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Research Article
Note on the genus Nemania (Xylariaceae) – first records and a new species of the genus from Iran
expand article infoMohammad Javad Pourmoghaddam, Christopher Lambert§|, Hermann Voglmayr, Seyed Akbar Khodaparast, Irmgard Krisai-Greilhuber, Marc Stadler#§
‡ University of Guilan, Rasht, Iran
§ Department Microbial Drugs, Helmholtz-Centre for Infection Research GmbH, Braunschweig, Germany
| Department for Molecular Cell Biology, Helmholtz-Centre for Infection Research GmbH, Braunschweig, Germany
¶ University of Vienna, Wien, Austria
# Technische Universität Braunschweig, Braunschweig, Germany
Open Access

Abstract

In a survey of xylarialean fungi in northern Iran, some specimens attributable to the genus Nemania were collected, cultured and sequenced. Morphological evidence and phylogenetic analyses of a combined ITS, LSU, RPB2 and TUB2 gene dataset confirmed the presence of Nemania diffusa and N. serpens in Iran for the first time. Furthermore, the new species N. hyrcana, which shows similarities to N. subaenea and its putative synonym N. plumbea, but significantly differs from the latter in its DNA sequences, was encountered. All species are illustrated, described and discussed. In the phylogenetic analyses, for the first time, the overlooked ex-type ITS sequences of the neotype of the generic type, N. serpens and that of the holotype of N. prava, were added to a multi-gene matrix of Nemania. This revealed that the two accessions of N. serpens (HAST 235 and CBS 679.86), for which multigene data are available in GenBank, are misidentified, while the Iranian accession of N. serpens has an almost identical ITS sequence to the neotype, confirming its morphological species identification. The two previously accepted species of Euepixylon, E. udum and E. sphaeriostomum, are embedded within Nemania and are revealed as close relatives of N. serpens, supporting the inclusion of Euepixylon in Nemania.

Keywords

Ascomycota, molecular phylogenetics, Nemania serpens, one new species, Sordariomycetes, taxonomy, Xylariales

Introduction

The genus Nemania S. F. Gray was established by Gray (1821) and has always been considered to belong to the family Xylariaceae Tul. & C. Tul., even though its species were placed in Hypoxylon for some time, according to the generic concepts established by Miller (1961) and other authors. The reason for this was that Nemania species superficially resemble those of Hypoxylon in having effused-pulvinate stromata on dead wood. Gray (1821) had used a somewhat ill-defined concept for this genus, which was resolved by Donk (1964) who selected Sphaeria serpens as the type of the genus. Later, Pouzar (1985a, 1985b) emended Nemania and separated the genus from Hypoxylon according to morphological characters and Petrini and Rogers (1986) confirmed this by studies on the cultures, pointing out the geniculosporium-like anamorph of Nemania species (vs. the nodulisporium-like anamorphs that are typical for Hypoxylon s. str.). The anamorph genus Geniculosporium had even eventually been erected, based on the conidial state of “Hypoxylon” (i.e. Nemania) serpens by Chesters and Greenhalgh (1964). This holomorphic concept has meanwhile been supported by molecular phylogenetic studies (e.g. Hsieh et al. 2010) that clearly revealed close affinities of Nemania to Xylaria and other genera with geniculosporium-like anamorphs. The most important monographs on the genus by Granmo et al. (1999) and Ju and Rogers (2002), however, still relied on morphological characters and many of the 37 taxa that were recognised by these authors have not yet been characterised by DNA sequence data.

Nemania is characterised by carbonaceous, superficial, multiperitheciate, effused-pulvinate stromata with papillate ostioles and variable presence of soft, whitish, brownish, grey or yellow internal tissue. Stromata do not release pigments in 10% potassium hydroxide (KOH). Asci are cylindrical, short or long stipitate, persistent, with an apical apparatus of various shapes, amyloid (like N. diffusa) or inamyloid (like N. serpens) in Melzer’s iodine reagent. Ascospores are pale brown to dark brown or blackish-brown, ellipsoidal, cylindrical or fusoid, inequilateral, slightly inequilateral or nearly equilateral, with acute, narrowly rounded or broadly rounded ends, with a straight, conspicuous or inconspicuous germ slit of spore length to much less than spore-length. It has geniculosporium-like anamorphs (Ju and Rogers 2002; Fournier et al. 2018).

During our survey of Xylariales specimens in northern Iran, three Nemania taxa were recorded. Species were identified, based on morphological and molecular phylogenetic analyses. As a result, a new species and records of two further species are reported from Iran, for which detailed morphological descriptions, illustrations and phylogenetic information are here provided.

Materials and methods

Morphological observation

The fungal specimens were collected in northern Iran (Guilan, Mazandaran and Golestan Provinces). For light microscopy, fresh collections, single ascospore isolations and cultures were examined for macro- and micromorphological characteristics, according to Ju and Rogers (2002) and Pourmoghaddam et al. (2018). Dried specimens were deposited in the University of Guilan Mycological Herbarium (GUM). Living cultures were deposited in the culture collection MUCL (Louvain la-Neuve, Belgium) and in the Iranian Fungal Culture Collection, Iranian Research Institute of Plant Protection, Tehran, Iran (IRAN).

DNA extraction, PCR and sequencing

DNA extraction of fresh cultures and amplification of the ITS (nuc rDNA internal transcribed spacer region containing ITS1-5.8S-ITS2), LSU (5' 1200 bp of the large subunit nuc 28S rDNA), RPB2 (partial second largest subunit of the DNA-directed RNA polymerase II) and TUB2 (partial β-tubulin) loci were carried out as described by Wendt et al. (2018).

Phylogenetic analyses

Published sequences of a single accession for each Nemania species served as basis for the sequence matrix. Information on all used strains, their corresponding sequences and GenBank accession numbers can be found in Table 1. In addition to the sequences retrieved from GenBank, ITS sequences of the holotype of N. prava and of the neotype of N. serpens were manually transcribed from the ITS alignment published as colour figure appendix 3 in Granmo et al. (1999), because these sequences have not been deposited in a public sequence repository. In addition, to have the ITS sequences of Granmo et al. (1999) available for further studies, the transcribed ex-type sequences were also submitted to GenBank (ex-neotype sequence of N. colliculosa: OP289676, ex-holotype sequence of N. prava: OP289674, ex-neotype sequence of N. serpens: OP289675). To reveal the phylogenetic position of the Iranian Nemania accessions, the newly-generated sequences were aligned with the GenBank sequences. All alignments were produced with the server versions of MAFFT v. 7.490 (www.ebi.ac.uk/Tools/mafft or http://mafft.cbrc.jp/alignment/server/; Katoh et al. 2019) and checked and refined using BioEdit v. 7.0.4.1 (Hall 1999).

Table 1.

Isolation and accession numbers of sequences used in the phylogenetic analyses. Isolates/sequences in bold were isolated/sequenced in present study. N/A: not available.

Species Strain number Origin Status GenBank accession numbers Reference
ITS LSU RPB2 TUB2
Amphirosellinia fushanensis HAST 91111209 Taiwan HT GU339496 N/A GQ848339 GQ495950 Hsieh et al. (2010)
Amphirosellinia nigrospora HAST 91092308 Taiwan HT GU322457 N/A GQ848340 GQ495951 Hsieh et al. (2010)
Anthostomelloides krabiensis MFLUCC 15-0678 Thailand HT KX305927 KX305928 KX305929 N/A Tibpromma et al. (2017)
Astrocystis concavispora MFLUCC 14.0174 Italy KP297404 KP340545 KP340532 KP406615 Daranagama et al. (2015)
Biscogniauxia nummularia MUCL 51395 France ET KY610382 KY610427 KY624236 KX271241 Wendt et al. (2018)
Clypeosphaeria mamillana CBS 140735 France ET KT949897 KT949897 MF489001 N/A Jaklitsch et al. (2016), Voglmayr et al. (2018)
Collodiscula bambusae GZU H0102 China KP054279 KP054280 KP276675 KP276674 Li et al. (2015)
Collodiscula fangjingshanensis GZU H0109 China HT KR002590 KR002591 KR002592 KR002589 Li et al. (2015)
Collodiscula japonica CBS 124266 China JF440974 JF440974 KY624273 KY624316 Jaklitsch and Voglmayr (2012), Wendt et al. (2018)
Coniolarelia limoniispora MUCL 29409 Japan MN984615 MN984624 MN987235 MN987240 Wittstein et al. (2020)
Dematophora bunodes CBS 123597 Peru MN984619 MN984625 N/A MN987245 Wittstein et al. (2020)
Dematophora buxi JDR 99 France GU300070 N/A GQ844780 GQ470228 Hsieh et al. (2010)
Dematophora necatrix CBS 349.36 Argentina AY909001 KF719204 KY624275 KY624310 Peláez et al. (2008), Wendt et al. (2018)
Dematophora pepo CBS 123592 Peru MN984620 N/A N/A MN987246 Wittstein et al. (2020)
Entoleuca mammata JDR 100 France GU300072 N/A GQ844782 GQ470230 Hsieh et al. (2010)
Graphostroma platystomum CBS 270.87 France HT JX658535 DQ836906 KY624296 HG934108 Stadler et al. (2014), Zhang et al. (2006), Wendt et al. (2018), Koukol et al. (2015)
Hypocreodendron sanguineum JDR 169 Mexico GU322433 N/A GQ844819 GQ487710 Hsieh et al. (2010)
Hypoxylon fragiforme MUCL 51264 Germany ET KC477229 KM186295 KM186296 KX271282 Stadler et al. (2013), Daranagama et al. (2015), Wendt et al. (2018)
Hypoxylon howeanum MUCL 47599 Germany AM749928 KY610448 KY624258 KC977277 Bitzer et al. (2008), Kuhnert et al. (2014), Wendt et al. (2018)
Kretzschmaria clavus YMJ 114 French Guiana EF026126 N/A GQ844789 EF025611 Hsieh et al. (2010)
Kretzschmaria deusta CBS 163.93 Germany KC477237 KY610458 KY624227 KX271251 Stadler et al. (2013), Wendt et al. (2018)
Kretzschmaria deusta CBS 826.72 Belgium KU683767 KU683767 KU684309 KU684190 U’Ren et al. (2016)
Kretzschmaria deusta MUCL 57705 Iran MH084755 OP359327 OP359596 OP359601 Pourmoghaddam et al. (2018), This study
Kretzschmaria hedjaroudei MUCL 57706 Iran HT MH084757 OP359328 OP359597 OP359602 Pourmoghaddam et al. (2018), This study
Kretzschmaria guyanensis HAST 89062903 Taiwan GU300079 N/A GQ844792 GQ478214 Hsieh et al. (2010)
Kretzschmaria lucidula YMJ 112 French Guiana EF026125 N/A GQ844790 EF025610 Hsieh et al. (2010)
Kretzschmaria megalospora YMJ 229 Malaysia EF026124 N/A GQ844791 EF025609 Hsieh et al. (2010)
Kretzschmaria neocaledonica HAST 94031003 Taiwan GU300078 N/A GQ844788 GQ478213 Hsieh et al. (2010)
Kretzschmaria pavimentosa JDR 109 Taiwan GU300077 N/A GQ844787 GQ478212 Hsieh et al. (2010)
Kretzschmaria sandvicensis JDR 113 USA GU300076 N/A GQ844786 GQ478211 Hsieh et al. (2010)
Linosporopsis ischnotheca CBS 145761 Switzerland ET MN818952 MN818952 MN820708 MN820715 Voglmayr and Beenken (2020)
Linosporopsis ochracea CBS 145999 Germany ET MN818958 MN818958 MN820714 MN820721 Voglmayr and Beenken (2020)
Nemania abortiva BISH 467 USA HT GU292816 N/A GQ844768 GQ470219 Hsieh et al. (2010)
Nemania aquilariae KUMCC 20-0268 China HT MW729422 MW729420 MW717891 MW881142 Tibpromma et al. (2021)
Nemania beaumontii HAST 405 Martinique GU292819 N/A GQ844772 GQ470222 Hsieh et al. (2010)
Nemania bipapillata HAST 90080610 Taiwan GU292818 N/A GQ844771 GQ470221 Hsieh et al. (2010)
Nemania camelliae GMB0068 China HT MW851889 MW851872 MW836055 MW836029 Pi et al. (2021)
Nemania caries GMB0070 China MW851874 MW851857 MW836071 MW836036 Pi et al. (2021)
Nemania changningensis GMB0056 China HT MW851875 MW851858 MW836061 MW836027 Pi et al. (2021)
Nemania chestersii JF 04024 France N/A DQ840072 DQ631949 DQ840089 Tang et al. (2007; 2009)
Nemania cyclobalanopsina GMB0062 China HT MW851883 MW851866 MW836057 MW836025 Pi et al. (2021)
Nemania delonicis MFLU 19-2124 Thailand HT MW240613 MW240542 MW342617 MW775574 Samarakoon et al. (2022)
Nemania diffusa HAST 91020401 Taiwan GU292817 N/A GQ844769 GQ470220 Hsieh et al. (2010)
Nemania ethancrensonii CBS 148337 USA HT ON869311 ON869311 ON808489 ON808533 Voglmayr et al. (2022)
Nemania feicuiensis GMB0059 China HT MW851880 MW851863 MW836063 MW836023 Pi et al. (2021)
Nemania fusoidispora GZUH0098 China MW851881 MW851864 MW836070 MW836037 Ariyawansa et al. (2015)
Nemania hyrcana MUCL 57704 Iran HT OP359332 OP359329 OP359598 OP359603 This study
Nemania hyrcana MUCL 57703 Iran OP359333 OP359330 OP359599 OP359604 This study
Nemania illita YMJ 236 USA EF026122 N/A GQ844770 EF025608 Hsieh et al. (2010)
Nemania lishuicola GMB0065 China HT MW851886 MW851869 MW836065 MW836033 Pi et al. (2021)
Nemania longipedicellata MFLU 18-0819 Thailand HT MW240612 MW240541 MW342616 MW775573 Samarakoon et al. (2022)
Nemania macrocarpa WSP 265 USA HT GU292823 N/A GQ844776 GQ470226 Hsieh et al. (2010)
Nemania maritima HAST 89120401 Taiwan ET GU292822 N/A GQ844775 GQ470225 Hsieh et al. (2010)
Nemania paraphysata MFLU 19-2121 Thailand HT MW240609 MW240538 MW342613 N/A Samarakoon et al. (2022)
Nemania plumbea JF TH-04-01 Thailand HT DQ641634 DQ840071 DQ631952 DQ840084 Tang et al. (2007; 2009)
Nemania prava CBS 679.86 Switzerland PT 2 KU683765 KU683765 KU684284 KU684188 U’Ren et al. (2016)
Nemania prava TROM 104 Norway HT OP2896743 N/A N/A N/A Granmo et al. (1999)
Nemania primolutea HAST 91102001 Taiwan HT EF026121 N/A GQ844767 EF025607 Hsieh et al. (2010)
Nemania rubi GMB0064 China HT MW851885 MW851868 MW836059 MW836021 Pi et al. (2021)
Nemania serpens TROM 174 Norway NT OP2896753 N/A N/A N/A Granmo et al. (1999)
Nemania serpens MUCL 57702 Iran OP359334 OP359331 OP359600 OP359605 This study
Nemania serpens HAST 235 Canada GU292820 N/A GQ844773 GQ470223 Hsieh et al. (2010)
Nemania sphaeriostoma JDR 261 USA GU292821 N/A GQ844774 GQ470224 Hsieh et al. (2010)
Nemania thailandensis MFLU 19-2117 Thailand HT MW240611 MW240540 MW342615 MW775572 Samarakoon et al. (2022)
Nemania uda CBS 148422 Austria HT ON869312 ON869312 ON808488 ON808532 Voglmayr et al. (2022)
Nemania yunnanensis KUMCC 20-0267 China HT MW729423 MW729421 MW717892 MW881141 Tibpromma et al. (2021)
Podosordaria mexicana WSP 176 Mexico GU324762 N/A GQ853039 GQ844840 Hsieh et al. (2010)
Podosordaria muli WSP 167 Mexico HT GU324761 N/A GQ853038 GQ844839 Hsieh et al. (2010)
Poronia pileiformis WSP 88113001 Taiwan ET GU324760 N/A GQ853037 GQ502720 Hsieh et al. (2010)
Poronia punctata CBS 656.78 Australia KT281904 KY610496 KY624278 KX271281 Senanayake et al. (2015), Wendt et al. (2018)
Rosellinia aquila MUCL 51703 France KY610392 KY610460 KY624285 KX271253 Wendt et al. (2018)
Rosellinia cf. akulovii MUCL 57710 Iran OL635184 OL635175 OL657210 OL657219 Pourmoghaddam et al. (2022)
Rosellinia cf. akulovii MUCL 57711 Iran OL635185 OL635176 OL657211 OL657220 Pourmoghaddam et al. (2022)
Rosellinia corticium MUCL 51693 France KY610393 KY610461 KY624229 KX271254 Wendt et al. (2018)
Rosellinia corticium STMA 13324 Germany MN984621 MN984627 MN987237 MN987241 Wittstein et al. (2020)
Rosellinia corticium MUCL 57714 Iran OL635180 OL635171 OL657206 OL657215 Pourmoghaddam et al. (2022)
Rosellinia nectrioides CBS 449.89 Sweden MN984622 MN984628 MN987239 N/A Wittstein et al. (2020)
Sarcoxylon compunctum CBS 359.61 South Africa KT281903 KY610462 KY624230 KX271255 Senanayake et al. (2015), Wendt et al. (2018)
Stilbohypoxylon elaeicola Y.M.J 173 French Guiana EF026148 N/A GQ844826 EF025616 Hsieh et al. (2010)
Stilbohypoxylon quisquiliarum Y.M.J 172 French Guiana EF026119 N/A GQ853020 EF025605 Hsieh et al. (2010)
Xylaria acuminatilongissima HAST 95060506 Taiwan HT EU178738 N/A GQ853028 GQ502711 Hsieh et al. (2010)
Xylaria adscendens J.D.R 865 Thailand GU322432 N/A GQ844818 GQ487709 Hsieh et al. (2010)
Xylaria arbuscula CBS 126415 Germany KY610394 KY610463 KY624287 KX271257 Fournier et al. (2011), Wendt et al. (2018)
Xylaria bambusicola WSP 205 Taiwan HT EF026123 N/A GQ844802 AY951762 Hsieh et al. (2010)
Xylaria brunneovinosa HAST 720 Martinique HT EU179862 N/A GQ853023 GQ502706 Hsieh et al. (2010)
Xylaria curta HAST 494 Martinique GU322444 N/A GQ844831 GQ495937 Hsieh et al. (2010)
Xylaria discolor HAST 131023 USA ET JQ087405 N/A JQ087411 JQ087414 Hsieh et al. (2010)
Xylaria hypoxylon CBS 122620 Sweden ET KY610407 KY610495 KY624231 KX271279 Sir et al. (2016), Wendt et al. (2018)
Xylaria multiplex HAST 580 Martinique GU300098 N/A GQ844814 GQ487705 Hsieh et al. (2010)
Xylaria polymorpha MUCL 49884 France KY610408 KY610464 KY624288 KX271280 Wendt et al. (2018)

For the phylogenetic analyses, 90 accessions of 86 species of Xylariaceae and four outgroup taxa from Graphostromataceae (Biscogniauxia nummularia, Graphostroma platystomum) and Hypoxylaceae (Hypoxylon fragiforme, H. howeanum) were included. We also included the newly-sequenced LSU, RPB2 and TUB2 loci of the Iranian collections of Kretzschmaria hedjaroudei (MUCL 57706) and K. deusta (MUCL 57705); for details on those accessions, see Pourmoghaddam et al. (2018). The sequence matrices of ITS, LSU, RPB2 and TUB2 were combined; after exclusion of ambiguously aligned and gappy regions, the resulting combined data matrix contained 4616 alignment positions from four loci (543 from ITS, 1275 from LSU, 1191 from RPB2 and 1607 from TUB2).

Maximum Likelihood (ML) analyses were performed with RAxML (Stamatakis 2006) as implemented in raxmlGUI 1.3 (Silvestro and Michalak 2012) using the ML + rapid bootstrap setting and the GTRGAMMA substitution model with 1000 bootstrap replicates.

Maximum Parsimony (MP) analyses were performed with PAUP v. 4.0a169 (Swofford 2002). All molecular characters were unordered and given equal weight; analyses were performed with gaps treated as missing data; the COLLAPSE command was set to MINBRLEN. MP analysis of the combined multilocus matrix was done using 1000 replicates of heuristic search with random addition of sequences and subsequent TBR branch swapping (MULTREES option in effect, steepest descent option not in effect). Bootstrap analyses with 1000 replicates were performed in the same way, but using 10 rounds of random sequence addition and subsequent branch swapping during each bootstrap replicate. Bootstrap values ≤ 70% are considered low, between 70 and 90% intermediate and ≥ 90% high.

Results

Molecular phylogeny

Of the 4616 characters of the combined matrix, 1884 were parsimony informative (284 in ITS, 142 in LSU, 613 in RPB2 and 845 in TUB2). The phylogram of the best ML tree (lnL = − 88,062.8606) obtained by RAxML is shown as Fig. 1. The MP analysis revealed two trees of length 20,490 (not shown) that had a similar topology to the ML tree. The phylogenies reveal a monophyletic clade of Nemania (including Euepixylon), like in previous studies (Wendt et al. 2018; Pi et al. 2021; Samarakoon et al. 2022; Voglmayr et al. 2022). Within Xylariaceae, the Nemania clade is most closely related to the genera Coniolariella, Dematophora, Entoleuca and Rosellinia.

Figure 1. 

Phylogram of the best ML trees (lnL = −88,062.8606) revealed by RAxML from an analysis of the combined ITS-LSU-RPB2TUB2 matrix of selected Xylariaceae. Strains in bold were sequenced in the current study; for strains marked with an asterisk (*), ITS sequences were transcribed from Appendix 3 of Granmo et al. (1999). ML and MP bootstrap support above 50% are given at the first and second positions, respectively, above or below the branches.

The genus Nemania (including Euepixylon) receives high ML (99%), but low MP (55%) support and contains three highly-supported subclades (N1-N3 in Fig. 1). The ML and MP analyses reveal the same topologies within Nemania, except for minor differences (not shown). As these differences are not relevant within the context of our study, they are not further considered here.

The new Nemania species clustered together with N. plumbea (JF TH-04-01) with maximum ML and MP BS support, which is a sister group to N. delonicis, also with maximum ML and MP BS support (Fig. 1). The ITS sequence of the Iranian collection of N. serpens is almost identical to the ex-neotype sequence from N. serpens (TROM 174) from Granmo et al. (1999) and they clustered together with maximum ML BS support. The N. serpens clade has a sister group relationship with N. changningensis with maximum ML BS support. However, another isolate deposited as N. serpens (HAST 235) is not contained within the N. serpens clade, but remotely placed as sister species to N. chestersii, indicating a misidentification. The ex-holotype ITS sequence of N. prava (TROM 104) from Granmo et al. (1999) was almost identical to N. serpens (CBS 679.86) and both cluster together with maximum BS support; the latter was re-identified and given in the phylogenetic tree (Fig. 1) as N. prava (see discussion for details). Remarkably, the two previously accepted species of Euepixylon, the European E. udum and the North American E. sphaeriostomum, are placed within Nemania subclade N1, but are not revealed as closest relatives (Fig. 1), supporting their classification within Nemania.

Taxonomy

Nemania hyrcana Pourmoghaddam, Voglmayr & Khodaparast, sp. nov.

MycoBank No: 845436
Figs 2, 3

Holotype

Iran, Guilan Province, Astara County, Darband Forest, 38°21'26"N, 48°50'19"E, 17 m elev., on fallen branch of Parrotia persica, 7 October 2017, leg. M.J. Pourmoghaddam (GUM 1628; living culture MUCL 57704).

Etymology

The epithet is derived from “Hyrcania”, an ancient biogeographical region, located in the south of the Caspian Sea where the specimens were collected.

Diagnosis

differs from Nemania subaenea by its smaller ascospores [12–16 × 4.5–6 vs. 14–17.5 × 6–7.5 µm].

Teleomorph

Stromata superficial, effused-pulvinate, up to 2.5 cm long, 0.2–1.4 cm wide, sessile, attachment to substrate with narrow connective; surface brown, dark brown, dark grey with a slightly shiny metallic tone, with conspicuous perithecial mounds; carbonaceous tissue immediately beneath the surface and between the perithecia; tissue beneath the perithecial layer conspicuous. Perithecia obovoid to spherical, 0.5–0.7 mm high × 0.4–0.6 mm wide; ostioles papillate to coarsely papillate. Asci cylindrical, with amyloid, urn-shaped apical apparatus, 3.5–4 µm high × 2.5–3 µm wide, stipe up to 130 µm long, spore-bearing part 60–85 × 8–12 µm. Ascospores smooth, unicellular, pale brown to brown, ellipsoid, inequilateral, with narrowly rounded ends, 12–16 × 4.5–6 µm, with straight germ slit much less than spore-length on dorsal side; perispore indehiscent in 10% KOH.

Figure 2. 

Nemania hyrcana (Holotype GUM 1628) A, B close-up view of stromatal surface C close-up view of stromatal surface showing ostioles D, E stroma in horizontal section showing perithecia F mature ascus in water with long stipe G immature ascus in water H mature ascus in water I mature ascus in Melzer’s reagent J immature and mature ascospores in water K–M ascospores in water showing straight germ slit much less than spore-length. Scale bars: 2 mm (A); 0.8 mm (B); 0.5 mm (C, E); 0.4 mm (D); 20 µm (F–I); 10 µm (J–M).

Cultures and anamorph

Colonies on OA covering a 9 cm Petri dish in 2 wk, at first white, becoming buff (45), felty, azonate; finally, attaining cream to grey after 50 days. Anamorph geniculosporium-like. Conidiophores variables in length, hyaline to light brown. Conidiogenous cells up to 50 × 2.5–3.5 µm, hyaline to light brown. Conidia hyaline, ellipsoid with truncate base, 3.5–6 × 2.5–3.5 µm (Fig. 3).

Figure 3. 

Culture and anamorphic structures of Nemania hyrcana (MUCL 57704) on OA A, B surface of colony after (A) 7 and (B) 50 days of incubation C conidia D–F general view of anamorph structure, conidiophores, conidiogenous cells and mature conidia of N. hyrcana. Scale bars: 10 µm (C); 20 µm (D–F).

Other specimen examined

Iran, Golestan Province, Aliabad-e-Katul County, Kaboudwall Forest, 36°52'25"N, 54°53'14"E, 1076 m elev., on dead branches (host unknown), 10 November 2017, leg. M.J. Pourmoghaddam (GUM 1627; living culture MUCL 57703, IRAN 3734C).

Notes

This species resembles Nemania subaenea (Fig. 4), which was erected based on a single specimen from Guyana by Ju and Rogers (2002). Later, Fournier et al. (2018) reported it from Martinique and also mentioned N. plumbea, another single-specimen-based species from Thailand (Tang et al. 2007), which differs from N. subaenea only in the stromatal surface colour and in having slightly smaller ascospores (Tang et al. 2007). However, neither Ju and Rogers (2002) nor Fournier et al. (2018), who proposed that N. plumbea should be regarded as a synonym of N. subaenea, studied the cultures and anamorph of the neotropical species. The type of N. plumbea, on the other hand, was cultured and DNA sequences are available for comparison with the Iranian species. A comparison of these sequence data revealed significant differences between the two Iranian strains of N. hyrcana (MUCL 57703/ MUCL 57704) and the ex-type strain of N. plumbea (29/31 bp differences of 494 nucleotide characters in the ITS: 19/20 substitutions, 10/11 indels; 2 bp differences of 764 nucleotide characters in the LSU: 2 substitutions; 27 bp differences of 884 nucleotide characters in the RPB2: 28/27 substitutions; and 319/321 bp differences of 1422 nucleotide characters in the TUB2: 279/282 substitutions, 40/39 indels). This supports the erection of a new species for the Iranian fungus, for which multiple specimens and two cultures are available. Even if N. plumbea is not regarded as a synonym of N. subaenea, it should be kept in mind that both taxa are derived from tropical areas that are far away from Iran.

Figure 4. 

Nemania subaenea (isotype) A herbarium label B close-up view of stromatal surface C close-up view of stromatal surface showing ostioles D, E stroma in horizontal section showing perithecia F immature ascus in water G ascus apical plug in Melzer’s reagent H immature and mature ascospores in water I ascospore in water showing straight germ slit much less than spore-length. Scale bars: 2 mm (B); 0.8 mm (C); 1 mm (D); 0.5 mm (E); 20 µm (F); 10 µm (G–I).

Nemania serpens (Pers.) Gray, Nat. Arr. Brit. Pl. (London) 1: 516 (1821).

Figs 5, 6

Teleomorph

Stromata superficial, effused-pulvinate, up to 4 cm long × 0.2–1.2 cm wide, sessile, attachment to substrate with strong connective; surface dark brown to black, with conspicuous perithecial mounds, carbonaceous immediately beneath surface; tissue between and beneath perithecia black to dark brown. Perithecia obovoid, 0.35–0.65 mm high × 0.25–0.4 mm wide, ostioles papillate to coarsely papillate. Asci cylindrical, stipe up to 130 µm long, spore-bearing part 55–70 × 7–9 µm, apical apparatus not bluing in Melzer’s reagent, dextrinoid (= red to red brown) in Lugol’s solution. Ascospores smooth, unicellular, pale brown to brown, ellipsoid, inequilateral, with narrowly or broadly rounded ends, 10–14 × 4–5(–6) µm, with straight germ slit much less than spore-length; perispore indehiscent in 10% KOH.

Figure 5. 

Nemania serpens (GUM 1625) A, B close-up view of stroma surface C close-up view of stroma surface showing ostioles D stroma in vertical section showing perithecia E, F mature asci in water G mature ascus in Melzer’s reagent, showing the inamyloid (not bluing) ascal apical apparatus H, I mature ascus in Lugol’s solution, showing the dextrinoid (= red to red brown) ascal apical apparatus J ascospore in water K ascospores in water showing straight germ slit much less than spore-length. Scale bars: 3 mm (A); 1 mm (B); 0.6 mm (C); 0.5 mm (D); 20 µm (E–I); 10 µm (J, K).

Cultures and anamorph

Colonies on OA covering a 9 cm Petri dish in 18 days, at first white becoming Vinaceous (57), felty, azonate; finally, attaining Amber (47) to Honey (64) after 50 days. Anamorph geniculosporium-like. Conidiophores variables in length, hyaline to light brown. Conidiogenous cells up to 60 × 2.5–3.2 µm, hyaline to light brown. Conidia hyaline, ellipsoid with truncate base, 3–4.8 × 2–3.5 µm (Fig. 6).

Figure 6. 

Culture and anamorphic structures of Nemania serpens (MUCL 57702) on OA A, B surface of colony after (A) 7 and (B) 50 days of incubation of N. serpens C conidia of N. serpens D, E general view of anamorph structure, conidiophores, conidiogenous cells and mature conidia of N. serpens. Scale bars: 10 µm (C); 20 µm (D, E).

Specimens examined

Iran, Mazandaran Province, Ramsar County, Safarud Forest, 36°53'49"N, 50°35'29"E, 815 m elev., on fallen branch of Parrotia persica, 29 October 2016, leg. M.J. Pourmoghaddam (GUM 1625; living culture MUCL 57702, IRAN 3735C); Guilan Province, Astara County, 38°23'04"N, 48°51'45.10"E, 1 m elev., on fallen branch of Parrotia persica, 22 October 2021, leg. M.J. Pourmoghaddam (GUM 1903).

Notes

Nemania serpens is a very common fungus in Europe (Petrini and Rogers 1986; http://pyrenomycetes.free.fr/, accessed 8 Aug 2022). In combination with pale olive brown ascospores with broadly rounded ends and with a short inconspicuous germ slit, N. serpens is characterised by a dextrinoid reaction of the ascal apical apparatus in Lugol’s solution, while it does not react in Melzer’s reagent, which is an exceptional combination within Nemania (Granmo et al. 1999; http://pyrenomycetes.free.fr/, accessed 8 Aug 2022). Most of the characters of the Iranian specimens are in accordance with the neotype specimen (Fig. 7; Ju and Rogers 2002), aside from insignificant variations in the size of ascospores. We studied the neotype material and did not observe a conspicuous ascal apical apparatus as described by Ju and Rogers (2002). Morphological species identification of the Iranian specimens is corroborated by the ITS sequence data, as the Iranian and the ex-neotype sequence of N. serpens are almost identical (3 substitutions, 3 gaps). Finally, we would like to mention that, for the neotype specimen, Daranagama et al. (2018) erroneously described the ascal apical apparatus as bluing (I+) in Melzer’s reagent, while their fig. 7h clearly shows a not bluing (I-) ascal apical apparatus.

Figure 7. 

Nemania serpens (neotype) A herbarium label B stromata on wood C, D close-up view of stroma surface E close-up view of stroma surface showing ostioles F, G mature ascus in water H mature ascus in Melzer’s reagent, showing the inamyloid (not bluing) ascal apical apparatus I ascospores in water showing straight germ slit much less than spore-length J, K ascospores in water. Scale bars: 3 mm (C); 1 mm (D); 0.5 mm (E); 20 µm (F–H); 10 µm (I–K).

Nemania diffusa (Sowerby) S.F. Gray, Nat. Arr. Brit. Pl. (London) 1: 517 (1821).

Fig. 8

Teleomorph

Stromata superficial, effused-pulvinate, discoid, up to 2 cm long × 0.3–1.5 cm wide, sessile, attachment to substrate with narrow connective; surface dark brown to blackish-brown, with inconspicuous perithecial mounds, carbonaceous immediately beneath surface; tissue between and beneath perithecia black to dark brown. Perithecia obovoid to cylindrical, 0.5–0.8 mm high × 0.3–0.5 mm wide. Ostioles papillate to coarsely papillate. Asci cylindrical, with amyloid, urn-shaped apical apparatus, 2–3 µm high × 1.5–2 µm wide, stipe up to 100 µm long, spore-bearing part 70–80 × 7–10 µm. Ascospores smooth, unicellular, brown to dark brown, ellipsoid, inequilateral, with narrowly rounded ends, 9.5–13(–14) × 4.5–6.5 µm, with straight germ slit spore-length on flattened side; perispore indehiscent in 10% KOH.

Specimen examined

Iran, Guilan Province, Rezvanshahr County, 37°37'52"N, 40°02'18"E, 7 m elev., on fallen branch of Quercus castaneifolia, 6 October 2016, leg. M.J. Pourmoghaddam (GUM 1626), ITS and LSU sequences GenBank OP352258 and OP352270, respectively.

Notes

Nemania diffusa, originally described from England (Sowerby 1803), is a widespread and fairly common species in Europe (Fournier et al. 2018). It has also been reported from North and South America (Petrini and Rogers 1986), Papua-New Guinea (Van der Gucht 1995) and Taiwan (Ju and Rogers 1999), but it has yet to be proven whether all these morphologically identified accessions are conspecific with the European ones. The Iranian specimen is in accordance with previous descriptions by Ju and Rogers (2002). It can be differentiated from N. albocincta by its larger ascospores [9.5–13.5 × (4.5–)5–6 vs. 8–10 × 4–5 µm], which are also more equilateral. Nemania obscura also differs from it in stromatal features and smaller, strongly inequilateral ascospores (8.2–9.4 × 4.5–5.3 µm) with subacute ends. Despite several attempts, we could not achieve a living culture. Therefore, to confirm our morphological species identification, we extracted DNA from stromata and performed PCR (ITS/LSU) and sequencing according to Pourmoghaddam et al. (2018). The ITS sequence of the Iranian collection (OP352258) is completely identical to numerous sequences of European accessions of N. diffusa, some of which are morphologically well-documented to represent the species (e.g. MW489542 from Switzerland; Senn-Irlet et al. 2021), confirming the species identification. However, as RPB2 and TUB2 could not be obtained, the Iranian accession of N. diffusa was not added to the phylogenetic multi-locus analyses.

Figure 8. 

Nemania diffusa (GUM 1626) A stromatal habit B close-up view of stromatal surface C, D close-up view of stroma surface showing ostioles E mature ascus in water F, G mature asci in Melzer’s reagent showing the amyloid (bluing) ascal apical apparatus H ascospore showing straight germ slit. Scale bars: 3 mm (B); 1.5 mm (C); 0.8 mm (D); 20 µm (E–G); 10 µm (H).

Discussion

In this study, we examined the phylogenetic relationships of our fresh collections with all species of Nemania for which multigene sequence data are available. We have performed a multigene analysis using ITS, LSU, RPB2 and TUB2 sequence data to determine the phylogenetic placement of these species. Nemania (including Euepixylon) clearly forms a monophyletic clade in the phylogenetic analysis which has been placed in Xylariaceae for a long time (Hyde et al. 2020). The results of our phylogenetic analyses agree well with those of Pi et al. (2021), their clade N6 corresponding to our clade N1, their clade N5 to our clade N2 and their clades N1–4 to our clade N3.

Remarkably, in the phylogenetic analyses, the two previously-accepted species of Euepixylon are not only contained within Nemania, but also do not form a monophyletic lineage, yet they are members of the same Nemania subclade 1 (N1; Fig. 1). Stroma morphology and the anamorph of Euepixylon matches Nemania, the main distinguishing feature being poroid (Euepixylon) vs. straight, conspicuous or inconspicuous germ slits of variable length (Nemania; Læssøe and Spooner 1993, Granmo et al. 1999). When re-establishing the genus Euepixylon, already Læssøe and Spooner (1993) doubted whether the genus will survive in the long run. Considering the results of the phylogenetic analyses, germ site morphology is clearly not a good character to separate Euepixylon from Nemania and the former genus should be considered as a synonym of the latter, which has already been implemented by for example, Pi et al. (2021) and Voglmayr et al. (2022) and which we, therefore, also adopt here. Synonymy of both genera is further supported by the fact that the type species of Euepixylon (E. udum), as well as Nemania (N. serpens), are revealed to be closely related within the Nemania subclade 1 (N1).

Most Nemania species are morphologically highly similar, which makes species delimitation and identification based on morphology alone difficult and confusing (Granmo et al. 1999; Ju and Rogers 2002; Fournier et al. 2018). Recently, much progress in reliable species identification has been achieved by DNA sequence data, particularly protein-coding genes such as RPB2 or TUB2, which have superior resolution compared to ITS or LSU (Lücking et al. 2020; Stadler et al. 2020). However, an obstacle for an improved species delimitation and classification is the lack of sequences of type material or well-identified reference specimens in GenBank, which is particularly important for morphologically difficult and complex lineages. Nemania serpens, the type species of the genus, is a good example of these problems. Until the present study, no verified sequence data were available in GenBank for N. serpens and the various accessions deposited under this name do not form a monophylum in phylogenetic analyses (data not shown). However, it has been widely ignored that Granmo et al. (1999), who neotypified N. serpens with a recent Norwegian collection (TROM 174), also generated and published an ITS sequence of their neotype. The reason for disregarding this ex-neotype ITS sequence in subsequent studies lies the fact that Granmo et al. (1999) published their sequences in their Appendix 3, a colour figure of the ITS alignment they used for their phylogenetic analyses, but they did not deposit them in a public sequence repository. The ITS sequences of Granmo et al. (1999) can, therefore, only be added to a sequence matrix if they are transcribed from this colour figure alignment, which we have done here. The addition of the ex-neotype ITS sequence of N. serpens from Granmo et al. (1999) to our sequence matrix revealed a high similarity to our Iranian isolate that was identified as N. serpens by morphological comparison with the neotype specimen. The phylogenetic analyses also revealed that another isolate (HAST 235), commonly included as N. serpens in phylogenies, is not closely related to the neotype, but forms a highly-supported clade with another species, N. chestersii, which indicates that HAST 235 does not represent N. serpens, but is misidentified.

A further example for incorrectly labelled sequences that could be clarified by inclusion of the ITS sequences of Granmo et al. (1999) refers to CBS 679.86, another accession erroneously deposited as N. serpens in GenBank. In the phylogenetic analyses, the accession CBS 679.86 has an ITS sequence almost identical to that of the ex-holotype sequence of N. prava from Granmo et al. (1999). However, this becomes conclusive considering that culture CBS 679.86 represents an ex-paratype culture of Hypoxylon atropurpureum var. brevistipitatum (Petrini and Rogers 1986), a synonym of Nemania prava (Granmo et al. 1999). Granmo et al. (1999) confirmed this synonymy by revealing identical ITS sequences for the holotype of N. prava, the holotype of Hypoxylon atropurpureum var. brevistipitatum and another paratype of the latter. It remains yet unclear why the sequences of culture CBS 679.86 have been deposited as N. serpens in GenBank. These exemplary cases once again demonstrate that species names of GenBank sequences, as well as the sources of the sequence data, need to be critically evaluated, in particular in taxonomically difficult groups.

Stromata of Nemania are highly carbonised and do not contain large amounts of secondary metabolites, as is the case in other phylogenetically closely-related genera, such as Dematophora and Rosellinia. Only small amounts of xylaral (in N. diffusa; Stadler et al. 2008) and BNT (in young Nemania specimens; Stadler and Hellwig 2005) have so far been detected.

Since the cultures of Xylariaceae are, in general, rich in production of secondary metabolites (Helaly et al. 2018; Becker and Stadler 2021), further analysis of Nemania species may be useful for a better taxonomic classification in the future. Chestersiene and furanone production have so far been described as characteristic metabolites, delimiting Nemania from Hypoxylon (Whalley and Edwards 1995). Even though this work was based on strains that are apparently not deposited in public collections, the respective compounds have, indeed, not been found in any other fungal genus. The lack of extant cultures for many described xylariaceous species, including for example, Rosellinia and Dematophora (cf. Wittstein et al. 2020), precludes comprehensive chemotaxonomic studies in the family. Recent progress in the generation of high-quality genome sequences could also enable the search for possible discriminatory biosynthetic gene clusters, as presence or absence of a cluster can serve as a predictor of the taxonomic relationship, which might be an option for future comprehensive sequencing campaigns (Wibberg et al. 2021; Kuhnert et al. 2021).

Xylariaceae is one of the most important ascomycete families found in the north of Iran which has regions with subtropical climates and houses numerous species. Until recently, studies on species biodiversity of Xylariaceae focused on the genera Xylaria (Hashemi et al. 2014, 2015), Kretzschmaria (Pourmoghaddam et al. 2018) and Rosellinia (Pourmoghaddam et al. 2022), which we here extend to the genus Nemania.

Acknowledgements

This work was supported by a grant from the Iran National Science Foundation (INSF) No. 99027605 to Mohammad Javad Pourmoghaddam. Christopher Lambert is grateful for a Ph.D. stipend from the Life Science Foundation, Braunschweig, Germany. This work also benefitted from the sharing of expertise within the DFG priority programme ‘‘Taxon-Omics: New Approaches for Discovering and Naming Biodiversity’’ (SPP 1991) funded by the Deutsche Forschungsgemeinschaft. Furthermore, we also gratefully acknowledge support from the curators of the Herbaria WSP and TROM who provided isotype and neotype specimens for the present study and to W. Till (WU) who managed the herbarium loans.

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Supplementary material

Supplementary material 1 

Alignment

Mohammad Javad Pourmoghaddam, Christopher Lambert, Hermann Voglmayr, Seyed Akbar Khodaparast, Irmgard Krisai-Greilhuber, Marc Stadler

Data type: Nex file.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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