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Research Article
Morphological and phylogenetic analyses reveal three new species and one new record of Tubeufia (Tubeufiales, Tubeufiaceae) from southern China
expand article infoJian Ma‡§, Li-Juan Zhang§‡, Saranyaphat Boonmee§, Xing-Juan Xiao‡, Ning-Guo Liu‡, Yuan-Pin Xiao‡, Zong-Long Luo|, Yong-Zhong Lu‡
‡ Guizhou Institute of Technology, Guiyang, China
§ Mae Fah Luang University, Chiang Rai, Thailand
| Dali University, Dali, China

Corresponding author: Yong-Zhong Lu ( yzlu86@gmail.com )

Academic editor: Nattawut Boonyuen
© 2023 Jian Ma, Li-Juan Zhang, Saranyaphat Boonmee, Xing-Juan Xiao, Ning-Guo Liu, Yuan-Pin Xiao, Zong-Long Luo, Yong-Zhong Lu.
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: Ma J, Zhang L-J, Boonmee S, Xiao X-J, Liu N-G, Xiao Y-P, Luo Z-L, Lu Y-Z (2023) Morphological and phylogenetic analyses reveal three new species and one new record of Tubeufia (Tubeufiales, Tubeufiaceae) from southern China. MycoKeys 99: 87-108. https://doi.org/10.3897/mycokeys.99.107606
Open Access

Abstract

During an investigation of helicosporous fungi in China, a total of seven helicosporous hyphomycetes were obtained from decaying wood in the southern region of the country. Based on phylogenetic analyses using a combined LSU, ITS, tef1α, and rpb2 sequence matrix, in conjunction with morphological comparisons, these taxa were classified within Tubeufia (Tubeufiaceae, Tubeufiales) and were recognized as three new species, viz. Tubeufia guttulata, T. hainanensis, and T. muriformis, as well as one new distribution record, viz. T. cocois. Evidence for these new taxa and the new record, descriptions, illustrations, notes, and phylogenetic evidence are provided for the newly collected helicosporous species.

Key words

asexual morph, new taxa, phylogeny, taxonomy

Introduction

Tubeufia was introduced by Penzig and Saccardo (1897) with the type species T. javanica and two other species (T. anceps and T. coronata). Tubeufia species are widely distributed in tropical and temperate regions, including freshwater and terrestrial habitats, occurring primarily on well-rotted wood (Barr 1979; Rossman 1987; Ho et al. 2002; Tsui and Berbee 2006; Tsui et al. 2007; Zhao et al. 2007; Boonmee et al. 2011, 2014; Chaiwan et al. 2017; Dai et al. 2017; Doilom et al. 2017; Lu et al. 2017, 2018a, 2018b, 2022, 2023; Tian et al. 2022). There are currently 56 accepted species in Tubeufia, as listed in Table 1. These species exhibit a wide range of morphological characteristics in both their sexual and asexual morphs. For example, although Tubeufia bambusicola, T. javanica, and T. latispora shared a close phylogenetic affinity, they possess distinct morphological features. Tubeufia bambusicola and T. latispora possess black ascomata that are densely covered with long, flexuous setae. These ascomata contain sessile asci, each containing eight fusiform ascospores. In contrast, T. javanica has white ascomata without seta and short pedicellate asci with eight filiform ascospores (Boonmee et al. 2014; Lu et al. 2017, 2018b). The asexual morphs of Tubeufia encompass both helicosporous and dictyosporous hyphomycetes. The helicosporous asexual morphs of Tubeufia display diverse shapes, with certain species exhibiting abundant, elongated conidiophores, while others possess extremely short conidiophores. For instance, T. abundata is characterized by abundant, branched, and long conidiophores, T. arctata exhibits rarely unbranched, short conidiophores, and T. machaerinae does not possess conidiophores (Lu et al. 2018b).

Table 1.
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Checklist of accepted Tubeufia species.

No. Species Distribution Habitat Molecular data Reference
1 T. abundata Thailand Freshwater Available Lu et al. 2018b
2 T. acaciae India Terrestrial Not available Tilak and Kale 1969
3 T. aciculospora Japan Terrestrial Not available Katsumoto and Harada 1979
4 T. aquatica China, Thailand Freshwater Available Luo et al. 2017; Lu et al. 2018b
5 T. bambusicola Thailand Terrestrial Available Lu et al. 2018b
6 T. brevis Thailand Freshwater Available Lu et al. 2018b
7 T. brevispina USA Terrestrial Not available Barr and Rogerson 1983; Crane et al. 1998
8 T. brunnea Thailand Freshwater Available Lu et al. 2018b
9 T. chiangmaiensis Thailand Terrestrial Available Boonmee et al. 2014
10 T. chlamydospora Thailand Freshwater Available Lu et al. 2018b
11 T. claspisphaeria China Freshwater Not available Kodsueb et al. 2004
12 T. cocois Thailand Freshwater/ Terrestrial Available Tian et al. 2022
13 T. cylindrothecia Thailand, USA Freshwater Available Luo et al. 2017
14 T. dactylariae China Terrestrial Not available Chang 2003
15 T. dentophora China Terrestrial Not available Lu et al. 2018b
16 T. dictyospora Thailand Freshwater/ Terrestrial Available Lu et al. 2018b
17 T. eccentrica China Freshwater Available Lu et al. 2018b
18 T. entadae Thailand Terrestrial Available Jayasiri et al. 2019
19 T. eugeniae India Terrestrial Not available Pande 2008
20 T. fangchengensis China Freshwater Available Lu et al. 2018b
21 T. filiformis Thailand Freshwater Available Lu et al. 2017
22 T. freycinetiae Thailand Terrestrial Available Tibpromma et al. 2018
23 T. garugae India Terrestrial Not available Pande 2008
24 T. geniculata China Freshwater Available Lu et al. 2018b
25 T. guangxiensis China Freshwater Available Chaiwan et al. 2017
26 T. hechiensis China Freshwater Available Lu et al. 2018b
27 T. hyalospora Thailand Freshwater Available Hyde et al. 2016
28 T. inaequalis Thailand Freshwater Available Lu et al. 2018b
29 T. javanica Thailand Terrestrial Available Boonmee et al. 2014
30 T. krabiensis Thailand Freshwater Available Lu et al. 2018b
31 T. latispora Thailand Freshwater Available Lu et al. 2017
32 T. laxispora Thailand Freshwater Available Lu et al. 2017
33 T. lilliputea Australia, China, India, Japan, USA Terrestrial Available Lu et al. 2018b
34 T. liyui China Freshwater Available Lu et al. 2023
35 T. longihelicospora China, Thailand Freshwater Available Boonmee et al. 2021; Tian et al. 2022
36 T. longiseta Thailand Terrestrial Available Dai et al. 2017
37 T. machaerinae China, USA Freshwater/ Terrestrial Available Lu et al. 2018b
38 T. mackenziei Thailand Freshwater Available Lu et al. 2017
39 T. nigroseptum China Freshwater Available Li et al. 2022
40 T. minuta Denmark, Sweden Terrestrial Not available Munk 1966
41 T. pachythrix Brazil Terrestrial Not available Rossman 1979
42 T. pandanicola Thailand Terrestrial Available Tibpromma et al. 2018
43 T. parvispora Thailand Terrestrial Available Tibpromma et al. 2018
44 T. parvula Britain, Sweden Terrestrial Not available Dennis 1975
45 T. roseohelicospora Thailand Freshwater Available Hyde et al. 2016
46 T. rubra Thailand Freshwater Available Lu et al. 2018b
47 T. sahyadriensis India Terrestrial Available Rajeshkumar et al. 2019
48 T. sessilis Thailand Terrestrial Available Lu et al. 2018b
49 T. silentvalleyensis India Terrestrial Not available Pande 2008
50 T. sympodihylospora China Freshwater Available Lu et al. 2018b
51 T. sympodilaxispora China Freshwater Available Lu et al. 2018b
52 T. sympodiophora China, Peru Freshwater/ Terrestrial Not available Lu et al. 2018b
53 T. taiwanensis China Freshwater Available Lu et al. 2018b
54 T. tectonae Thailand Freshwater/ Terrestrial Available Doilom et al. 2017; Lu et al. 2018b
55 T. tratensis Thailand Freshwater Available Lu et al. 2018b
56 T. xylophila China, India Freshwater/ Terrestrial Available Lu et al. 2018b

The helicosporous taxa of Tubeufia represent a promising biological resource capable of producing novel bioactive secondary metabolites. Fan et al. (2019) discovered that T. rubra exhibited a significant antifungal impact against seven plant pathogenic fungi, viz. Alternaria solani (ZYB), Botryosphaeria dothidea (B12), Fusarium graminearum (CM), Magnaporthe grisea (DWB), Phoma sp. (HGHM), Phytophthora parasitica (HJB) and Rhizoctorzia solani (WB). The inhibition rate of T. rubra against these fungal pathogens exceeded 60%, indicating its potential as an effective antifungal agent. Fan et al. (2019) also discovered that the ethyl acetate extract from the fermentation broth of T. machaerinae inhibited the human cervical cancer cell line (HeLa) and human prostate cancer cell line (PC-3) by (98.92 ± 0.15%) and (97.86 ± 0.18%), respectively. According to Chen et al. (2020), both T. hechiensis and T. rubra exhibited the ability to reverse multidrug resistance in tumor cells. Zeng et al. (2022) discovered a newly isolated compound called Rubricin A from T. rubra, which demonstrated the capacity to inhibit the expression of P-glycoprotein (P-gp) and effectively reverse multidrug resistance in tumor cells. Qian et al. (2023) reported the isolation of two novel compounds, viz. Rubracin D and E, and sixteen known glyceroglycolipids from T. rubra. Rubracin D and E demonstrated significant multidrug resistance reversal activities on MCF-7/ADM, K562/ADM, and A549/ADM cell lines.

In this study, seven helicosporous taxa were collected from the southern provinces of Hainan and Guizhou in China. Based on morphological evidence and phylogenetic analyses, three novel species were introduced and designated as Tubeufia guttulata, T. hainanensis and T. muriformis, and one new distribution record, viz. T. cocois. The new species are described with detailed morphological descriptions and illustrations.

Materials and methods

Sample collection, specimen examination, and isolation

From August 2021 to March 2022, decaying wood samples were collected from Hainan and Guizhou provinces in southern China. The collected information includes locations, dates, altitudes, latitudes, and longitude. Fresh specimens were placed in zip-lock bags and sterile, moist plastic boxes, and then incubated at room temperature for a period of two weeks. Using a stereomicroscope (SMZ-168, Nikon, Japan), the fungal colonies growing on decaying wood surfaces were carefully examined, observed, and documented through photography. Morphological features such as conidiophores, conidiogenous cells, and conidia were further captured using an ECLIPSE Ni compound microscope (Nikon, Tokyo, Japan) in conjunction with a Canon 90D digital camera. Measurements were taken with the Tarosoft (R) Image Frame Workprogram. Photoplates were developed with Adobe PhotoShop CC 2019 (Adobe Systems, USA).

According to the method described by Senanayake et al. (2020), helicosporous strains were isolated and purified on water agar (WA), and germinated conidia were aseptically transferred to fresh potato dextrose agar (PDA) plates. Mycelium was cultured on Potato Dextrose Agar (PDA) and incubated at a temperature of 25 °C for a period of 6–7 weeks. During this time, various morphological characteristics including color, shape, and size were carefully observed and recorded. Subsequently, dried specimens of the fungal cultures were deposited in the Herbarium of Kunming Institute of Botany, Chinese Academy of Sciences (Herb. HKAS), Kunming, China, and the Herbarium of Guizhou Academy of Agriculture Sciences (Herb. GZAAS), Guiyang, China. Cultures were deposited in the China General Microbiological Culture Collection Center (CGMCC; https://www.cgmcc.net/english/), Beijing, China, and the Guizhou Culture Collection, China (GZCC), Guiyang, China for future reference and scientific documentation. Faces of fungi (FOF; https://www.facesoffungi.org) numbers were obtained in accordance with Jayasiri et al. (2015) and MycoBank numbers of the new species were registered in the MycoBank database (https://www.mycobank.org/).

DNA extraction, PCR amplification, and sequencing

Fresh fungal hyphae were gently scraped and transferred to a 1.5-mL microcentrifuge tube using a sterile toothpick. Genomic DNA was extracted using the Biospin Fungus Genomic DNA Extraction Kit (BioFlux, China) and following the manufacturer’s protocol for DNA extraction. Specific forward and reverse primers, namely ITS5/ITS4, LR0R/LR5, fRPB2-5F/fRPB2-7cR, and EF1-983F/EF1-2218R, were employed to amplify the internal transcribed spacer (ITS, White et al. 1990), large ribosomal subunit (LSU, Vilgalys and Hester 1990), and RNA polymerase II second-largest subunit (rpb2, Liu et al. 1999) and translation elongation factor 1-α gene (tef1α, Rehner and Buckley 2005) sequence fragments, respectively. The polymerase chain reaction (PCR) conditions employed were in accordance with the reaction conditions outlined in the publications by Lu et al. (2017, 2018a). PCR amplification reactions were conducted in a 50-μL reaction volume containing 44 μL of 1.1× T3 Supper PCR Mix (Qingke Biotech, China), 2 μL of forward and reverse primers, and 2 μL of DNA template. The products were detected by 1% agarose gel electrophoresis following PCR amplification, with primers and PCR product sequencing provided by Beijing Qingke Biotechnology Co., Ltd.

Phylogenetic analyses

The original sequences were examined with BioEdit v 7.0.5.3 (Hall 1999) and assembled with SeqMan v. 7.0.0 (DNASTAR, Madison, WI, USA; Swindell and Plasterer 1997). The taxa used in this study (Table 2) were downloaded based on high levels of identity (> 90%) and selected outgroups (https://blast.ncbi.nlm.nih.gov/Blast.cgi). The polygenic dataset was aligned by MAFFT v.7.473 (https://mafft.cbrc.jp/alignment/server/, Katoh and Standley 2013; Katoh et al. 2019). The data were trimmed using trimAl.v1.2rev59 software (Capella-Gutiérrez et al. 2009). The multigenic sequences (LSU-ITS-tef1α-rpb2) were merged using SequenceMatrix-Windows-1.7.8 software (Vaidya et al. 2011). The aligned Fasta file was converted to Nexus format file for Bayesian inference (BI) analyses using AliView v. 1.27 (Daniel et al. 2010).

Table 2.
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Taxa used in this study and their GenBank accession numbers of DNA sequences.

Taxon Strain GenBank Accessions
ITS LSU tef1α rpb2
Acanthohelicospora aurea GZCC 16-0060 KY321323 KY321326 KY792600 MF589911
A. guianensis UAMH 1699 AY916479 AY856891 – –
T. abundata MFLUCC 17-2024T MH558769 MH558894 MH550961 MH551095
T. aquatica MFLUCC 16-1249T KY320522 KY320539 KY320556 MH551142
T. aquatica DLUCC 0574 – KY320538 KY320555 MH551141
T. aquatica MFLUCC 17-1794 MH558770 MH558895 MH550962 MH551096
T. bambusicola MFLUCC 17-1803T MH558771 MH558896 MH550963 MH551097
T. brevis MFLUCC 17-1799T MH558772 MH558897 MH550964 MH551098
T. brunnea MFLUCC 17-2022T MH558773 MH558898 MH550965 MH551099
T. chiangmaiensis MFLUCC 17-1801 MH558774 MH558899 MH550966 MH551100
T. chiangmaiensis MFLUCC 11-0514T KF301530 KF301538 KF301557 –
T. chlamydospora MFLUCC 16-0223T MH558775 MH558900 MH550967 MH551101
T. cocois MFLUCC 22–0001T OM102541 OL985957 OM355486 OM355491
T. cocois GZCC 22-2038 OR030844 OR030837 OR046681 –
T. cylindrothecia BCC 3559 – AY849965 – –
T. cylindrothecia BCC 3585 AY916482 AY856908 – –
T. cylindrothecia DLUCC 0572 KY320520 KY320537 KY320554 –
T. cylindrothecia MFLUCC 16-1253 KY320519 KY320536 KY320553 –
T. cylindrothecia MFLUCC 16-1283 KY320518 KY320535 KY320552 MH551143
T. cylindrothecia MFLUCC 17-1792 MH558776 MH558901 MH550968 MH551102
T. dictyospora MFLUCC 17-1805T MH558778 MH558903 MH550970 MH551104
T. dictyospora MFLUCC 16-0220 MH558777 MH558902 MH550969 MH551103
T. eccentrica GZCC 16-0048 MH558780 MH558905 MH550972 MH551106
T. eccentrica GZCC 16-0084 MH558781 MH558906 MH550973 MH551107
T. eccentrica MFLUCC 17-1524T MH558782 MH558907 MH550974 MH551108
T. eccentrica GZCC 16-0035 MH558779 MH558904 MH550971 MH551105
T. entadae MFLU 18-2102 MK347727 MK347943 – –
T. fangchengensis MFLUCC 17-0047T MH558783 MH558908 MH550975 MH551109
T. filiformis MFLUCC 16-1128T – KY092407 KY117028 MF535284
T. filiformis MFLUCC 16-1135 KY092416 KY092411 KY117032 MF535285
T. filiformis MFLUCC 16-0236 – MH558938 MH550976 MH551110
T. freycinetiae MFLUCC 16-0252T MH275089 MH260323 MH412786 –
T. geniculata BCRC FU30849T LC335817 – – –
T. geniculata NCYU U2-1B LC335816 – – –
T. guangxiensis GZCC 16-0054 MG012027 MG012020 MG012006 MG012013
T. guangxiensis GZCC 16-0090 MG012029 MG012022 MG012008 MG012015
T. guangxiensis GZCC 16-0091 MG012028 MG012021 MG012007 MG012014
T. guangxiensis MFLUCC 17-0038 MG012026 MG012019 MG012005 MG012012
T. guangxiensis MFLUCC 17-0045T MG012025 MG012018 MG012004 MG012011
T. guangxiensis MFLUCC 17-0046 MH558784 MH558909 MH550977 MH551111
T. guangxiensis GZCC 16-0041 MG012030 MG012023 MG012009 MG012016
T. guttulata GZCC 23-0404T OR030841 OR030834 OR046678 OR046684
T. guttulata GZCC 23-0590 OR066413 OR066420 OR058859 OR058852
T. hainanensis GZCC 22-2015T OR030842 OR030835 OR046679 OR046685
T. hainanensis GZCC 23-0589 OR066414 OR066421 OR058860 OR058853
T. hechiensis MFLUCC 17-0052T MH558785 MH558910 MH550978 MH551112
T. hyalospora MFLUCC 15-1250T MH558786 MH558911 MH550979 –
T. inaequalis GZCC 16-0079 MH558787 MH558912 MH550980 MH551113
T. inaequalis GZCC 16-0087 MH558788 MH558913 MH550981 MH551114
T. inaequalis MFLUCC 17-0053T MH558789 MH558914 MH550982 MH551115
T. inaequalis MFLUCC 17-1989 MH558790 MH558915 MH550983 MH551116
T. inaequalis MFLUCC 17-1998 MH558791 MH558916 MH550984 MH551117
T. inaequalis BCC 8808 AY916481 AY856910 – –
T. javanica MFLUCC 12-0545 KJ880034 KJ880036 KJ880037 –
T. krabiensis MFLUCC 16-0228T MH558792 MH558917 MH550985 MH551118
T. latispora MFLUCC 16-0027T KY092417 KY092412 KY117033 MH551119
T. laxispora MFLUCC 16-0013 MH558793 MH558918 MH550986 MH551120
T. laxispora MFLUCC 16-0219 KY092414 KY092409 KY117030 MF535286
T. laxispora MFLUCC 16-0232T KY092413 KY092408 KY117029 MF535287
T. laxispora MFLUCC 17-2023 MH558794 MH558919 MH550987 MH551121
T. lilliputea NBRC 32664 AY916483 AY856899 – –
T. liyui GZCC 22-2030T OP888466 OP888465 – –
T. longihelicospora MFLUCC 21-0814 OM331690 OM331688 – –
T. longihelicospora MFLUCC 21-0815 OM331691 OM331705 – –
T. longihelicospora MFLUCC21-0151 OL606156 OL606149 OL964520 OL964526
T. longihelicospora MFLUCC 16-0753T NR_182938 – – –
T. longiseta MFLUCC 15-0188T KU940133 – – –
T. machaerinae MFLUCC 17-0055T MH558795 MH558920 MH550988 MH551122
T. mackenziei MFLUCC 16-0222T KY092415 KY092410 KY117031 MF535288
T. muriformis GZCC 22-2039T OR030843 OR030836 OR046680 OR046686
T. muriformis GZCC 23-0591 OR066415 OR066422 OR058861 OR058854
T. nigroseptum CGMCC 3.20430T MZ092716 MZ853187 OM022002 OM022001
T. pandanicola MFLUCC 16-0321T MH275091 MH260325 – –
T. parvispora MFLUCC 17-1992 MH558796 MH558921 MH550989 MH551123
T. parvispora MFLUCC 17-2003 MH558797 MH558922 MH550990 MH551124
T. parvispora MFLUCC 17-2009 MH558798 MH558923 MH550991 MH551125
T. roseohelicospora MFLUCC 16-0230 MH558799 MH558924 MH550992 MH551126
T. roseohelicospora MFLUCC 17-1797 MH558800 MH558925 MH550993 MH551127
T. roseohelicospora MFLUCC 15-1247T KX454177 KX454178 – MH551144
T. rubra GZCC 16-0083T MH558802 MH558927 MH550995 MH551129
T. rubra GZCC 16-0081 MH558801 MH558926 MH550994 MH551128
T. sahyadriensis NFCCI 4252/RAJ 99.1T MH033849 MH033850 MH033851 –
T. sahyadriensis NFCCI RAJ 99.2 MN393081 MN393082 MN393083 –
T. sessilis MFLUCC 16-0021T MH558803 – MH550996 MH551130
T. sympodihylospora GZCC 16-0051 MH558805 MH558929 MH550998 MH551132
T. sympodihylospora MFLUCC 17-0044T MH558806 MH558930 MH550999 MH551133
T. sympodihylospora GZCC 16-0049 MH558804 MH558928 MH550997 MH551131
T. sympodilaxispora BCC 3580 – DQ296554 – –
T. sympodilaxispora GZCC 16-0058T MH558807 MH558931 MH551000 MH551134
T. sympodilaxispora MFLUCC 17-0048 MH558808 MH558932 MH551001 MH551135
T. taiwanensis BCRC FU30844T LC316605 – – –
T. tectonae MFLUCC 16-0235 MH558809 MH558933 MH551002 MH551136
T. tectonae MFLUCC 17-1985 MH558810 MH558934 MH551003 MH551137
T. tectonae MFLUCC 12-0392T KU144923 KU764706 KU872763 –
T. tratensis MFLUCC 17-1993T MH558811 MH558935 MH551004 MH551138
T. xylophila MFLUCC 17-1520 MH558813 MH558937 MH551006 MH551140
T. xylophila GZCC 16-0038 MH558812 MH558936 MH551005 MH551139
Tubeufiaceae sp. BCC 3512 AY916484 AY856905 – –
Tubeufiaceae sp. BCC 3381 – AY787932 – –

Note: “T” denotes ex-type strain. Newly generated sequences are indicated in bold. “-” means no data available in GenBank.

Maximum likelihood (ML) analysis was carried out using the IQ Tree online website (http://iqtree.cibiv.univie.ac.at/), employing Bayesian Information Criteria (BIC) as the criterion for model selection, as described by Nguyen et al. (2015). The server automatically conducted tests to determine the appropriate substitution model for the analysis.

Bayesian inference (BI) analysis was conducted in MrBayes on XSEDE (3.2.7a) (Ronquist et al. 2012). The best-fit substitution model GRT + I +G was decided for LSU, ITS, tef1α and rpb2 matrix by MrModeltest 2.3 under the Akaike Information Criterion (AIC) (Nylander et al. 2008). Four simultaneous Markov chains were run for 10,000,000 generations, and trees were sampled every 1000th generations. Burn-in phase was set at 25% and the remaining trees were used for calculating posterior probabilities (PP).

Phylogenetic trees were visualized and edited using FigTree v. 1.4.4 and Adobe Illustrator CC 2019v. 23.1.0 (Adobe Systems, USA). In addition, Adobe PhotoShop CC 2019 (Adobe Systems, USA) was used to create the photo-plates.

Phylogenetic results

The phylogenetic position of the newly isolated taxa was determined in this study using partial LSU-ITS-tef1α-rpb2 nucleotide sequences. The concatenated sequence matrix consisted of LSU (1–845 bp), ITS (846–1440 bp), tef1α (1441–2352 bp), and rpb2 (2353–3397 bp) for a total of 97 taxa, including two outgroup taxa, resulting in a matrix of 3,397 characters. Maximum likelihood (ML) and Bayesian inference (BI) analyses were conducted on the concatenated datasets of LSU, ITS, tef1α, and rpb2, both yielding similar tree topologies, and the ML tree is shown in Fig. 1.

Figure 1. 

Phylogenetic tree generated from maximum likelihood (ML) analysis based on a combined LSU, ITS, tef1α, and rpb2 sequence data. The bootstrap support values of ML are equal to or greater than 75%, and Bayesian posterior probabilities (PP) equal to or greater than 0.95 are given near the nodes as ML/PP, respectively. Acanthohelicospora aurea GZCC 16–0060 and A. guianensis UAMH 1699 were used as outgroup taxa. The new species are indicated in red bold and newly generated sequences are indicated in black bold. “T” denotes ex-type strain. Symbols after generic names in Tubeufia indicate the habitats of taxa as explained in the phylogram.

Based on the multigene phylogenetic tree depicted in Fig. 1, our study revealed that the seven new collections belong to three distinct species within the genus Tubeufia. Tubeufia guttulata is a significantly distinct lineage from T. cocois with 100% ML/1.00 PP supports. T. hainanensis establishes a sister lineage to Tubeufiaceae BCC 3512 with 85% ML/0.99 PP supports. T. muriformis can be distinguished from other related Tubeufia species by its distinct muriform conidia. Based on phylogenetic and morphological evidence, our new isolate, GZCC 22–2038, is recognized as T. cocois.

Taxonomy

Tubeufia guttulata J. Ma & Y.Z. Lu, sp. nov.

MycoBank No: 900504
Facesoffungi Number: FoF14265
Fig. 2

Etymology

The epithet ‘‘guttulata’’ refers to the guttulate conidia of this taxon.

Holotype

HKAS 128936

Description

Saprobic on decaying wood in a terrestrial habitat. Sexual morph Undetermined. Asexual morph Hyphomycetous, helicosporous. Colonies on natural substrate superficial, effuse, gregarious, white. Mycelium partly immersed, hyaline to pale brown, septate, branched hyphae, smooth, with masses of crowded, glistening conidia. Conidiophores macronematous, mononematous, flexuous, cylindrical, branched or unbranched, septate, 101–247 μm long, 5.5–8 μm wide (x̄ = 165 × 7 μm, n = 20), the lower part pale brown and the upper part hyaline, smooth-walled. Conidiogenous cells holoblastic, mono- to polyblastic, integrated, sympodial, intercalary or terminal, cylindrical, with a denticulate protrusion, truncate at apex after conidial secession, 9–16 μm long, 4–6 μm wide (x̄ = 12 × 5 μm, n = 25), hyaline to pale brown, smooth-walled. Conidia solitary, acropleurogenous, helicoid, rounded at tip, 25–34 μm diam and conidial filament 4–6 μm wide (x̄ = 29 × 5 μm, n = 30), 170–220 μm long (x̄ = 189 μm, n = 30), indistinctly septate, coiled 11/4–21/4 times, becoming uncoiled in water, guttulate, hyaline, smooth-walled.

Figure 2. 

Tubeufia guttulata (HKAS 128936, holotype) a, b colonies on the host surface c–e conidiophores, conidiogenous cells and conidia f–i conidiogenous cells bearing conidia j germinated conidium k–p conidia q, r colonies on PDA, q from above r from below. Scale bars: 50 μm (c–e); 20 μm (h–p); 10 μm (f, g).

Culture characteristics

Conidia germinating on water agar and producing germ tubes within 8 h. Colonies on PDA circular with umbonate surface and undulate edge. Growth rate 21 mm diam in 42 days at 25 °C, with a brown center with pale brown edges on PDA.

Material examined

China, Hainan Province, Wuzhishan City, Shui Man Town, Wuzhishan National Nature Reserve, 18°92′N, 109°63′E, on rotting wood in a terrestrial habitat, 26 December 2021, Jian Ma, WZS70 (HKAS 128936, holotype; GZAAS 23–0408, isotype), ex-type living cultures CGMCC, GZCC 23–0404; Ibid., WZS99 (GZAAS 23–0593, paratype), living culture GZCC 23–0590.

Notes

Tubeufia guttulata is a sister species to T. cocois with 100% ML/1.00 PP supports, however, the phylogenetic tree shows that they are distinct species. Morphologically, Tubeufia guttulata differs from T. cocois in that it has longer conidiophores (101–247 μm vs. 38–123 μm) and larger conidia (170–220 μm vs. 116–136 μm). In addition, the helicoid conidia of T. guttulata become uncoiled in water, while T. cocois are coiled (Tian et al. 2022).

Tubeufia hainanensis J. Ma & Y.Z. Lu, sp. nov.

MycoBank No: 900505
Facesoffungi Number: FoF14266
Fig. 3

Etymology

The epithet ‘‘hainanensis’’ refers to the collecting site.

Holotype

HKAS 125884.

Description

Saprobic on decaying wood in moist ground. Sexual morph Undetermined. Asexual morph Hyphomycetous, helicosporous. Colonies on natural substrate superficial, effuse, gregarious, white. Mycelium superficial, partly immersed, hyaline to pale brown, septate, branched hyphae, smooth. Conidiophores macronematous, mononematous, straight to slightly flexuous, cylindrical, unbranched, septate, 44–56 μm long, 4–5 μm wide, pale brown to hyaline, smooth-walled. Conidiogenous cells holoblastic, mono- to polyblastic, integrated, sympodial, intercalary or terminal, cylindrical, with a denticulate protrusion, truncate at apex after conidial secession, 8–14 μm long, 3–5 μm wide (x̄= 9.5 × 4 μm, n = 20), hyaline to pale brown, smooth-walled. Conidia solitary, acropleurogenous, helicoid, rounded at tip, 16–21 μm diam conidial filament 1.5–4 μm wide (x̄ = 19 × 3 μm, n = 30), 127–175 μm long (x̄ = 144 μm, n = 30), indistinctly septate, coiled 31/2–33/4 times, becoming uncoiled in water, guttulate, hyaline, smooth-walled.

Figure 3. 

Tubeufia hainanensis (HKAS 125884, holotype) a, b colonies on the host surface c–e conidiophores, conidiogenous cells and conidia f–h conidiogenous cells bearing conidia j–o conidia i germinated conidium p, q colonies on PDA, p from above q from below. Scale bars: 20 μm (c–e, i–l); 10 μm (f–h, m–o).

Culture characteristics

Conidia germinating on water agar and producing germ tubes within 8 h. Colonies on PDA circular with umbonate surface and undulate edge. Growth rate 43 mm diam in 50 days at 25 °C, with a pale brown surface.

Material examined

China, Hainan Province, Haikou City, Xiuying District, Ecological leisure trail, 20°01′N, 110°25′E, on decaying wood in terrestrial habitat, 10 August 2021, Jian Ma, HK1 (HKAS 125884, holotype; GZAAS 22–2015, isotype), ex-type living cultures CGMCC, GZCC 22–2015; Ibid., HK1-2 (HKAS 125883, paratype), living culture GZCC 23–0589.

Notes

Tubeufia hainanensis resembles T. parvispora morphologically, with solitary, acropleurogenous, hyaline, helicoid conidia. However, Tubeufia hainanensis can be distinguished from T. parvispora by its unbranched conidiophores (Lu et al. 2018b). Tubeufia hainanensis formed a sister clade to Tubeufiaceae (BBC 3512) with 85% ML/0.99 PP supports (Fig. 1), and the phylogeny indicated that it is distinct species.

Tubeufia muriformis J. Ma & Y.Z. Lu, sp. nov.

MycoBank No: 900506
Facesoffungi Number: FoF14267
Fig. 4

Etymology

The epithet ‘‘muriformis’’ refers to the multi-septate conidia of this taxon.

Holotype

HKAS 128853.

Description

Saprobic on decaying bamboo in a terrestrial habitat. Sexual morph Undetermined. Asexual morph Hyphomycetous, helicosporous. Colonies on natural substrate superficial, effuse, gregarious, white. Mycelium superficial, partly immersed, hyaline to pale brown, septate, branched hyphae, smooth, with masses of crowded, glistening conidia. Conidiophores macronematous, mononematous, straight or flexuous, simple, cylindrical, branched or unbranched, indistinctly septate, 13–36 μm long, 3.5–7.5 μm wide, hyaline, smooth-walled. Conidiogenous cells holoblastic, monoblastic, integrated, sympodial, terminal, cylindrical, truncate at apex after conidial secession, hyaline, smooth-walled. Conidia solitary, acrogenous, muriform, curved, 23–25 μm diam and conidial filament 11–15 μm wide (x̄ = 24 × 13 μm, n = 20), 16.5–58.5 μm long (x̄ = 49 μm, n = 20), composed of two rows of cells with pale, multi-septate, apical cells cylindrical, basal cells truncate, constricted at septae, tapering toward base and top of conidia, coiled 1/4–1 times, not becoming loose in water, guttulate, hyaline to pale brown, thick-walled, smooth-walled.

Culture characteristics

Conidia germinating water agar and producing germ tubes within 12 h. Growth on PDA with a circular shape and umbonate surface and entire edge. Growth rate 42 mm diameter in 40 days at 25 °C with a pale brown surface.

Figure 4. 

Tubeufia muriformis (HKAS 128853, holotype) a, b colonies on the host surface c–e conidiophores, conidiogenous cells and conidia d, f–i conidiogenous cells k–o conidia j germinated conidium p, q colonies on PDA, p from above q from below. Scale bars: 20 μm (c–f, j–k); 10 μm (g–i, l–o).

Material examined

China, Guizhou Province, Qianxinan Prefecture, Xianheping National Forest Park, 24°97′N, 105°63′E, on submerged decaying wood in a freshwater stream, 16 March 2022, Jian Ma, XHP38 (HKAS 128853, holotype; GZAAS 22-2039, isotype), ex-type living cultures CGMCC, GZCC 22–2039; Ibid., XHP64 (GZAAS 23–0594, paratype), living culture GZCC 23–0591.

Notes

Tubeufia muriformis shares morphological similarities with Xenosporium helicominum, characterized by the presence of mononematous, straight or flexuous conidiophores, monoblastic, terminal, cylindrical conidiogenous cells, and muriform, curved, hyaline to pale-brown conidia. However, T. muriformis can be distinguished from X. helicominum with its branched conidiophores and larger conidia (23–25 × 11–15 μm vs. 14–16.5 × 5.5–6.5 µm; Zhao et al. 2007). Moreover, T. muriformis differs from other Tubeufia species in that it has muriform, curved conidia (Lu et al. 2018b).

The phylogenetic analysis indicated that Tubeufia muriformis formed a closely related clade with T. bambusicola, supported by ML bootstrap value of 100% and PP of 1.00. This phylogenetic relationship confirms that Tubeufia muriformis and T. bambusicola are distinct species, as demonstrated by the phylogenetic tree.

Tubeufia cocois X.G. Tian & Tibpromma et al. Journal of Fungi 8: 22 (2021).

MycoBank No: 555070
Facesoffungi Number: FoF10576
Fig. 5

Description

Saprobic on submerged decaying wood in a freshwater stream. Sexual morph Undetermined. Asexual morph Hyphomycetous, helicosporous. Colonies on natural substrate superficial, effuse, gregarious, white. Mycelium superficial and partly immersed, hyaline, septate, branched hyphae, smooth, with glistening conidia. Conidiophores macronematous, mononematous, straight or slightly flexuous, cylindrical, unbranched, septate, 33–85 μm long, 5–7.5 μm wide (x̄ = 48.5 × 6 μm, n = 20), the lower part pale brown and the upper part hyaline, smooth-walled. Conidiogenous cells holoblastic, polyblastic, integrated, sympodial, terminal, cylindrical, denticulate, with a tooth-like protrusion, 1.5–4 μm long, 1.5–2.5 μm wide, truncate at apex after conidial secession, 4.5–10.5 μm long, 4.5–6 μm wide (x̄ = 8.5 × 5.5 μm, n = 20), hyaline, smooth-walled. Conidia solitary, acropleurogenous, helicoid, rounded at tip, 23–29 μm diam and conidial filament 4–6.5 μm wide (x̄ = 26 × 5.5 μm, n = 30), 100.5–138 μm long (x̄ = 118 μm, n = 25), indistinctly septate, coiled 2–21/2 times, not becoming loose in water, guttulate, hyaline, smooth-walled.

Figure 5. 

Tubeufia cocois (GZAAS 22–2038) a, b colonies on the host surface c–f conidiophores and conidiogenous cells g–j conidiogenous cells l–q conidia k germinated conidium r, s colonies on PDA, r from above s from below. Scale bars: 20 μm (c, d, f); 10 μm (e, g–q).

Culture characteristics

Conidia germinating on water agar and producing germ tubes within 8 h. Colonies on PDA circular with flat surface and undulate edge. Growth rate 26 mm diameter in 35 days at 25 °C, with a dark brown to black surface.

Material examined

China, Hainan Province, Qiongzhong Li and Miao Autonomous County, Baihualing Rainforest cultural tourism area, 18°98′N, 109°82′E, on rotting wood in a freshwater stream, 29 December 2021, Jian Ma, BH5 (GZAAS 22–2038), living culture GZCC 22–2038.

Notes

Tian et al. (2022) introduced Tubeufia cocois from the dead leaves of Cocos nucifera in Thailand. Our newly isolated strain (GZCC 22–2038) clusters with T. cocois (MFLUCC 22–0001) with 93% ML/1.00 PP support. Morphologically, our new isolate shares the same morphological characteristics with the holotype (MFLU 21–0192) of T. cocois, thus we identified our new isolate as T. cocois. This is the first discovery of this species in a freshwater habitat and the first discovery of this species in China.

Discussion

In this study, a total of seven helicosporous hyphomycetous taxa were collected from the southern Chinese provinces of Guizhou and Hainan. By utilizing a combination of multigene phylogenetic analysis and morphological evidence, three previously unknown species were characterized and designated as Tubeufia guttulata, T. hainanensis, and T. muriformis. Additionally, an additional taxon, T. cocois, was documented for the first time in this study.

Tubeufia is the largest genus within the family Tubeufiaceae. Currently, this genus contains 59 species (Lu et al. 2018b, 2023; Rajeshkumar et al. 2019; Boonmee et al. 2021; Li et al. 2022; Tian et al. 2022), including the newly introduced species in this study, of which 29 are found in freshwater habitat, 24 in terrestrial habitats, and six from both freshwater and terrestrial habitats (Barr 1979; Rossman 1987; Ho et al. 2002; Tsui and Berbee 2006; Tsui et al. 2007; Zhao et al. 2007; Boonmee et al. 2011, 2014; Chaiwan et al. 2017; Dai et al. 2017; Doilom et al. 2017; Lu et al. 2017, 2018b, 2022, 2023; Tian et al. 2022). Among them, 39 species produce a helicosporous conidial state.

It should be noted that the morphological features of helicosporous fungi belonging to the genus Tubeufia exhibit distinct differences compared to other helicosporous genera. Summarizing the morphological characteristics of Tubeufia at the genus level is challenging due to the absence of similarity in conidiophores and conidia among its species. Such as the morphology of the newly discovered species Tubeufia muriformis resembles Xenosporium rather than Tubeufia (Goos 1990; Zhao et al. 2007). This discovery expands the asexual morphological characteristics of the genus Tubeufia, which is distinguished by conidia that are curved dorsoventrally. Lu et al. (2018b) reported dictyosporous conidia in Tubeufia, while Rajeshkumar et al. (2019) discovered a new dictyosporous asexual morph, indicating that this genus may contain many undiscovered species. In addition, the sexual morphs of Tubeufia exhibit considerable diversity, indicating a rapid evolutionary rate within this genus. The wide range of morphological variations observed may be related to the adaptation of species to environmental changes. Given the recent research progress in uncovering new structurally active compounds in Tubeufia species, there is a compelling need for further investigations into the taxonomy and secondary metabolites of this genus (Chen et al. 2020; Zeng et al. 2022; Qian et al. 2023).

Acknowledgments

We would like to thank Shaun Pennycook (Manaaki Whenua Landcare Research, New Zealand) for advising us on fungal nomenclature. The authors would like to express their sincere appreciation to the two reviewers for their invaluable input and insightful feedback. Their valuable contributions have greatly contributed to the development and improvement of this manuscript.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

This work was funded by Guizhou Provincial Key Technology R&D Program (grant No. Qian Ke He Zhi Cheng [2021] Generally 200), Guizhou Province high-level talent innovation and entrepreneurship merit funding project (No. 202104), Youth Science and Technology Talent Development Project from Guizhou Provincial Department of Education (QJHKYZ [2021]263) and the academic emerging project of the Guizhou Institute of Technology (GZLGXM-15).

Author contributions

Morphological data, photo-plates and phylogenetic analyzes were completed by Jian Ma, Li-Juan Zhang and Xing-Juan Xiao. The original draft was written by Jian Ma, and Saranyaphat Boonmee, Ning-Guo Liu, Yuan-Pin Xiao, Zong-Long Luo, Yong-Zhong Lu revised the paper.

Author ORCIDs

Jian Ma https://orcid.org/0009-0008-1291-640X

Li-Juan Zhang https://orcid.org/0000-0002-3234-6757

Saranyaphat Boonmee https://orcid.org/0000-0001-5202-2955

Xing-Juan Xiao https://orcid.org/0009-0003-8769-4534

Ning-Guo Liu https://orcid.org/0000-0002-9169-2350

Yuan-Pin Xiao https://orcid.org/0000-0003-1730-3545

Zong-Long Luo https://orcid.org/0000-0001-7307-4885

Yong-Zhong Lu https://orcid.org/0000-0002-1033-5782

Data availability

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

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