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Research Article
Morphology and multigene phylogeny reveal three new species of Distoseptispora (Distoseptisporales, Distoseptisporaceae) on palms (Arecaceae) from peatswamp areas in southern Thailand
expand article infoOmid Karimi‡§, K. W. Thilini Chethana§, Antonio R. G. de Farias§, Raheleh Asghari§, Saithong Kaewchai|, Kevin D. Hyde§#, Qirui Li‡
‡ Guizhou Medical University, Guiyang, China
§ Mae Fah Luang University, Chiang Rai, Thailand
| Princess of Naradhiwas University, Narathiwat, Thailand
¶ Mushroom Research Foundation, Chiang Rai, Thailand
# Zhongkai University of Agriculture and Engineering, Guangzhou, China

Corresponding author: Qirui Li ( lqrnd2008@163.com )

Academic editor: Nalin Wijayawardene
© 2024 Omid Karimi, K. W. Thilini Chethana, Antonio R. G. de Farias, Raheleh Asghari, Saithong Kaewchai, Kevin D. Hyde, Qirui Li.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Karimi O, Chethana KWT, de Farias ARG, Asghari R, Kaewchai S, Hyde KD, Li Q (2024) Morphology and multigene phylogeny reveal three new species of Distoseptispora (Distoseptisporales, Distoseptisporaceae) on palms (Arecaceae) from peatswamp areas in southern Thailand. MycoKeys 102: 55-81. https://doi.org/10.3897/mycokeys.102.112815
Open Access

Abstract

Peatswamp forest is a unique habitat that supports high biodiversity, particularly fungal diversity. The current study collected submerged and dead plant parts from Eleiodoxa conferta, Eugeissona tristis and Licuala paludosa from a peatswamp forest in Narathiwat Province, Thailand. Morphological features coupled with multigene phylogenetic analyses of ITS, LSU, rpb2 and tef1-α sequence data identified our isolates as new Distoseptispora species (viz. D. arecacearum sp. nov., D. eleiodoxae sp. nov. and D. narathiwatensis sp. nov.). Morphological descriptions, illustrations and notes are provided.

Key words

asexual morph, molecular phylogeny, novel taxa, saprobic fungi, Sordariomycetes, taxonomy

Introduction

Most peatswamp forests can be found in tropical rainforests where peat is submerged for most of the year and characterised by low nutrient contents and high acidity due to lack of fully decomposed plant materials (Page et al. 1999, 2011; Jackson et al. 2009; Lampela et al. 2016; Ratnayake 2020). Peatswamp forests are unique ecosystems due to their high species diversity and significant role in maintaining a stable global climate. They function as carbon sinks, storing twice as much carbon as all global forest biomass (Hakim et al. 2017; Fujimoto et al. 2019; Shuhada et al. 2020). Beyond carbon storage, peatlands offer valuable benefits. They play vital roles in the water cycle, storing and filtering water and mitigating floods by slowing peak flows. Home to diverse plants and animals, these wetlands support millions of people. Additionally, they hold archaeological relics and provide insights into past environmental conditions through their peat layers, aiding predictions about the future climate (Parish et al. 2008; Posa et al. 2011; Minayeva and Sirin 2012; UNEP 2022). Asian peatlands are amongst the most diverse and geographically extensive in the world, with over 160 million hectares and the majority of tropical peatlands are found in Southeast Asia (e.g. Brunei, Indonesia, Malaysia, Papua New Guinea and Thailand) (UNEP 2022).

These habitats support many flora, including an extensive number of bryophytes, ferns and palms (Arecaceae) (Prentice 2011; Rieley 2016). Arecaceae comprises iconic monocotyledonous flowering plants belonging to 188 genera and 2,585 species that are distributed throughout tropical and subtropical areas of the world. However, they are most diverse in highly threatened moist tropical forest habitats (Dransfield et al. 2008; Palmweb 2023; POWO 2023). In peatswamp forests, many palm species, such as Areca macrocalyx Zipp. ex Blume, Calamus concinnus Mart, Cyrtostachys renda Blume, Eugeissona tristis Griff, Eleiodoxa conferta (Griff.) Burret, Licuala longicalycata Furtado, L. paludosa Griff, Metroxylon sagu Rottb and Nenga pumila (Blume) H.Wendl. ex Schaedtler can be found (Calabon et al. 2022), exerting different biological functions.

Several studies on palm fungi have focused on saprobic, endophytic and plant pathogenic life modes from different habitats worldwide (Hyde 1988; Taylor et al. 1999; Fröhlich and Hyde 2000; Fröhlich et al. 2000; Hyde et al. 2000; Taylor and Hyde 2003; Pilantanapak et al. 2005; Lumyong et al. 2009; Liu et al. 2010; Wikee et al. 2013; Konta et al. 2016a, 2016b, 2016c, 2017, 2020a, 2020b, 2020c, 2021a, 2021b, 2023; Chou et al. 2019; El Meleigi et al. 2019; Kinge et al. 2019; Marin-Felix et al. 2019; Chen et al. 2020; Mapook et al. 2020; Zhang et al. 2020; Tian et al. 2022). Even though many palm trees grow in peatswamp forests, there are few records of fungal studies in these environments, mostly reported from Thailand (Pinruan et al. 2002, 2004a, 2004b, 2004c, 2004d, 2007, 2008, 2010a, 2010b, 2014; Pinnoi et al. 2003a, 2003b, 2004, 2006, 2009, 2010; Voglmayr and Yule 2006; Sivichai and Boonyuen 2010; Boonyuen et al. 2012), of which many lack molecular data. Pinnoi et al. (2006) studied saprobic fungi on dead palm material in the Sirindhorn peatswamp forest, Narathiwat Province, Thailand and listed 462 ascomycetous and basidiomycetous taxa from various parts of palm materials (such as dry, damp and submerged palm materials), based on morphological identification and also recorded five sporidesmium-like taxa. Pinnoi et al. (2009) identified 88 fungal species from 212 collections of Calamus sp. in Thailand, with six records resembling sporidesmium-like taxa.

Distoseptispora K.D. Hyde, McKenzie & Maharachch belongs to Distoseptisporaceae, Distoseptisporales, Sordariomycetes, Ascomycota and comprises sporidesmium-like taxa (Wijayawardene et al. 2022). Su et al. (2016) proposed Distoseptisporaceae to accommodate sporidesmium-like taxa with Distoseptispora as the type genus and D. fluminicola McKenzie, Hong Y. Su, Z.L. Luo & K.D. Hyde as the type species. Subsequently, Luo et al. (2019) introduced Distoseptisporales to accommodate Distoseptisporaceae, based on multigene phylogenetic analyses of LSU, SSU, rpb2 and tef1-α sequence data. Distoseptispora is characterised by short, septate, olivaceous to brown conidiophores. The conidiogenous cells are monoblastic and determinate, bearing acrogenous conidia that are brown, euseptate, distoseptate or muriform and cut off by cross walls at the basal cell with a basal scar (Yang et al. 2018). The genus exhibits morphology similar to Sporidesmium, but can be distinguished by having shorter conidiophores and darker conidia with pale round apexes (Su et al. 2016). To date, Distoseptispora comprises 65 species listed in the MycoBank database (https://www.mycobank.org/; Accessed in August 2023), with molecular data available for all reported species in the GenBank. The estimated divergence time for Distoseptisporaceae is approximately 44.21 million years ago (MYA), after the Tertiary–Cretaceous extinction event (Hyde et al. 2020), which could have created conducive conditions for Distoseptispora to thrive as a saprobe on various hosts (Phukhamsakda et al. 2022).

Peatswamp forests are unique, endangered ecosystems and their fungal biodiversity is little known. Therefore, in the current study, we aimed to study fungal species on different palm materials from peatswamp forests in Thailand, based on morphology and phylogeny. This study introduces three new species, Distoseptispora arecacearum, D. eleiodoxae and D. narathiwatensis, associated with Eleiodoxa conferta, Eugeissona tristis and Licuala paludosa from a peatswamp forest in Narathiwat Province, Thailand, based on morphological characteristics coupled with multigene phylogenetic analyses (ITS, LSU, rpb2 and tef1-α).

Materials and methods

Sample collection, morphological study and isolation

Decaying leaves of Eleiodoxa conferta, Eugeissona tristis and Licuala paludosa were collected from a peatswamp forest in Narathiwat Province, Thailand, in April 2022. Wet (submerged) and dry (aerial part) palm specimens were placed in plastic bags and brought to the laboratory. The submerged materials were kept moist and examined periodically for fungal fruiting structures and the dry materials were examined immediately or incubated in moisture chambers. Small pieces of the collected specimens were examined under a Leica EZ4 stereomicroscope and isolated into axenic culture using a single spore technique (Choi et al. 1999) in the Difco potato dextrose agar (PDA) media supplemented with Streptomycin 0.5 g/l. Germinating spores were transferred to new PDA and incubated at 25 ± 1 °C in dark conditions for two weeks. The micro-morphological characters were examined and photographed using a digital camera (Canon 600D, Japan) fitted to a compound microscope (Nikon ECLIPSE Ni, Japan) and the measurements were obtained using the Tarosoft (R) Image Frame Work programme version 0.9.7 (Tarosoft, Thailand). The ex-type living cultures were deposited at the Mae Fah Luang University Culture Collection (MFLUCC) and the herbarium specimens at the Mae Fah Luang University Herbarium (MFLU). The Facesoffungi (FoF) and Index Fungorum numbers were obtained, as explained in Jayasiri et al. (2015) and Index Fungorum (http://www.indexfungorum.org), respectively.

DNA extraction, PCR amplification and sequencing

Genomic DNA was extracted from fresh fungal mycelia using the Biospin Fungus Genomic DNA Extraction Kit (BioFlux, P.R. China), according to the manufacturer’s standard protocol. Polymerase chain reactions (PCR) were conducted to amplify the internal transcribed spacer region rDNA (ITS), 28S large subunit rDNA (LSU), RNA polymerase II second largest subunit (rpb2) and translation elongation factor 1-alpha (tef1-α) using primers and conditions listed in Table 1. The PCR products were visualised on 1% agarose gels, stained with 4S Green Stain and sequenced at SolGent Co., Ltd (South Korea).

Table 1.
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Primers and PCR protocols.

Gene regions Primers PCR conditions References
ITS ITS5/ITS4 95 °C for 4 min, 40 cycles of 94 °C for 45 s, 56 °C for 1 min and 72 °C for 2 min, 72 °C for 10 min White et al. (1990)
LSU LR0R/LR5 94 °C for 3 min, 40 cycles of 94 °C for 30 s, 50 °C for 45 s and 72 °C for 2 min, 72 °C for 10 min Vilgalys and Hester (1990), Rehner and Samuels (1994)
rpb2 fRPB2-5f/fRPB2-7cR 95 °C for 5 min, 35 cycles of 95 °C for 1 min, 55 °C for 1.25 min and 72 °C for 2 min, 72 °C for 10 min Liu et al. (1999)
tef1-α EF1-983F/EF1-2218R 94 °C for 3 min, 40 cycles of 94 °C for 30 s, 54 °C for 50 s and 72 °C for 2 min, 72 °C for 10 min Rehner (2001)

Sequence alignment and Phylogenetic analyses

The obtained sequences of ITS, LSU, rpb2 and tef1-α were assembled using SeqMan software version 7.1.0 (DNASTAR Inc., WI) and subjected to BLASTn search against the GenBank nucleotide database at National Center for Biotechnology Information (NCBI) to identify closely-related sequences. Sequence data of related taxa were obtained from previous publications (Su et al. 2016; Yang et al. 2018, 2021; Crous et al. 2019; Hyde et al. 2019; Luo et al. 2019; Monkai et al. 2020; Phukhamsakda et al. 2020; Sun et al. 2020; Ma et al. 2022; Zhai et al. 2022; Zhang et al. 2022; Afshari et al. 2023) and downloaded from the GenBank database (Table 2). The sequences were aligned using MAFFT v.7 online web server (http://mafft.cbrc.jp/alignment/server/index.html, Katoh et al. 2019) under default settings and the alignments were trimmed in NGPhylogeny online web server (https://ngphylogeny.fr/workflows/wkmake/3a4ab1bef8e7ff3c, Lemoine et al. 2019). The sequence datasets were combined using SequenceMatrix software version 1.9 (Vaidya et al. 2011). The Maximum Likelihood (ML) phylogenetic analysis was run in the CIPRES Science Gateway platform (Miller et al. 2010), using RAxMLHPC2 on the XSEDE (v. 8.2.10) tool (Stamatakis 2014) under the GTRCAT substitution model and 1,000 non-parametric bootstrap replicates. For Bayesian Inference (BI) analysis, the optimal substitution model of each region was determined using jModelTest2 on the CIPRES Science Gateway under the Akaike Information Criterion (AIC) (Darriba et al. 2012). Bayesian analysis was performed using MrBayes v. 3.2.6 on XSEDE at the CIPRES Science Gateway with four simultaneous Markov Chain runs for 1,000,000 generations. The resulting trees were visualised in FigTree v. 1.4.0 (Rambaut 2012) and edited in Microsoft PowerPoint 2019 (Forethought, Inc., The United States).

Table 2.
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GenBank accession numbers used in the phylogenetic analyses.

Taxon Identifier GenBank accession number
ITS LSU rpb2 tef1-α
Aquapteridospora aquatica MFLUCC 17-2371* NR172447 NG075413 – –
A. fusiformis MFLU 18-1601* MK828652 MK849798 – MN194056
Distoseptispora adscendens HKUCC 10820 – DQ408561 DQ435092 –
D. amniculi MFLUCC 17-2129* MZ868770 MZ868761 MZ892982 –
D. appendiculata MFLUCC 18-0259* MN163009 MN163023 – MN174866
D. aqualignicola KUNCC 21-10729* OK341186 ON400845 OP413474 OP413480
D. aquamyces KUNCC 21-10732* OK341187 OK341199 OP413476 OP413482
D. aquatica MFLUCC 15-0374* MF077552 KU376268 – –
D. aquatica MFLUCC 16-0904 MK828649 MK849794 – MN194053
D. aquatica MFLUCC 18-0646 MK828648 MK849793 – MN194052
D. aquatica S-965 MK828647 MK849792 MN124537 MN194051
D. aquisubtropica GZCC 22-0075* ON527933 ON527941 ON533685 ON533677
D. arecacearum MFLUCC 23-0211* OR234707 OR510857 OR250439 OR250442
D. arecacearum MFLUCC 23-0212 OR354399 OR510860 OR481048 OR481045
D. atroviridis GZCC 20-0511* MZ868772 MZ868763 MZ892984 MZ892978
D. atroviridis GZCC 19-0531 MW133915 MZ227223 – –
D. bambusae MFLUCC 20-0091* NR170068 NG074430 MT232881 MT232880
D. bambusae MFLU 17-1653 MT232712 MT232717 MT232882 –
D. bangkokensis MFLUCC 18-0262* MZ518205 MZ518206 – –
D. cangshanensis MFLUCC 16-0970* MG979754 MG979761 – MG988419
D. caricis CPC: 36498* NR166325 MN567632 MN556805 –
D. caricis CPC: 36442 MN562125 – MN556806 –
D. chinensis GZCC 21-0665 MZ474871 MZ474867 – MZ501609
D. clematidis MFLUCC 17-2145* MT310661 MT214617 MT394721 –
D. clematidis KUN-HKAS:112708 MW723056 MW879523 – –
D. crassispora KUMCC 21-10726* OK310698 OK341196 OP413473 OP413479
D. curvularia KUMCC 21-10725* OK310697 OK341195 OP413472 OP413478
D. cylindricospora KUN-HKAS:115796* OK491122 OK513523 – OK524220
D. dehongensis KUMCC 18-0090* MK085061 MK079662 – MK087659
D. dipterocarpi MFLUCC 22-0104 * OP600053 OP600052 OP595140 –
D. effusa GZCC 19-0532* MW133916 MZ227224 – –
D. eleiodoxae MFLUCC 23-0213* OR234706 OR510856 OR250438 OR250441
D. eleiodoxae MFLUCC 23-0214 OR354398 OR510859 OR481047 OR481044
D. euseptata MFLUCC 20-0154* MW081539 MW081544 MW151860 –
D. euseptata MFLU 20-0568 MW081540 MW081545 MW084996 MW084994
D. fasciculata KUMCC 19-0081* NR172452 NG075417 – MW396656
D. fluminicola MFLUCC 15-0417* MF077553 KU376270 – –
D. fusiformis GZCC 20-0512* MZ868773 MZ868764 MZ892985 MZ892979
D. guizhouensis GZCC 21-0666* MZ474868 MZ474869 MZ501611 MZ501610
D. guttulata MFLUCC 16-0183* MF077543 MF077554 – MF135651
D. hyalina MFLUCC 17-2128* MZ868769 MZ868760 MZ892981 MZ892976
D. hydei MFLUCC 20-0115* MT734661 MT742830 MT767128 –
D. lancangjiangensis DLUCC 1864* MW723055 MW879522 – –
D. leonensis HKUCC 10822 – DQ408566 DQ435089 –
D. licualae MFLUCC 14-1163* ON650686 ON650675 – ON734007
D. lignicola MFLUCC 18-0198* MK828651 MK849797 – –
D. longispora HFJAU 0705* MH555359 MH555357 – –
D. martinii CGMCC 3.18651 KU999975 KX033566 – –
D. meilingensis JAUCC 4728 OK562391 OK562397 – OK562409
D. mengsongensis HJAUP C2126* OP787876 OP787874 – OP961937
D. multiseptata MFLUCC 15-0609* KX710145 KX710140 – MF135659
D. nabanheensis HJAUP C2003* OP787877 OP787873 – OP961935
D. narathiwatensis MFLUCC 23-0215* OR234708 OR510858 OR250440 OR250443
D. narathiwatensis MFLUCC 23-0216 OR354400 OR510861 OR481049 OR481046
D. neorostrata MFLUCC 18-0376* MN163008 MN163017 – –
D. nonrostrata KUNCC 21-10730* OK310699 OK341198 OP413475 OP413481
D. obclavata MFLUCC 18-0329* MN163012 MN163010 – –
D. obpyriformis MFLUCC 17-1694* – MG979764 MG988415 MG988422
D. obpyriformis DLUCC 0867 MG979757 MG979765 MG988416 MG988423
D. pachyconidia KUMCC 21-10724* OK310696 OK341194 OP413471 OP413477
D. palmarum MFLUCC 18-1446* MK085062 MK079663 MK087670 MK087660
D. palmarum MFLU 18-0588 NR165897 NG067856 – –
D. phangngaensis MFLUCC 16-0857* NR166230 – – MF135653
D. rayongensis MFLUCC 18-0415* NR171938 NG073624 – MH463253
D. rayongensis MFLU 18-1045 MH457172 MH457137 MH463255 –
D. rostrata MFLUCC 16-0969* MG979758 MG979766 MG988417 MG988424
D. rostrata DLUCC 0885 MG979759 MG979767 – MG988425
D. rostrata MFLU 18-0479 NR157552 NG064513 – –
D. saprophytica MFLUCC 18-1238* NR172454 NG075419 MW504069 MW396651
D. septata GZCC 22-0078* ON527939 ON527947 ON533690 ON533683
D. sinensis HJAUP C2044* OP787878 OP787875 – OP961936
D. songkhlaensis MFLUCC 18-1234* MW286482 MW287755 – MW396642
D. submersa MFLUCC 16-0946 MG979760 MG979768 MG988418 MG988426
D. suoluoensis MFLUCC 17-0224* NR168764 NG068552 – MF135654
D. tectonae MFLUCC 12-0291* KX751711 KX751713 KX751708 KX751710
D. tectonigena MFLUCC 12-0292* NR154018 KX751714 KX751709 –
D. thailandica MFLUCC 16-0270* MH275060 MH260292 – MH412767
D. thysanolaenae KUN-HKAS: 112710 MW723057 MW879524 – MW729783
D. thysanolaenae KUMCC 18-0182 MK045851 MK064091 – MK086031
D. tropica GZCC 22-0076* ON527935 ON527943 ON533687 ON533679
D. verrucosa GZCC 20-0434* MZ868771 MZ868762 MZ892983 MZ892977
D. wuzhishanensis GZCC 22-0077* ON527938 ON527946 – ON533682
D. xishuangbannaensis KUMCC 17-0290* MH275061 MH260293 MH412754 MH412768
D. yongxiuensis JAUCC 4725 OK562388 OK562394 – OK562406
D. yongxiuensis JAUCC 4726 OK562389 OK562395 – OK562407
D. yunjushanensis JAUCC 4723 OK562392 OK562398 – OK562411
D. yunjushanensis JAUCC 4724 OK562393 OK562399 – OK562410
D. yunnanensis MFLUCC 20-0153* MW081541 MW081546 MW151861 MW081541

Ex-type strains are indicated with an asterisk (*) after the collection number; “–” indicates unavailable sequences; sequences produced in the current study are in bold.

Abbreviations

CGMCC: China General Microbiological Culture Collection Center, Chinese Academy of Sciences, Beijing, China; CPC: Collection of P.W. Crous, Utrecht, The Netherlands; DLUCC: Dali University Culture Collection, Yunnan, China; GZCC: Guizhou Culture Collection, Gui Yang, China; HFJAU: Herbarium of Fungi, Jiangxi Agricultural University, Nanchang, China; HKUCC: The University of Hong Kong Culture Collection, Hong Kong, China; JAUCC: Jiangxi Agricultural University Culture Collection, Nanchang, China; KUMCC: Kunming Institute of Botany Culture Collection, Kunming, China; KUN-HKAS: Herbarium of Cryptogams, Kunming Institute of Botany Academia Sinica; MFLU: Mae Fah Luang University Herbarium, Chiang Rai, Thailand; MFLUCC: Mae Fah Luang University Culture Collection, Chiang Rai, Thailand.

Results

Phylogenetic analyses

The combined ITS, LSU, rpb2 and tef1-α dataset consisted of 83 strains, with Aquapteridospora aquatica X.D. Yu, W. Dong & H. Zhang (MFLUCC 17-2371) and A. fusiformis Z.L. Luo, D.F. Bao, H.Y. Su & K.D. Hyde (MFLU 18-1601) as outgroup taxa (Table 2). The final alignment comprised 3,383 characters (ITS: 567 bp, LSU: 855 bp, rpb2: 1,051 bp, tef1-α: 909 bp), including gaps. The final ML optimisation likelihood value of the best RAxML tree was -33894.57 and the matrix had 1,637 distinct alignment patterns, with 29.85% undetermined characters or gaps. Estimated base frequencies were as follows: A = 0.240315, C = 0.262752, G = 0.283175, T = 0.213758; substitution rates AC = 1.324179, AG = 3.427671, AT = 1.239665, CG = 0.914354, CT = 6.950002, GT = 1.0; gamma distribution shape parameter α = 0.273123. The RAxML and Bayesian analyses yielded a similar tree topology.

The topology of our phylogenetic tree is nearly identical to previous publications, but there are some differences, which may be due to different taxon sampling. As new species are introduced into this genus frequently, taxon sampling conducted for different studies varies. In our phylogenetic analyses, two strains of the new species Distoseptispora arecacearum (MFLUCC 23-0211 and MFLUCC 23-0212) formed a robust subclade (100% ML, 1.00 PP) independently. The species has close relationships with D. amniculi (MFLUCC 17-2129), D. bangkokensis (MFLUCC 18-0262), D. cangshanensis (MFLUCC 16-0970) and D. cylindricospora (KUN-HKAS:115796) with 82% ML bootstrap support. The other two new species, D. eleiodoxae and D. narathiwatensis, clustered with D. saprophytica (MFLUCC 18-1238), D. palmarum (MFLU 18-0588 and MFLUCC 18-1446) and D. tropica (GZCC 22-0076) with 0.96 PP support. Distoseptispora eleiodoxae (strains MFLUCC 23-0213 and MFLUCC 23-0214) formed a robust subclade (100% ML, 1.00 PP) basal to D. narathiwatensis (MFLUCC 23-0215 and MFLUCC 23-0216), D. saprophytica (MFLUCC 18-1238) and D. palmarum (MFLU 18-0588 and MFLUCC 18-1446) with 90% ML and 1.00 PP support. Distoseptispora narathiwatensis (MFLUCC 23-0215 and MFLUCC 23-0216) formed a sister clade with D. saprophytica (MFLUCC 18-1238) with 100% ML and 1.00 PP support (Fig. 1).

Figure 1. 

Maximum Likelihood tree generated from combined ITS, LSU, rpb2 and tef1-α sequence data. Bootstrap support values ≥ 65% and Bayesian posterior probabilities ≥ 0.95 are demonstrated at the nodes. The new taxa are indicated in red bold. Ex-type strains are in black bold.

Taxonomy

Distoseptispora arecacearum O. Karimi, Q.R. Li & K.D. Hyde, sp. nov.

Index Fungorum number: IF900843
Facesoffungi number: FoF14756
Fig. 2

Etymology

The epithet ‘‘arecacearum’’ refers to host family, Aceraceae.

Holotype

MFLU 23-0276.

Description

Saprobic on submerged rachis of Licuala paludosa in peatswamp forest. Sexual morph: Undetermined. Asexual morph: Hyphomycetous. Colonies gregarious or scattered, effuse, hairy, dark brown to black. Mycelium mostly immersed, composed of branched, septate, smooth hyphae. Conidiophores 70–140 × 5.1–6.3 µm (x̄ = 110 × 5.5 µm, n = 20), macronematous, mononematous, unbranched, erect, straight or flexuous, cylindrical, smooth, thick-walled, brown, 4–7 septa, sometimes consists a swollen cell in the middle or towards the apex. Conidiogenous cells 13–25 × 4.5–6 µm (x̄ = 17 × 5 µm, n = 20), monoblastic or polyblastic, terminal or subterminal, determinate, cylindrical, brown. Conidia 25–60 × 7–17 µm (x̄ = 44 × 10 µm, n = 30), acrogenous, solitary, cylindrical, obclavate to obpyriform or irregular, straight or curved, 4–10-distoseptate, brown, thick-walled, smooth, round apex, truncated base, sometimes with percurrent regeneration forming a secondary conidium from the conidial apex.

Figure 2. 

Distoseptispora arecacearum (MFLU 23-0276, holotype) a host material b colonies on the substrate c–e conidiophores and conidia f–i conidia j, k culture on PDA. Scale bars: 200 µm (b); 50 µm (c–e); 10 µm (f–i).

Culture characteristics

Colonies grown on PDA, reaching 50 mm in diameter after 15 days at 25 °C, under dark conditions, circular, fimbriate edge, flat, dull surface, radiating outwards, felted, medium dense, without pigment diffusion and sporulation, brown on the top, reverse dark brown to black.

Material examined

Thailand. Narathiwat Province: Yi-ngo District, peatswamp forest, on submerged rachis of Licuala paludosa, 06 April 2022, Omid Karimi, S5PP3SG (MFLU 23-0276, holotype); ex-type culture MFLUCC 23-0211, additional living culture MFLUCC 23-0212.

Notes

Morphologically, our proposed new species is similar to Distoseptispora dehongensis W. Dong, H. Zhang & K.D. Hyde and D. obpyriformis Z.L. Luo & H.Y. Su in having macronematous, mononematous, unbranched, erect, straight or flexuous, cylindrical, septate conidiophores, terminal, determinate, cylindrical, brown conidiogenous cells and acrogenous, distoseptate, straight or curved conidia (Luo et al. 2018; Hyde et al. 2019). However, our isolate differs from D. dehongensis (HKAS 101738) in having longer and wider conidiophores (70–140 × 5.1–6.3 µm vs. 45–80 × 4–5 µm), with swollen cells, longer and wider conidia (25–60 × 7–17 µm vs. 17–30 × 7.5–10 µm) and more distosepta (4–10-distoseptate vs. 3–5-distoseptate). Distoseptispora arecacearum (MFLU 23-0276) differs from D. obpyriformis (MFLU 18–0476) in having conidiophores with swollen cells and shorter conidia (25–60 µm vs. 53–71 µm) (Luo et al. 2018). The BLASTn searches of the ITS sequence of D. arecacearum (MFLUCC 23-0211) resulted in D. aquatica Z.L. Luo, H.Y. Su & K.D. Hyde (MFLUCC 18-0646) with 92.21% similarity across 100% of the query sequence coverage, while the LSU sequence of D. arecacearum has 99.09% similarity across 100% of the sequence coverage with D. phangngaensis J. Yang, Maharachch. & K.D. Hyde (MFLUCC 16-0857). Distoseptispora arecacearum (MFLU 23-0276) is easily distinguishable from D. aquatica (HKAS 83991) in having longer conidiophores (70–140 µm vs. 29–41 μm) and shorter conidia (25–60 µm vs. 110–157 µm) with less distosepta (4–10-distoseptate vs. 15–28-distoseptate) (Su et al. 2016). Distoseptispora arecacearum (MFLU 23-0276) differs from D. phangngaensis (MFLU 17-0855) in having longer conidiophores (70–140 µm vs. 18–30(–40) μm) and shorter conidia (25–60 µm vs. 165–350 µm) (Yang et al. 2018). Therefore, we introduced D. arecacearum (MFLU 23-0276) as a novel species, based on morphological and phylogenetic analyses.

Distoseptispora eleiodoxae O. Karimi, Q.R. Li & K.D. Hyde, sp. nov.

Index Fungorum number: IF900844
Facesoffungi number: FoF14757
Fig. 3

Etymology

The epithet “eleiodoxae” refers to the name of the host genus, Eleiodoxa conferta.

Holotype

MFLU 23-0277.

Description

Saprobic on submerged rachis of Eleiodoxa conferta in peatswamp forest. Sexual morph: Undetermined. Asexual morph: Hyphomycetous. Mycelium immersed to superfacial, septate, smooth, brown to dark brown. Colonies on submerged rachis, solitary, scattered, dark brown to black. Conidiophores 71–161 × 5–6.5 µm (x̄ = 110 × 5.7 µm, n = 20), macronematous, mononematous, cylindrical, erect, straight to flexuous, unbranched, smooth or finely verrucose, thick-walled, dark brown, 5–10-septate with lobed basal cells, percurrent proliferations at the apex. Conidiogenous cells 13.5–18.8 × 5–6.8 µm (x̄ = 15.96 × 5.6 µm, n = 20), holoblastic, monoblastic, terminal, integrated, cylindrical to ampulliform, percurrent, brown to dark brown, smooth. Conidia 31.5–48 × 13.5–15.8 µm (x̄ = 40.8 × 14.8 µm, n = 30), secession schizolytic, solitary, obpyriform, rostrate, truncated base, 6–7-euseptate, verrucose, thick-walled, brown with dark brown to black cells in the middle, paler towards the apex.

Figure 3. 

Distoseptispora eleiodoxae (MFLU 23-0277, holotype) a host material b, c colonies on the substrate d–f conidiophores and conidia g conidiogenous cell h–j conidia k culture on PDA (top and reverse). Scale bars: 100 µm (b, c); 30 µm (d–f); 10 µm (g–j).

Culture characteristics

Colonies grown on PDA, reaching 30 mm in diameter after 15 days at 25 °C, under dark conditions, circular, entire to radially with lobate edge, well-defined margin, low convex, dull surface, felted, dense, mycelium superficial to immersed, without pigment diffusion and sporulation, greyish-brown on the top with dark brown margin, reverse brown with dark brown centre and margin.

Material examined

Thailand. Narathiwat Province: Yi-ngo District, peatswamp forest, on submerged rachis of Eleiodoxa conferta, 06 April 2022, Omid Karimi, S5PP8N1SG (MFLU 23-0277, holotype); ex-type culture MFLUCC 23-0213, additional living culture MFLUCC 23-0214.

Notes

Distoseptispora eleiodoxae (MFLU 23-0277) shares similar characteristics with D. tropica J. Ma & Y.Z. Lu (HKAS 123761), in having macronematous, mononematous, cylindrical, erect, straight, unbranched conidiophores with holoblastic, monoblastic, terminal, cylindrical, thick-walled conidiogenous cells and verrucose, rostrate conidia (Ma et al. 2022). However, D. eleiodoxae (MFLU 23-0277) differs from D. tropica (HKAS 123761) in having shorter and wider obpyriform conidia (31.5–48 × 13.5–15.8 µm vs. 39–75 × 7.5–10.5 µm), with broad and darker middle cells, no guttules and lacking conspicuous hyphae attachment to conidia. The BLAST search against GenBank showed that the ITS and LSU sequences of the new isolate, D. eleiodoxae (MFLUCC 23-0213), share 84.25% similarity across 100% sequence coverage with D. tropica (GZCC 22-0076) and 96.09% similarity across 100% sequence coverage with D. effusa L.L. Liu & Z.Y. Liu, respectively. Distoseptispora eleiodoxae (MFLU 23-0277) differs from D. effusa (GZAAS 20-0427) in having shorter conidia (31.5–48 vs. 35.5–113 µm) (Yang et al. 2021). Based on a pairwise comparison of ITS, LSU, rpb2 and tef1-α nucleotides, D. eleiodoxae (MFLUCC 23-0213) differs from D. tropica (GZCC 22-0076) in 70/536 bp (13.05%) for ITS, 50/834 bp (5.99%) for LSU, 141/1052 bp (13.40%) for rpb2 and 96/888 bp (10.8%) for tef1-α (without including gaps). Therefore, we introduced D. eleiodoxae (MFLU 23-0277) as a novel species, based on the morphological evidence and according to the species delimitation guidelines proposed by Chethana et al. (2021) and Maharachchikumbura et al. (2021).

Distoseptispora narathiwatensis O. Karimi, Q.R. Li & K.D. Hyde, sp. nov.

Index Fungorum number: IF900845
Facesoffungi number: FoF14758
Fig. 4

Etymology

The epithet “narathiwatensis” refers to Narathiwat Province, where the holotype was collected.

Holotype

MFLU 23-0278.

Description

Saprobic on dead petiole of Eugeissona tristis in peatswamp forest. Sexual morph: Undetermined. Asexual morph: Hyphomycetous. Colonies superficial, effuse, hairy, gregarious, brown. Mycelium immersed to superficial, composed of septate, branched, pale brown hyphae. Conidiophores 27–155 × 3–6.5(–7) μm (x̄ = 104 × 5 μm, n = 50), macronematous, mononematous, cylindrical, straight or flexuous, occasionally slightly curved in the middle and near the base and the apex, up to 10 septa, slightly constricted at septa, unbranched, brown, thin-walled, smooth, often containing inflated or constricted cells at the apex or middle, sometimes percurrent with annellations. Conidiogenous cells 7–17 × 4–5.5 μm (x̄ = 12.5 × 5 μm, n = 30), holoblastic, mono- to polyblastic, integrated, determinate, terminal and intercalary, subcylindrical, brown, smooth. Conidia 12–38 × 4.5–8 μm (x̄ = 27 × 6.5 μm, n = 30), secession schizolytic, solitary or occasionally catenate, dry, thin-walled, smooth, subcylindrical to obclavate to conical, straight or curved, 1–7-distoseptate, slightly constricted at septa, olivaceous to brown, apex rounded, truncated base with slightly pigmented scar, often the primary cells of conidia are narrower than the second ones which are often inflated.

Figure 4. 

Distoseptispora narathiwatensis (MFLU 23-0278, holotype) a host material b colonies on the substrate c–e conidiophores and conidia f conidiogenous cell g–j conidia k, l culture on PDA. Scale bars: 100 μm (b); 50 μm (c–e); 10 μm (f–j).

Culture characteristics

Colonies grown on PDA, reaching 50 mm in diameter after 15 days at 25 °C, under dark conditions, circular, entire margin, well-defined margin, low convex, dull surface, felted, dense, mycelium mostly superficial, without pigment diffusion and sporulation, medium brown to reddish-brown with dark brown edge on the top, reverse-side dark brown to black.

Material examined

Thailand. Narathiwat Province: Yi-ngo District, peatswamp forest, on dead petiole of Eugeissona tristis, 06 April 22, Omid Karimi, 35Y (MFLU 23-0278, holotype); ex-type culture MFLUCC 23-0215, additional living culture MFLUCC 23-0216.

Notes

Distoseptispora narathiwatensis (MFLU 23-0278) is similar to D. saprophytica (MFLU 18-1568), but it can be distinguished in having longer and wider conidiophores (27–155 × 3–6.5 (–7) μm vs. 50–140 × 3.2–4.2 μm) and conidiogenous cells (7–17 × 4–5.5 μm vs. 5–11.5 × 3–4.5 μm). In D. narathiwatensis (MFLU 23-0278), the conidiophore is slightly curved at the base, middle and near the top in contrast to D. saprophytica (MFLU 23-0278), which is characterised by sharp curving near the base; also in D. narathiwatensis, the conidiophore cells are often inflated or constricted at the apex or middle which is not observed in D. saprophytica (Dong et al. 2021). Conidiogenous cells of D. narathiwatensis are terminal and intercalary and their conidia are not acrogenous as in D. saprophytica. The primary cell in the conidium is often narrower than the second one and the second cell is often inflated, which is not observed in D. saprophytica. The BLAST search against the GenBank showed that the ITS and rpb2 sequences of the new isolate, D. narathiwatensis (MFLUCC 23-0215), share 98.33% similarity across 100% sequence coverage and 98.63% similarity across 78% sequence coverage with D. saprophytica (MFLUCC 18-1238), respectively. In a BLAST search against GenBank, the LSU and tef1-α sequences of D. narathiwatensis (MFLUCC 23-0215) share 99.3% similarity across 85% sequence coverage and 94.12% similarity across 94% sequence coverage with D. palmarum (MFLU 18-0588), respectively. However, D. palmarum is distinguished in having longer (12–38 μm vs. 35–180 μm), elongated, greenish-black to brown conidia (Hyde et al. 2019). Based on a pairwise comparison of ITS and LSU nucleotides, D. narathiwatensis (MFLUCC 23-0215) differs from D. saprophytica (MFLUCC 18-1238) by 22/580 bp (3.8%), 16/870 bp (1.8%) differences, respectively (without including gaps). Therefore, we introduced D. narathiwatensis (MFLU 23-0278) as a novel species, based on the morphological evidence and according to the species delimitation guidelines proposed by Chethana et al. (2021) and Maharachchikumbura et al. (2021).

Discussion

Peatswamp forests are unique habitats found in only a few regions worldwide (Jackson et al. 2009). The destruction caused by humans threatens them; hence more extensive studies on fungal identification are needed before the extinction of fungal species. Pinnoi et al. (2006, 2009) recorded sporidesmium-like taxa on the palm species Eleiodoxa conferta and Calamus sp. in Sirindhorn peatswamp forest, Narathiwat, Thailand, based on morphological data. In this study, three new Distoseptispora species (D. arecacearum, D. eleiodoxae and D. narathiwatensis) from peatswamp forest in Thailand are introduced, based on multilocus phylogenetic analysis (ITS, LSU, rpb2 and, tef1-α) (Fig. 1) and morphology (Figs 2–4).

The fungal diversity in peatswamp forest has not been well studied and a few previously studies (Pinruan et al. 2002, 2004a, 2004b, 2007, 2008, 2010a, 2010b, 2014; Pinnoi et al. 2003a, 2003b, 2004, 2006, 2009, 2010; Voglmayr and Yule 2006; Sivichai and Boonyuen 2010; Boonyuen et al. 2012) show a high fungal diversity in this habitat, especially in Thailand, but some of the previous studies (Pinruan et al. 2002, 2007, 2014; Pinnoi et al. 2003a, 2003b, 2004, 2006, 2009; Sivichai and Boonyuen 2010) lack molecular data. As only morphological data are insufficient to identify a fungal species (Chethana et al. 2021; Maharachchikumbura et al. 2021), studying the fungal diversity by combining morphological and molecular data are required and this has been followed in this study.

Except for Distoseptispora hyalina J. Yang & K.D. Hyde and D. licualae Konta & K.D. Hyde, most Distoseptispora species have been recorded as having an asexual morph and their characters, such as size, shape, colour and the number of septa in conidiophores and conidia, are crucial for distinguishing species. Morphologically, Distoseptispora is similar to Ellisembia Subram and Sporidesmium Link; therefore, it is problematic to recognise Distoseptispora species by only morphological signatures (Su et al. 2016; Hyde et al. 2019; Luo et al. 2019; Yang et al. 2021). Different studies have explored the taxonomy of Distoseptispora using various combinations of gene regions, such as combined ITS, LSU (Tibpromma et al. 2018), combined LSU, ITS, rpb2 (Monkai et al. 2020) or combined LSU, ITS, tef1-α and rpb2 (Zhang et al. 2022). In our study, we constructed the phylogenetic tree using concatenated ITS, LSU, rpb2 and tef1-α. In this study, Distoseptispora clematidis (MFLUCC 17-2145) and D. nabanheensis Jing W. Liu, X.G. Zhang & Jian Ma (HJAUP C2003) formed a sister clade, consistent with previous research (Liu et al. 2023). However, D. clematidis (KUN-HKAS:112708) appeared separated from these two taxa, presenting an unresolved relationship. The phylogenetic relationship amongst these three taxa is not comparable with the previous studies due to the lack of all these taxa together in their phylogenetic trees (Afshari et al. 2023; Liu et al. 2023). The unresolved clade’s origin may stem from the lack of rpb2 sequence data for D. clematidis (KUN HKAS:112708) in contrast to the other two taxa where this gene region is available. This suggests that different taxon sampling and protein-coding sequences can influence the topology of the tree. However, further studies are essential to validate this hypothesis.

Morphologically, some taxa that share similarities exhibit distinct phylogenies. For instance, D. arecacearum shares a morphological resemblance with D. dehongensis, although they are phylogenetically distinct. Similarly, D. eleiodoxae shows morphological similarities to D. tropica, but resides in a separate clade in the phylogenetic tree. Distoseptispora narathiwatensis forms a sister clade with D. saprophytica despite the differences highlighted by the pairwise comparison of ITS, LSU and other genetic markers. These encompass 22/580 bp (3.8%) and 16/870 bp (1.8%) differences for ITS and LSU, respectively, excluding gaps. Moreover, distinctions in the morphology of conidiophores and the absence of acrogenous conidia further contribute to the differentiation between D. narathiwatensis and D. saprophytica. Our study confirmed the necessity of associating molecular data with morphological characters to distinguish them, as previously demonstrated in other studies (Su et al. 2016; Hyde et al. 2019; Luo et al. 2019; Yang et al. 2021; Ma et al. 2022).

To date, the majority of Distoseptispora species have been reported from China (42 species) and Thailand (23 species), primarily on dead plant materials in freshwater (44 species) and terrestrial (21 species) habitats. In most cases, the hosts are unknown. Although in 19 cases, their hosts have been identified, two of which have been reported from palm, including D. palmarum from Cocos nucifera and D. licualae from dead leaves of Licuala glabra in terrestrial habitats (Hyde et al. 2016, 2021; Su et al. 2016; Xia et al. 2017; Tibpromma et al. 2018; Yang et al. 2018; Luo et al. 2019; Phookamsak et al. 2019; Monkai et al. 2020; Phukhamsakda et al. 2020, 2022; Song et al. 2020; Sun et al. 2020; Dong et al. 2021; Li et al. 2021; Shen et al. 2021; Jayawardena et al. 2022; Ma et al. 2022; Zhai et al. 2022; Zhang et al. 2022; Konta et al. 2023; Liu et al. 2023). Distoseptispora species have been recorded as saprophytes and their reported limited geographic distribution (China and Thailand) is most likely due to increased attention by mycologists in these areas on saprophytic fungi in aquatic and terrestrial habitats. This study shows that there is much to be done in this regard. Ongoing and future investigations will reveal the diversity and functions of these microorganisms in this ecosystem.

Acknowledgements

Omid Karimi would like to thank the National Science, Research and Innovation Fund: Thailand Science Research Innovation (Basic Research Fund 2023) entitled ‘Taxonomy, Phylogeny and Chemo-profiling of selected families in Xylariales (662A01003)’ for the financial support and Mr. Arttapon Walker for his valuable help in collecting samples. Shaun Pennycook is thanked for advising to give epithets for the new taxa. Omid Karimi and Raheleh Asghari would like to thank the Mae Fah Luang University Partial Scholarship for the doctoral degree programme and Mushroom Research Foundation. Kevin D. Hyde would like to thank the National Research Council of Thailand (NRCT) grant “Total fungal diversity in a given forest area with implications towards species numbers, chemical diversity and biotechnology” (grant no. N42A650547). Qirui Li would like to thank the China National Natural Science Foundation (31960005 and 32000009).

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

The National Science, Research and Innovation Fund: Thailand Science Research Innovation (Basic Research Fund 2023) entitled ‘Taxonomy, Phylogeny and chemo-profiling of selected families in Xylariales (662A01003), China National Natural Science Foundation (31960005 and 32000009), National Research Council of Thailand (NRCT) grant “Total fungal diversity in a given forest area with implications towards species numbers, chemical diversity and biotechnology” (grant no. N42A650547)

Author contributions

Morphological identification, photo-plates, and phylogenetic analyzes were completed by Omid Karimi and Raheleh Asghari. The original draft was written by Omid Karimi, and K.W. Thilini Chethana, Antonio R.G. Farias, Saithong Kaewchai, Kevin D. Hyde, Qirui Li revised the paper.

Author ORCIDs

Omid Karimi https://orcid.org/0000-0001-9652-2222

K.W. Thilini Chethana https://orcid.org/0000-0002-5816-9269

Antonio R.G. de Farias https://orcid.org/0000-0003-4768-1547

Raheleh Asghari https://orcid.org/0009-0006-4897-5327

Saithong Kaewchai https://orcid.org/0009-0004-9335-7697

Kevin D. Hyde https://orcid.org/0000-0002-2191-0762

Qirui Li https://orcid.org/0000-0001-8735-2890

Data availability

All of the data that support the findings of this study are available in the main text.

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