialemoniopsidaceae is considered a synonym of Thyridiaceae because Phialemoniopsis, the type genus of Phialemoniopsidaceae, was revealed congeneric with Thyridium and is placed in the synonymy of the latter genus in this study. The type genera of both families, that is, Thyridium and Phialemoniopsis, share many morphological features in their asexual states, as noted below.

Thyridium Nitschke, Pyrenomyc. Germ. 1: 110 (1867).

Melanospora subgen. Bivonella Sacc., Syll. fung. (Abellini) 2: 464 (1883).

Bivonella (Sacc.) Sacc., Syll. fung. (Abellini) 9: 989 (1891).

Pleurocytospora Petr., Annls mycol. 21: 256 (1923).

Sinosphaeria J.Z. Yue & O.E. Erikss., Syst. Ascom. 6: 231 (1987).

Phialemoniopsis Perdomo, Dania García, Gené, Cano & Guarro, Mycologia 105: 408 (2013).

Type species

Thyridium vestitum (Fr.) Fuckel, Jb. nassau.Ver. Naturk. 23–24: 195 (1870) [1869–70].

Sexual morph

Stromata scattered to grouped, subepidermal to erumpent, yellowish to dark brown, red in KOH or not changing. Ascomata perithecial, subglobose to ampulliform, single to grouped, immersed in stromata to erumpent through host surface. Ascomatal wall composed of several layers of polygonal, dark brown cells. Ostiolar neck cylindrical, short or long, separated or convergent in upper stromata, periphysate. Paraphyses numerous, septate, unbranched, cylindrical, hyaline. Asci unitunicate, cylindrical, broadly rounded at the apex, with a pronounced non-amyloid apical annulus, pedicellate. Ascospores obovoid or ellipsoid, smooth, pale brown to brown, with several transverse and 0–3 longitudinal or oblique septa.

Asexual morph

Coelomycetous and/or hyphomycetous morphs formed. Coelomycetous asexual morph: Conidiomata pycnidial, single to grouped, superficial or immersed in stromata, globose to subglobose, composed of polygonal to prismatic cells, often becoming cup-shaped when mature, surrounded by setose hyphae. Conidiomatal wall composed of several layers of polygonal, dark brown cells. Ostiolar neck cylindrical, central, periphysate. Setose hyphae erect, usually unbranched, septate, cylindrical, with slightly pointed or blunt tips, hyaline to pale brown, smooth-walled. Conidiophores hyaline, thin-walled, simple or irregularly branched, with branches bearing a small group of phialides terminally. Phialides swollen at the base, tapering at the tip, hyaline. Conidia obovoid to oblong, with a slightly apiculate base, hyaline, smooth-walled, in slimy masses. Hyphomycetous synasexual morph: Colonies effuse or sporodochial. Conidiophores micronematous, mononematous, hyaline, thin-walled, simple or irregularly branched, with branches bearing a small group of phialides terminally. Phialides swollen at the base, tapering at the tip, hyaline. Adelophialides absent or rarely present. Conidia ellipsoidal to allantoid, with a slightly apiculate base, hyaline, smooth-walled, in slimy head. Chlamydospores absent or rarely present, hyaline to pale brown, thick- and rough-walled.

Notes

The newly obtained Thyridium collections formed synasexual morphs, coelomycetous and hyphomycetous, in culture that were similar to those of Phialemoniopsis, having coelomycetous and/or hyphomycetous conidial states in culture (Perdomo et al. 2013). In this study, Phialemoniopsis is treated as a synonym of Thyridium because of their morphological similarities in asexual morphs and phylogenetic relatedness. The genus Pleurocytospora has been proposed as a synonym of Thyridium by culture studies (Leuchtmann and Müller 1986). We agree that the morphological features of Pleurocytospora, such as phialidic conidiogenous cells and hyaline, ellipsoidal conidia formed from both coelomycetous and hyphomycetous states (Leuchtmann and Müller 1986), are almost identical to those of the generic concept of Thyridium emended here.

We accept both Bivonella and Sinosphaeria as synonyms of Thyridium, as proposed in previous studies (Eriksson and Yue 1989; Checa et al. 2013). Sinosphaeria (typified by S. bambusicola = Thyridium chrysomallum; Yue and Eriksson 1987) was established as a new genus without knowing the existence of Bivonella (typified by B. lycopersici; Saccardo 1891). Both genera are characterised by yellowish stromata. The validity of these genera being synonymised under Thyridium is confirmed by the presence of T. flavostromatum, which has yellowish stromata, in the strongly supported Thyridium clade (Fig. 1).

Figure 3. 

Thyridium flavostromatum (A–S KT 3891 = HHUF 30647 T–AC culture KT 3891 = MAFF 247509) A–S sexual morph A–C appearance of stromata on substrate D, E ascomata in longitudinal section (D in 2% KOH) F ostiolar neck of ascoma G paraphyses H ascomatal wall I–K asci L apex of the ascus M stipe of the ascus N–R ascospores S germinating ascospore T–AC hyphomycetous asexual morph T sporulation in culture U phialides V slimy conidial heads W conidiophores X phialide Y adelophialide Z–AB conidia AC chlamydospores and conidia. Scale bars: 1 mm (A); 500 µm (B, C); 100 µm (D, E); 50 µm (F); 10 µm (G–K, M, S, U, V); 5 µm (L, N–R, W–AC); 250 µm (T).

Thyridium flavostromatum R. Sugita & Kaz. Tanaka, sp. nov.

MycoBank No: 841917
Figs 3, 6A

Holotype

Japan, Yamaguchi, Nagato, Misumikami, near Kusaritoge, on dead twigs of Phyllostachys pubescens, 26 March 2018, K. Tanaka, K. Arayama and R. Siguta, KT 3891 (HHUF 30647, holotype designated here), living culture MAFF 247509.

Etymology

The name refers to yellowish stromata.

Sexual morph

Stromata scattered to grouped, subepidermal, becoming erumpent to superficial, 0.7–1.4 mm long, 0.4–0.7 mm wide, yellowish to dark brown, red in 2% KOH. Ascomata perithecial, subglobose to ampulliform, mostly 2–6 grouped, 190–240 µm high, 200–220 µm diam., immersed in stromata to erumpent through host surface. Ascomatal wall 15–23 µm thick, composed of 5–8 layers of polygonal, 2.5–7 × 1.5–3.5 µm, dark brown cells. Ostiolar neck central, cylindrical, 80–140 µm long, 55–90 µm wide, periphysate. Paraphyses numerous, septate, unbranched, cylindrical, 50–105 µm long. Asci unitunicate, cylindrical, 62.5–90 × 6.5–10 µm (av. 78.7 × 7.8 µm, n = 30), broadly rounded at the apex, with a pronounced non-amyloid apical annulus, short-stalked (5–17.5 µm long), with 8 ascospores. Ascospores obovoid to ellipsoid, smooth, hyaline to pale brown, with 3 transverse and 0–2 vertical septa, 9.5–14 × 5–7.5 µm (av. 11.3 × 5.8 µm, n = 50), l/w 1.4–2.5 (av. 2.0, n = 50).

Asexual morph (nature)

Not observed.

Asexual morph (culture)

Hyphomycetous asexual morph formed. Conidiophores micronematous, mononematous, hyaline, thin-walled, simple or irregularly branched, with branches bearing a group of 2–3 phialides terminally. Phialides swollen at the base, tapering at the tip, hyaline, 3–6 × 1–1.5 µm. Adelophialides rarely present. Conidia ellipsoidal to allantoid, with a slightly apiculate base, hyaline, smooth-walled, 2–7 × 1–2.5 µm (av. 4.1 × 1.6 µm, n = 50). Chlamydospores rarely present, solitary, 3.5–6.5 µm diam., hyaline to pale brown, thick- and rough-walled.

Culture characteristics

Colonies on MEA at 25 °C attained 28–29 mm diam. after a week in the dark, whitish. On OA attained 35–37 mm diam., whitish. On PDA attained 28–31 mm diam., whitish to buff (45; Rayner 1970) (Fig. 6A).

Notes

Phylogenetic analyses based on ITS, act, and tub2 sequences suggested that T. flavostromatum was closely related to T. curvatum, T. hongokgense and T. limonesiae (Fig. 2), of which only T. hongokgense has unknown conidial state. Although T. curvatum forms sporodochial conidiomata (Perdomo et al. 2013), those are not found in T. flavostromatum. Conidia of T. limonesiae (2.3–4.9 × 1.4–2 μm; Martinez et al. 2021) are smaller than those of T. flavostromatum (2–7 × 1–2.5 µm). Thyridium flavostromatum is similar to T. lasiacidis on Lasiacis ligulata (Samuels and Rogerson 1989) in 1) having yellowish stromata becoming red in KOH, and 2) ellipsoidal ascospores with three transverse septa, with or without one longitudinal septum in 1–2 median cells. However, T. lasiacidis differs from T. flavostromatum by ascomata with a longer ostiolar neck (90–170 µm long) and dark brown ascospores with terminal pale brown cells (Samuels and Rogerson 1989).

Thyridium pluriloculosum (Perdomo, Dania García, Gené, Cano & Guarro) R. Sugita & Kaz. Tanaka, comb. nov.

MycoBank No: 841918
Figs 4, 6B

Basionym

Phialemoniopsis pluriloculosa Perdomo, Dania García, Gené, Cano & Guarro, Mycologia 105: 412 (2013).

Holotype

USA, Nevada, human toe nail, D.A. Sutton, CBS H-20782, living culture CBS 131712 = UTHSC 04–7 = FMR 11070 (not seen).

Sexual morph

Stromata scattered to grouped, pulvinate, circular to elliptical in outline, elevated beyond bark surface forming pustules, 0.6–0.7 mm high, 0.9–1.0 mm diam., dark brown to black. Ascomata perithecial, subglobose to ampulliform, 4–8 grouped, 700–780 µm high, 220–280 µm diam., immersed in stromata. Ascomatal wall 17–25 µm thick, composed of 7–10 layers of polygonal, 4–6.5 × 2–4 µm, dark brown cells. Ostiolar neck central, cylindrical, 400–430 µm long, 100–110 µm wide, periphysate. Paraphyses septate, unbranched, cylindrical, 92.5–110 µm long, 3.5–5.5 µm wide. Asci unitunicate, cylindrical, 110–175 × 9–12.5 µm (av. 145.6 × 10.3 µm, n = 15), broadly rounded at the apex, with a pronounced non-amyloid apical annulus, pedicellate (12.5–27.5 µm long), with 8 ascospores. Ascospores fusiform to ellipsoid, smooth, brown, with 3 transverse and 0–2 oblique or vertical septa, 13.5–18 × 6–8 µm (av. 15.5 × 7.3 µm, n = 50), l/w 1.7–2.6 (av. 2.1, n = 50).

Asexual morph (nature)

Conidiomata pycnidial, globose to subglobose, grouped, 220–300 µm high, 90–150 µm diam., immersed in stromata. Conidiomatal wall 8–18 µm thick, composed of 3–5 layers of polygonal, 3–4.5 × 2.5–4 µm, dark brown cells. Ostiolar neck central, cylindrical, 80–110 µm long, 90–110 µm wide, composed of polygonal cells, periphysate. Conidiophores hyaline, thin-walled, with branches bearing a group of 2–5 phialides terminally. Phialides tapering toward the tip, hyaline, 11–16 × 1–2 µm. Conidia ellipsoidal, with a slightly apiculate base, hyaline, smooth-walled, 3–4.5 × 1–2 µm (av. 3.7 × 1.5 µm, n = 50). Chlamydospores not observed.

Figure 4. 

Thyridium pluriloculosum (A–Y KT 3803 = HHUF 30648 Z–AL culture KT 3803 = MAFF 247508) A–R sexual morph A, B appearance of stromata on substrate (B transverse sections) C ascomata in longitudinal section D ostiolar neck of ascoma E paraphyses F ascomatal wall G pseudostromatic tissue H–J asci K apex of ascus L–Q ascospores R germinating ascospore S–AF coelomycetous asexual morph (S–Y nature Z–AF culture) S appearance of conidiomata on substrate T conidiomata in longitudinal section U conidiomatal wall V conidiophores W phialide X, Y conidia Z–AB conidiomata in culture (AB multiloculate conidiomata) AC setose hypha of conidiomata AD conidiophores with groups of phialides AE, AF conidia AG–AL hyphomycetous synasexual morph AG, AH sporulation in culture AI phialide AJ, AK conidia AL chlamydospores. Scale bars: 1 mm (A, B, S, AB); 500 µm (C, Z, AA); 100 µm (D, T); 20 µm (AG, AH); 10 µm (E–J, L–R, U, V); 5 µm (K, W–Y, AC–AF, AI–AL).

Asexual morph (culture)

Coelomycetous asexual morph: Conidiomata pycnidial, scattered, single to grouped, superficial, globose to subglobose, 180–380 µm high, mostly 80–580 µm diam., up to 1170 µm diam. when grouped, often becoming cup-shaped when mature, surrounded by setose hyphae. Conidiomatal wall composed of polygonal to prismatic, 3–4.5 × 2.5–4 µm, dark brown cells. Setose hyphae erect, usually unbranched, septate, up to 360 µm long, 2–3 µm wide, pale brown. Conidiophores hyaline, thin-walled, simple or irregularly branched, with branches bearing a group of 2–5 phialides terminally. Phialides tapering toward the tip, hyaline, 10–25 × 1–2.5 µm. Conidia ellipsoidal, with a slightly apiculate base, hyaline, smooth-walled, in slimy masses, 3–4.5 × 1–2 µm (av. 3.8 × 1.4 µm, n = 50). Hyphomycetous synasexual morph: Conidiophores micronematous, mononematous, hyaline, simple or rarely branched. Phialides slightly tapering toward the tip, 4–11 × 1–2.5 µm, hyaline. Adelophialide absent. Conidia allantoid, hyaline, smooth-walled, in slimy heads, 3–9 × 1–2.5 µm (av. 6.2 × 1.7 µm, n = 50). Chlamydospores rarely present, solitary, 3.5–6.5 µm diam., hyaline to pale brown, thick- and rough-walled.

Culture characteristics

Colonies on MEA at 25 °C attained 31–33 mm diam. after a week in the dark, whitish. On OA attained 32–36 mm diam., whitish to grey olivaceous (107). On PDA attained 32–33 mm diam., whitish to buff (45) (Fig. 6B).

Specimen examined

Japan, Aomori, Hirakawa, Hirofune, Shigabo Forest Park, on dead twigs of Betula maximowicziana, 10 October 2017, K. Tanaka, KT 3803 (HHUF 30648), living culture MAFF 247508.

Notes

The conidia from aerial hyphae of strain KT 3803 were larger (3–9 × 1–2.5 µm) in culture than those of the original description of Thyridium pluriloculosum (3–5 × 1–2.5 µm; Perdomo et al. 2013). However, we identified this new collection on Betula maximowicziana as T. pluriloculosum, based on the high sequence homology of three loci with ex-type culture of this species (CBS 131712; 99.6% in ITS, 99.2% in act, and 99.5% in tub2). The sexual-asexual relationship of T. pluriloculosum was verified in this study. Although this species has been reported from clinical sources as an asexual morph (Perdomo et al. 2013), the recently collected material represents a sexual morph on plant material.

In Thyridium, T. betulae has also been recorded on Betula sp. in France (Roumeguère 1891). Although sequences of T. betulae are unavailable for molecular comparison, it is clearly different from T. pluriloculosum in having ascospores with 5–7 transverse and one longitudinal septum.

Thyridium punctulatum (I. Hino & Katum.) R. Sugita & Kaz. Tanaka, comb. nov.

MycoBank No: 841919
Figs 5, 6C

Basionym

Pleospora punctulata I. Hino & Katum., Icones Fungorum Bamb. Jpn.: 181 (1961).

Holotype

Japan, Shizuoka, Fuji Bamboo Garden, on dead twigs of Phyllostachys nigra var. henonis, 1 April 1958, K. Katumoto, YAM 21851.

Epitype

Japan, Yamaguchi, Hagi, Akiragi, near Chikurindoro-park, on dead twigs of Phyllostachys nigra var. nigra, 26 March 2018, K. Tanaka, K. Arayama and R. Sugita, KT 3905 (HHUF 30649 epitype designated here; MBT 10004137), ex-epitype culture MAFF 247510.

Sexual morph

Stromata scattered to grouped, subepidermal, becoming erumpent to superficial, 0.5–1.2 mm long, 0.2–0.4 mm wide, dark brown. Ascomata perithecial, subglobose to conical, single to 2–3 grouped, 130–190 µm high, 140–230 µm diam., immersed in stromata to erumpent through host surface. Ascomatal wall 7–15 µm thick, composed of 3–5 layers of polygonal, 3–6.5 × 1–4.5 µm, dark brown cells. Ostiolar neck central, cylindrical, 37–85 µm long, 37–63 µm wide, periphysate. Paraphyses numerous, septate, unbranched, cylindrical, hyaline, 77–103 µm long. Asci unitunicate, cylindrical, 67.5–105 × 7.5–11.5 µm (av. 82.9 × 9.4 µm, n = 60), broadly rounded at the apex, with a pronounced non-amyloid apical annulus, short-stalked (3.5–11.5 µm long), with 8 ascospores. Ascospores ellipsoid to oblong, smooth, pale brown, with 3 transverse and 1–2 vertical septa, 10–15 × 5–9 µm (av. 12.8 × 7.0 µm, n = 60), l/w 1.4–2.4 (av. 1.8, n = 60).

Figure 5. 

Thyridium punctulatum (A–N, Q, R KT 3905 = HHUF 30649 O, P YAM 21851 S, T, W–AB culture KT 1015 = JCM 13159 = MAFF 239669 U, V, AC–AK culture KT 3905 = MAFF 247510) A–R sexual morph A, B appearance of stromata on substrate C, D ascomata in longitudinal section E ostiolar neck of ascoma F paraphyses G ascomatal wall H–J asci K apex of ascus L stipe of ascus M–Q ascospores R germinating ascospore S–AD coelomycetous asexual morph S–V conidiomata in culture W conidioma in longitudinal section X conidiomatal wall Y setose hyphae of conidiomata Z, AA conidiophores AB phialides AC, AD conidia AE–AK hyphomycetous synasexual morph AE conidiophore AF slimy head AG phialide AH–AJ conidia AK chlamydospores. Scale bars: 1 mm (A, S); 500 µm (B); 100 µm (C, W); 50 µm (D); 10 µm (E–J, L, R, X–AA, AE, AF); 5 µm (K, M–Q, AB–AD, AG–AK); 200 µm (T–V).

Asexual morph (nature)

Not observed.

Asexual morph (culture)

Coelomycetous asexual morph: Conidiomata pycnidial, single to grouped, superficial, globose to subglobose, 100–250 µm high, 170–620 µm diam., composed of polygonal to prismatic, 3.5–7.5 × 2.5–4 µm cells, often becoming cup-shaped when mature, surrounded by setose hyphae. Setose hyphae erect, usually unbranched, septate, up to 225 µm long, 1.5–2.5 µm wide, pale brown. Conidiophores hyaline, thin-walled, simple or irregularly branched, with branches bearing a group of 2–5 phialides terminally. Phialides swollen at the base, tapering at the tip, 7–20 × 1–3 µm, hyaline. Conidia ellipsoidal to obovoid, with a slightly apiculate base, hyaline, smooth-walled, in slimy masses, 2–3.5 × 1–2 µm (av. 2.9 × 1.4 µm, n = 50). Hyphomycetous synasexual morph: Conidiophores micronematous, mononematous, hyaline, thin-walled, simple or irregularly branched, with branches bearing a group of 2–3 phialides terminally. Phialides swollen at the base, tapering at the tip, hyaline, 3–9 × 1–2 µm. Adelophialide absent. Conidia ellipsoidal to allantoid, hyaline, smooth-walled, in slimy heads, 2.5–8 × 1–3 µm (av. 4.3 × 1.6 µm, n = 87). Chlamydospores rarely present, solitary or chained, 4–5.5 µm diam., hyaline to pale brown.

Culture characteristics

Colonies on MEA at 25 °C attained 31–32 mm diam. after a week in the dark, granulose, whitish. On OA attained 38–39 mm diam., granulose, whitish. On PDA attained 35–36 mm diam., whitish to buff (45) (Fig. 6C).

Figure 6. 

Colony characters of Thyridium species used in this study on MEA (bottom right), OA (bottom left) and PDA (upper) within 1 week at 25 °C in the dark A T. flavostromatum (culture KT 3891 = MAFF 247509) B T. pluriloculosum (culture KT 3803 = MAFF 247508) C T. punctulatum (culture KT 3905 = MAFF 247510). Scale bars: 3 cm (A–C).

Other specimen examined

Japan, Iwate, Morioka, Ueda, Campus of Iwate University, on dead culms of Phyllostachys pubescens, 17 February 2003, K. Tanaka and Y. Harada, KT 1015 (HHUF 29350), living culture JCM 13159 = MAFF 239669.

Notes

This species has been described from Phyllostachys nigra var. henonis, as a species of Pleospora (Dothideomycetes; Hino 1961). Our phylogenetic analysis (Fig. 1) shows that this species is a member of the genus Thyridium (Sordariomycetes). The morphological features of this species are consistent with those of the genus Thyridium, including immersed to erumpent, single to grouped, perithecial ascomata with a cylindrical ostiolar neck, unitunicate asci and muriform, pigmented ascospores (Eriksson and Yue 1989). Therefore, we propose a new combination, T. punctulatum, for Pleospora punctulata.

Thyridium cornearis (Perdomo, Dania García, Gené, Cano & Guarro) R. Sugita & Kaz. Tanaka, comb. nov.

MycoBank No: 841920

Basionym

Phialemoniopsis cornearis Perdomo, Dania García, Gené, Cano & Guarro, Mycologia 105: 408 (2013).

Thyridium curvatum (W. Gams & W.B. Cooke) R. Sugita & Kaz. Tanaka, comb. nov.

MycoBank No: 841921

Phialemoniopsis curvata (W. Gams & W.B. Cooke) Perdomo, Dania García, Gené, Cano & Guarro, Mycologia 105: 410 (2013).

Basionym

Phialemonium curvatum W. Gams & W.B. Cooke, Mycologia 75: 980 (1983).

Thyridium endophyticum (Lei Su & Y.C. Niu) R. Sugita & Kaz. Tanaka, comb. nov.

MycoBank No: 841922

Basionym

Phialemoniopsis endophytica Lei Su & Y.C. Niu, Mycol. Progr. 15: 3 (2016).

Thyridium hongkongense (Tsang, Chan, Ip, Ngan, Chen, Lau, Woo) R. Sugita & Kaz. Tanaka, comb. nov.

MycoBank No: 841923

Basionym

Phialemoniopsis hongkongensis Tsang, Chan, Ip, Ngan, Chen, Lau, Woo, J. Clin. Microbiol. 52: 3284 (2014).

Thyridium limonesiae (A. Riat, L.W. Hou & Crous) R. Sugita & Kaz. Tanaka, comb. nov.

MycoBank No: 841927

Basionym

Phialemoniopsis limonesiae A. Riat, L.W. Hou & Crous, Emerging Microbes & Infections 10: 403 (2021).

Thyridium oculorum (Gené & Guarro) R. Sugita & Kaz. Tanaka, comb. nov.

MycoBank No: 841924

Phialemoniopsis ocularis (Gené & Guarro) Perdomo, Dania García, Gené, Cano & Guarro, Mycologia 105: 411 (2013).

Basionym

Sarcopodium oculorum Gené & Guarro, J. Clin. Microbiol. 40: 3074 (2002).

Discussion

We show that the asexual genus Phialemoniopsis (established by Perdomo et al. 2013) is a synonym of the sexual genus Thyridium (established by Nitschke 1867). We found a new species of Thyridium (T. flavostromatum), transferred Pleospora punctulata into Thyridium, and proposed seven new combinations in Thyridium for strains previously treated in Phialemoniopsis. We provided a revised generic circumscription of Thyridium based on both sexual and asexual characteristics and revealed the phylogenetic relationships of species within this genus.

The genus Thyridium has been defined mainly on the basis of sexual characters (Nitschke 1867; Eriksson and Yue 1989). Currently, 33 species are recorded in this genus (http://www.indexfungorum.org, 2021). Asexual morphs are unknown in most species of Thyridium, with the exceptions of T. flavum and T. vestitum, in which asexual morphs have been recorded based on sexual-asexual association on the same specimen (Petch 1917) and on the basis of culture study (Leuchtmann and Müller 1986, this study), respectively. In contrast, the genus Phialemoniopsis has been defined based only on asexual characters (Perdomo et al. 2013). Its ordinal affiliation within Sordariomycetes has not been resolved, but recent phylogenetic analyses of this class suggest that Phialemoniopsis is close to Thyridium (Hyde et al. 2021). In our phylogenetic analysis, all species previously described as Phialemoniopsis (marked with blue circle; Fig. 1) were clustered in a single clade, including the type species of Thyridium (T. vestitum), as well as two new strains proposed here (T. flavostromatum and T. punctulatum). Both genera have similar asexual morphs, which have conidiophores bearing small groups of phialides, hyaline phialidic conidiogenous cells, and ellipsoidal or allantoid, hyaline conidia in both coelomycetous and hyphomycetous states (Petch 1917; Leuchtmann and Müller 1986; Perdomo et al. 2013). Morphological and molecular phylogenetic evidence clearly shows that Phialemoniopsis is congeneric with Thyridium.

Synonymising Phialemoniopsis under Thyridium expanded information about the asexual morphs of Thyridium. In this genus, only T. vestitum has been demonstrated to have asexual morphs by culture studies (Leuchtmann and Müller 1986). It has both coelomycetous and hyphomycetous complex asexual morphs, which have phialidic conidiogenous cells with collarette and ellipsoidal to allantoid hyaline conidia (Leuchtmann and Müller 1986). Members of Phialemoniopsis also have coelomycetous and/or hyphomycetous conidial states (Perdomo et al. 2013; Tsang et al. 2014; Su et al. 2016; Martinez et al. 2021). The close relationship of Phialemoniopsis and Thyridium suggests that such complex asexual morphs may be common within Thyridium species.

In Thyridium, T. endophyticum and T. curvatum have been isolated from both plants and animals (Gam and McGinnis 1983; Halleen et al. 2007; Perdomo et al. 2013; Su et al. 2016; Ito et al. 2017). There are several examples of fungal species, including human pathogens, detected from various substrates. For example, Phaeoacremonium minimum is a pathogen on grapevines, where it forms both sexual and asexual morphs (Crous et al. 1996; Pascoe et al. 2004), but it has also been reported as a causative agent of subcutaneous phaeohyphomycosis in humans as asexual morph (Choi et al. 2011). Other species of Thyridium may also have cryptic life cycles and can colonise each host substrate at different reproductive stages. An example of this prediction can be found in T. pluriloculosum. This species was originally found in human nails as an asexual fungus (Perdomo et al. 2013), and its sexual state was rediscovered on twigs of Betula maximowicziana in our study.

Epitypification of the type species of Thyridium (T. vestitum) will be a necessary issue in the future. We used sequences from two non-type strains (CBS 113027, CBS 125582) of this species for phylogenetic analyses but they did not form a monophyletic clade (Fig. 1). Sequence differences between these two strains were found at 34 positions with four gaps in the LSU. These results indicate that the strains obtained from Acer pseudoplatanus (CBS 113027) and no host information (CBS 125582) in Austria are not conspecific. A fresh collection of T. vestitum on original host plant from the type locality (Ribes rubrum, Sweden; Fries 1823) and its phylogenetic analysis are required to fix generic circumscription of Thyridium.

Thyridiales established here may encompass other genera and families with morphologies distinct from the genus Thyridium (Thyridiaceae). Some species of “Linocarpon” and “Neolinocarpon” are nested within the Thyridiales (Fig. 1). Linocarpon and Neolinocarpon sensu stricto belong to Linocarpaceae (Chaetosphaeriales) and are morphologically distinct from Thyridium in having filiform, straight or curved, unicellular, hyaline, or pale-yellowish ascospores (Huhndorf and Miller 2011; Konta et al. 2017). The “Linocarpon” and “Neolinocarpon” species phylogenetically unrelated to Linocarpon and Neolinocarpon sensu stricto may be new lineages in Thyridiaceae or belong to its own new undescribed family. However, we cannot clarify the phylogenetic/taxonomic relatedness of these atypical Linocarpon-like species because none of them are ex-types and their morphological information are unavailable. Further molecular phylogenetic study of these fungi based on protein-coding sequences and finding additional specimens/isolates of “Linocarpon” and “Neolinocarpon” species related to Thyridium will be necessary to clarify their taxonomic affiliation and better understand the concept of Thyridiales.

Acknowledgments

We gratefully acknowledge Y. Harada and K. Arayama for their help with the collection of fungal specimens. We thank the curator of YAM, S. Ito, who permitted us to examine type collection. This work was partially supported by grants from the Japan Society for the Promotion of Science (JSPS 19K06802).

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