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. 2021 Aug 4;10(8):745. doi: 10.3390/biology10080745

New Species of Talaromyces (Fungi) Isolated from Soil in Southwestern China

Zhi-Kang Zhang 1, Xin-Cun Wang 2,*, Wen-Ying Zhuang 2, Xian-Hao Cheng 1, Peng Zhao 1,*
Editors: Fabiana Canini, Laura Zucconi
PMCID: PMC8389673  PMID: 34439977

Abstract

Simple Summary

Talaromyces species are distributed all around the world and occur in various environments, e.g., soil, air, living or rotten plants, and indoors. Some of them produce enzymes and pigments of industrial importance, while some cause Talaromycosis. Talaromyces marneffei, a well-known and important human pathogen, is endemic to Southeast Asia and causes high mortality, especially in HIV/AIDS patients and those with other immunodeficiencies. China covers 3 of the 35 global biodiversity hotspots. During the explorations of fungal diversity in soil samples collected at different sites of southwestern China, two new Talaromyces species, T. chongqingensis X.C. Wang and W.Y. Zhuang and T. wushanicus X.C. Wang and W.Y. Zhuang, were discovered based on phylogenetic analyses and morphological comparisons. They are described and illustrated in detail. Six phylogenetic trees of the sections Talaromyces and Trachyspermi were constructed based on three-gene datasets and revealed the phylogenetic positions of the new species. This work provided a better understanding of biodiversity and phylogeny of the genus. The results make the concepts of the two sections of Talaromyces well-established. The discovery will be beneficial for future evaluation of the potential usages and functions of the new species.

Abstract

Southwestern China belongs among the global biodiversity hotspots and the Daba Mountains are recognized as one of the priority conservation areas. During the exploration of fungal biodiversity from soil samples collected from Mount Daba, two species of Talaromyces were discovered as new to science based on phylogenetic analyses and morphological comparisons. Talaromyces chongqingensis sp. nov. is a sister taxon of T. minioluteus and T. minnesotensis in the section Trachyspermi; and T. wushanicus sp. nov., affiliated to the section Talaromyces, is closely related to T. cnidii and T. siamensis. The new species differ from their sisters in DNA sequences, growth rates, and morphological characteristics. Descriptions and illustrations of them are provided in detail.

Keywords: Ascomycota, biodiversity hotspot, DNA barcodes, Eurotiales, phylogeny, taxonomy, Trichocomaceae

1. Introduction

Talaromyces C.R. Benj. is a cosmopolitan genus occurring in various environments, e.g., soil, air, living or rotten plants, and indoors. Its beneficial and harmful effects on humans have been well documented. Enzymes and pigments produced by some species of the genus are of industrial importance, such as β-glucosidase produced by T. amestolkiae N. Yilmaz et al. [1] and T. cellulolyticus T. Fujii et al. [2], and red pigments by T. atroroseus N. Yilmaz et al. [3,4]. Talaromycosis caused by several species were also reported [5,6]. Among them, T. marneffei (Segretain et al.) Samson et al., endemic to Southeast Asia, is a well-known and important human pathogen causing high mortality in the absence of proper diagnosis and prompt treatment, especially in HIV/AIDS patients and those with other immunodeficiencies [7].

A total of 170 Talaromyces species were accepted and classified into seven sections according to a recent monographic study [8]. Moreover, T. albisclerotius B.D. Sun et al., T. aspriconidius B.D. Sun et al., T. aureolinus L. Wang, T. bannicus L. Wang, T. brevis B.D. Sun et al., T. guizhouensis B.D. Sun et al., T. penicillioides L. Wang, T. pulveris Crous, T. rufus B.D. Sun et al., T. sparsus L. Wang, T. tenuis B.D. Sun et al., and T. yunnanensis Doilom and C.F. Liao were later described [9,10,11,12]. In the section (sect.) Trachyspermi Yaguchi and Udagawa, 30 species are commonly accepted; and in the sect. Talaromyces, the largest part of the genus, 75 species have been recognized.

During the explorations of fungal diversity in soil samples collected at different sites of Chongqing and Sichuan in southwestern China, two Talaromyces species belonging to the sections Talaromyces and Trachyspermi were further discovered as new to science based on phylogenetic analyses and morphological comparisons. They are described and illustrated in detail.

2. Materials and Methods

2.1. Fungal Materials

Cultures were isolated from soil samples collected from Chongqing and areas nearby in Sichuan Province in October 2020. Dried cultures were deposited in the Herbarium Mycologicum Academiae Sinicae (HMAS), and the living ex-type strains were preserved in the China General Microbiological Culture Collection Center (CGMCC).

2.2. Morphological Observations

Morphological characterization was conducted following the standardized methods [13]. Four standard growth media were used: Czapek yeast autolysate agar (CYA, yeast extract Oxoid, Hampshire, UK), malt extract agar (MEA, Amresco, Solon, OH, USA), yeast extract agar (YES) and potato dextrose agar (PDA). The methods for inoculation, incubation, microscopic examinations, and digital recordings were following our previous studies [14,15,16].

2.3. DNA Extraction, PCR Amplification, and Sequencing

DNA was extracted from the cultures grown on PDA for 7 days using the Plant Genomic DNA Kit (DP305, TIANGEN Biotech, Beijing, China). Polymerase chain reaction (PCR) amplifications of the internal transcribed spacer (ITS), beta-tubulin (BenA), calmodulin (CaM) and RNA polymerase II second largest subunit (RPB2) gene regions were conducted with routine methods [14,15,16]. The products were purified and subject to sequencing on an ABI 3730 DNA Sequencer (Applied Biosystems, Bedford, MA, USA). Although the ITS region, the recommended standard DNA barcode for fungi, is not sufficient to discriminate the species of this genus, the sequences provided here will be helpful for other researchers in case of need.

2.4. Phylogenetic Analyses

The forward and reverse sequences newly generated in this study were assembled using Seqman v. 7.1.0 (DNASTAR Inc., Madison, WI, USA). The assembled sequences were deposited in GenBank. Previously described species from the corresponding sections, which were used for phylogenetic analyses, are listed in Table 1 and Table 2. Newly generated sequences of this study are shown in Table 3. For each section, three datasets of BenA, CaM, and RPB2 were compiled. Sequences of each dataset (35 species for sect. Trachyspermi and 79 species for sect. Talaromyces) were aligned using MAFFT v. 7.221 [17], and then manually edited in BioEdit v. 7.1.10 [18] and MEGA v. 6.0.6 [19]. Maximum likelihood (ML) analyses were performed using RAxML-HPC2 [20] on XSEDE 8.2.12 on CIPRES Science Gateway v. 3.3 [21] with the default GTRCAT model. Bayesian Inference (BI) analyses were performed with MrBayes v. 3.2.5 [22]. Appropriate nucleotide substitution models and parameters were determined by Modeltest v. 3.7 [23]. The consensus trees were viewed in FigTree v. 1.3.1 (Available online: http://tree.bio.ed.ac.uk/software/figtree/ (accessed on 1 September 2015)). The type species of section Talaromyces served as outgroup taxon of the Trachyspermi tree and vice versa.

Table 1.

Previously described Talaromyces species used in phylogenetic analyses of the sect. Trachyspermi.

Species Strain Locality Substrate ITS BenA CaM RPB2
T. aerius A.J. Chen et al. 2016 CGMCC 3.18197 T China: Beijing indoor air KU866647 KU866835 KU866731 KU866991
T. affinitatimellis Rodr.-Andr. et al. 2019 CBS 143840 T Spain honey LT906543 LT906552 LT906549 LT906546
T. albisclerotius B.D. Sun et al. 2020 CBS 141839 T China: Guizhou soil MN864276 MN863345 MN863322 MN863334
T. albobiverticillius (H.M. Hsieh et al.) Samson et al. 2011 CBS 133440 T China: Taiwan decaying leaves HQ605705 KF114778 KJ885258 KM023310
T. amyrossmaniae Rajeshkumar et al. 2019 NFCCI 1919 T India decaying fruits of Terminalia bellerica MH909062 MH909064 MH909068 MH909066
T. assiutensis Samson and Abdel-Fattah 1978 CBS 147.78 T Egypt soil JN899323 KJ865720 KJ885260 KM023305
T. atroroseus N. Yilmaz et al. 2013 CBS 133442 T South Africa house dust KF114747 KF114789 KJ775418 KM023288
T. austrocalifornicus Yaguchi and Udagawa 1993 CBS 644.95 T USA soil JN899357 KJ865732 KJ885261 MN969147
T. basipetosporus Stchigel et al. 2019 CBS 143836 T Argentina honey LT906542 LT906563 n.a. LT906545
T. brasiliensis R.N. Barbosa et al. 2018 CBS 142493 T Brazil honey MF278323 LT855560 LT855563 MN969198
T. catalonicus Guevara-Suarez et al. 2020 CBS 143039 T Spain herbivore dung LT899793 LT898318 LT899775 LT899811
T. clemensii Visagie and N. Yilmaz 2019 PPRI 26753 T South Africa wood in mine MK951940 MK951833 MK951906 MN418451
T. convolutus Udagawa 1993 CBS 100537 T Nepal soil JN899330 KF114773 MN969316 JN121414
T. diversus (Raper and Fennell) Samson et al. 2011 CBS 320.48 T USA mouldy leather KJ865740 KJ865723 KJ885268 KM023285
T. erythromellis (A.D. Hocking) Samson et al. 2011 CBS 644.80 T Australia soil JN899383 HQ156945 KJ885270 KM023290
T. guatemalensis A. Nováková et al. 2019 CCF 6215 T Guatemala soil MN322789 MN329687 MN329688 MN329689
T. halophytorum Y.H. You and S.B. Hong 2020 KACC 48127 T South Korea roots of Limonium tetragonum MH725786 MH729367 MK111426 MK111427
T. heiheensis X.C. Wang and W.Y. Zhuang 2017 CGMCC 3.18012 T China: Heilongjiang rotten wood KX447526 KX447525 KX447532 KX447529
T. minioluteus (Dierckx) Samson et al. 2011 CBS 642.68 T unknown unknown JN899346 MN969409 KJ885273 JF417443
T. minnesotensis Guevara-Suarez et al. 2017 CBS 142381 T USA human ear LT558966 LT559083 LT795604 LT795605
T. pernambucoensis R. Cruz et al. 2019 URM 6894 T Brazil soil LR535947 LR535945 LR535946 LR535948
T. resinae (Z.T. Qi and H.Z. Kong) Houbraken and X.C. Wang 2020 CGMCC 3.4387 T China: Guizhou resin of Eucalyptus tereticornis MT079858 MN969442 MT066184 MN969221
T. rubrifaciens W.W. Gao 2016 CGMCC 3.17658 T China: Beijing hospital air KR855658 KR855648 KR855653 KR855663
T. solicola Visagie and K. Jacobs 2012 DAOM 241015 T South Africa soil FJ160264 GU385731 KJ885279 KM023295
T. speluncarum Rodr.-Andr. et al. 2020 CBS 143844 T Spain sparkling wine LT985890 LT985901 LT985906 LT985911
T. subericola Rodr.-Andr. et al. 2020 CBS 144322 T Spain sparkling wine LT985888 LT985899 LT985904 LT985909
T. systylus S.M. Romero et al. 2015 BAFCcult 3419 T Argentina soil KP026917 KR233838 KR233837 n.a.
T. trachyspermus (Shear) Stolk and Samson 1973 CBS 373.48 T USA unknown JN899354 KF114803 KJ885281 JF417432
T. ucrainicus (Panas.) Udagawa 1966 CBS 162.67 T Ukraine potato starch JN899394 KF114771 KJ885282 KM023289
T. udagawae Stolk and Samson 1972 CBS 579.72 T Japan soil JN899350 KF114796 KX961260 MN969148
T. flavus (Klöcker) Stolk and Samson 1972 CBS 310.38 T New Zealand unknown JN899360 JX494302 KF741949 JF417426
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Table 2.

Previously described Talaromyces species used in phylogenetic analyses of the sect. Talaromyces.

Species Strain Locality Substrate ITS BenA CaM RPB2
T. aculeatus (Raper and Fennell) Samson et al. 2011 CBS 289.48 T USA textile KF741995 KF741929 KF741975 MH793099
T. adpressus A.J. Chen et al. 2016 CGMCC 3.18211 T China: Beijing indoor air KU866657 KU866844 KU866741 KU867001
T. alveolaris Guevara-Suarez et al. 2017 CBS 142379 T USA human bronchoalveolar lavage LT558969 LT559086 LT795596 LT795597
T. amazonensis N. Yilmaz et al. 2016 CBS 140373 T Colombia leaf litter KX011509 KX011490 KX011502 MN969186
T. amestolkiae N. Yilmaz et al. 2012 CBS 132696 T South Africa house dust JX315660 JX315623 KF741937 JX315698
T. angelicae S.H. Yu et al. 2013 KACC 46611 T South Korea dried root of Angelica gigas KF183638 KF183640 KJ885259 KX961275
T. annesophieae Houbraken 2017 CBS 142939 T Netherlands soil MF574592 MF590098 MF590104 MN969199
T. apiculatus Samson et al. 2011 CBS 312.59 T Japan soil JN899375 KF741916 KF741950 KM023287
T. argentinensis Jurjević and S.W. Peterson 2019 NRRL 28750 T Ghana soil MH793045 MH792917 MH792981 MH793108
T. aurantiacus (J.H. Mill. et al.) Samson et al. 2011 CBS 314.59 T USA soil JN899380 KF741917 KF741951 KX961285
T. aureolinus L. Wang 2021 CGMCC 3.15865 T China: Yunnan soil MK837953 MK837937 MK837945 MK837961
T. australis Visagie et al. 2015 CBS 137102 T Australia soil under pasture KF741991 KF741922 KF741971 KX961284
T. bannicus L. Wang 2021 CGMCC 3.15862 T China: Yunnan soil MK837955 MK837939 MK837947 MK837963
T. beijingensis A.J. Chen et al. 2016 CGMCC 3.18200 T China: Beijing indoor air KU866649 KU866837 KU866733 KU866993
T. calidicanius (J.L. Chen) Samson et al. 2011 CBS 112002 T China: Taiwan soil JN899319 HQ156944 KF741934 KM023311
T. californicus Jurjević and S.W. Peterson 2019 NRRL 58168 T USA air MH793056 MH792928 MH792992 MH793119
T. cnidii S.H. Yu et al. 2013 KACC 46617 T South Korea dried roots of Cnidium sp. KF183639 KF183641 KJ885266 KM023299
T. coprophilus Guevara-Suarez et al. 2020 CBS 142756 T Spain herbivore dung LT899794 LT898319 LT899776 LT899812
T. cucurbitiradicus L. Su and Y.C. Niu 2018 ACCC 39155 T China: Beijing endophyte from root of pumpkin (Cucurbita moschata) KY053254 KY053228 KY053246 n.a.
T. derxii Takada and Udagawa 1988 CBS 412.89 T Japan cultivated soil JN899327 JX494306 KF741959 KM023282
T. dimorphus X.Z. Jiang and L. Wang 2018 CGMCC 3.15692 T China: Hainan forest soil KY007095 KY007111 KY007103 KY112593
T. domesticus Jurjević and S.W. Peterson 2019 NRRL 58121 T USA floor swab MH793055 MH792927 MH792991 MH793118
T. duclauxii (Delacr.) Samson et al. 2011 CBS 322.48 T France canvas JN899342 JX091384 KF741955 JN121491
T. euchlorocarpius Yaguchi et al. 1999 CBM PF1203 T Japan soil AB176617 KJ865733 KJ885271 KM023303
T. flavovirens (Durieu and Mont.) Visagie et al. 2012 CBS 102801 T Spain unknown JN899392 JX091376 KF741933 KX961283
T. flavus (Klöcker) Stolk and Samson 1972 CBS 310.38 T New Zealand unknown JN899360 JX494302 KF741949 JF417426
T. francoae N. Yilmaz et al. 2016 CBS 113134 T Colombia leaf litter KX011510 KX011489 KX011501 MN969188
T. funiculosus (Thom) Samson et al. 2011 CBS 272.86 T India Lagenaria vulgaris JN899377 MN969408 KF741945 KM023293
T. fuscoviridis Visagie et al. 2015 CBS 193.69 T Netherlands soil KF741979 KF741912 KF741942 MN969156
T. fusiformis A.J. Chen et al. 2016 CGMCC 3.18210 T China: Beijing indoor air KU866656 KU866843 KU866740 KU867000
T. galapagensis Samson and Mahoney 1977 CBS 751.74 T Ecuador soil under Maytenus obovata JN899358 JX091388 KF741966 KX961280
T. indigoticus Takada and Udagawa 1993 CBS 100534 T Japan soil JN899331 JX494308 KF741931 KX961278
T. intermedius (Apinis) Stolk and Samson 1972 CBS 152.65 T UK swamp soil JN899332 JX091387 KJ885290 KX961282
T. kabodanensis Houbraken et al. 2016 CBS 139564 T Iran hypersaline soil KP851981 KP851986 KP851995 MN969190
T. kendrickii Visagie et al. 2015 CBS 136666 T Canada forest soil KF741987 KF741921 KF741967 MN969158
T. lentulus X.Z. Jiang and L. Wang 2018 CGMCC 3.15689 T China: Shandong soil KY007088 KY007104 KY007096 KY112586
T. liani (Kamyschko) N. Yilmaz et al. 2014 CBS 225.66 T China soil JN899395 JX091380 KJ885257 KX961277
T. louisianensis Jurjević and S.W. Peterson 2019 NRRL 35823 T USA air MH793052 MH792924 MH792988 MH793115
T. macrosporus (Stolk and Samson) Frisvad et al. 1990 CBS 317.63 T South Africa apple juice JN899333 JX091382 KF741952 KM023292
T. mae X.Z. Jiang and L. Wang 2018 CGMCC 3.15690 T China: Shanghai forest soil KY007090 KY007106 KY007098 KY112588
T. malicola Jurjević and S.W. Peterson 2019 NRRL 3724 T Italy rhizosphere of an apple tree MH909513 MH909406 MH909459 MH909567
T. mangshanicus X.C. Wang and W.Y. Zhuang 2016 CGMCC 3.18013 T China: Hunan soil KX447531 KX447530 KX447528 KX447527
T. marneffei (Segretain et al.) Samson et al. 2011 CBS 388.87 T Vietnam bamboo rat (Rhizomys sinensis) JN899344 JX091389 KF741958 KM023283
T. muroii Yaguchi et al. 1994 CBS 756.96 T China: Taiwan soil MN431394 KJ865727 KJ885274 KX961276
T. mycothecae R.N. Barbosa et al. 2018 CBS 142494 T Brazil nest of stingless bee (Melipona scutellaris) MF278326 LT855561 LT855564 LT855567
T. neofusisporus L. Wang 2016 CGMCC 3.15415 T China: Tibet leaf sample KP765385 KP765381 KP765383 MN969165
T. oumae-annae Visagie et al. 2014 CBS 138208 T South Africa house dust KJ775720 KJ775213 KJ775425 KX961281
T. panamensis (Samson et al.) Samson et al. 2011 CBS 128.89 T Panama soil JN899362 HQ156948 KF741936 KM023284
T. penicillioides L. Wang 2021 CGMCC 3.15822 T China: Guizhou soil MK837956 MK837940 MK837948 MK837964
T. pinophilus (Hedgc.) Samson et al. 2011 CBS 631.66 T France PVC JN899382 JX091381 KF741964 KM023291
T. pratensis Jurjević and S.W. Peterson 2019 NRRL 62170 T USA effluent of water treatment plant MH793075 MH792948 MH793012 MH793139
T. primulinus (Pitt) Samson et al. 2011 CBS 321.48 T USA unknown JN899317 JX494305 KF741954 KM023294
T. pseudofuniculosus Guevara-Suarez et al. 2020 CBS 143041 T Spain herbivore dung LT899796 LT898323 LT899778 LT899814
T. purgamentorum N. Yilmaz et al. 2016 CBS 113145 T Colombia leaf litter KX011504 KX011487 KX011500 MN969189
T. purpureogenus (Stoll) Samson et al. 2011 CBS 286.36 T unknown unknown JN899372 JX315639 KF741947 JX315709
T. qii L. Wang 2016 CGMCC 3.15414 T China: Tibet leaf sample KP765384 KP765380 KP765382 MN969164
T. rapidus Guevara-Suarez et al. 2017 CBS 142382 T USA human bronchoalveolar lavage LT558970 LT559087 LT795600 LT795601
T. ruber (Stoll) N. Yilmaz et al. 2012 CBS 132704 T UK aircraft fuel tank JX315662 JX315629 KF741938 JX315700
T. rubicundus (J.H. Mill. et al.) Samson et al. 2011 CBS 342.59 T USA soil JN899384 JX494309 KF741956 KM023296
T. sayulitensis Visagie et al. 2014 CBS 138204 T Mexico house dust KJ775713 KJ775206 KJ775422 MN969146
T. siamensis (Manoch and C. Ramírez) Samson et al. 2011 CBS 475.88 T Thailand forest soil JN899385 JX091379 KF741960 KM023279
T. soli Jurjević and S.W. Peterson 2019 NRRL 62165 T USA soil MH793074 MH792947 MH793011 MH793138
T. sparsus L. Wang 2021 CGMCC 3.16003 T China: Beijing soil MT077182 MT083924 MT083925 MT083926
T. stellenboschiensis Visagie and K. Jacobs 2015 CBS 135665 T South Africa soil JX091471 JX091605 JX140683 MN969157
T. stipitatus (Thom) C.R. Benj. 1955 CBS 375.48 T USA rotting wood JN899348 KM111288 KF741957 KM023280
T. stollii N. Yilmaz et al. 2012 CBS 408.93 T Netherlands AIDS patient JX315674 JX315633 JX315646 JX315712
T. striatoconidium (R.F. Castañeda and W. Gams) Houbraken et al. 2020 CBS 550.89 T Cuba leaf litter of Pachyanthus poirettii MN431418 MN969441 MN969360 MT156347
T. thailandensis Manoch et al. 2013 CBS 133147 T Thailand forest soil JX898041 JX494294 KF741940 KM023307
T. tumuli Jurjević and S.W. Peterson 2019 NRRL 62151 T USA soil from prairie MH793071 MH792944 MH793008 MH793135
T. veerkampii Visagie et al. 2015 CBS 500.78 T Columbia soil KF741984 KF741918 KF741961 KX961279
T. verruculosus (Peyronel) Samson et al. 2011 NRRL 1050 T USA soil KF741994 KF741928 KF741944 KM023306
T. versatilis Bridge and Buddie 2013 IMI 134755 T UK unknown MN431395 MN969412 MN969319 MN969161
T. viridis (Stolk and G.F. Orr) Arx 1987 CBS 114.72 T Australia soil AF285782 JX494310 KF741935 JN121430
T. viridulus Samson et al. 2011 CBS 252.87 T Australia soil JN899314 JX091385 KF741943 JF417422
T. xishaensis X.C. Wang et al. 2016 CGMCC 3.17995 T China: Hainan soil KU644580 KU644581 KU644582 MZ361364
T. trachyspermus (Shear) Stolk and Samson 1973 CBS 373.48 T USA unknown JN899354 KF114803 KJ885281 JF417432
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Table 3.

New species and newly generated sequences reported in this study.

Species Strain Locality Substrate ITS BenA CaM RPB2
T. chongqingensis X.C. Wang and W.Y. Zhuang sp. nov. CS26-67 T China: Chongqing soil MZ358001 MZ361343 MZ361350 MZ361357
CS26-63 China: Chongqing soil MZ358002 MZ361344 MZ361351 MZ361358
CS26-73 China: Chongqing soil MZ358003 MZ361345 MZ361352 MZ361359
CS26-75 China: Chongqing soil MZ358004 MZ361346 MZ361353 MZ361360
T. wushanicus X.C. Wang and W.Y. Zhuang sp. nov. CS17-05 T China: Chongqing soil MZ356356 MZ361347 MZ361354 MZ361361
CS17-04 China: Chongqing soil MZ356357 MZ361348 MZ361355 MZ361362
CS17-06 China: Chongqing soil MZ356358 MZ361349 MZ361356 MZ361363
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3. Results

3.1. Phylogenetic Analysis

The characteristics of datasets used in the phylogenetic analyses are presented in Table 4. Phylogenetic analyses of the section Trachyspermi revealed that T. chongqingensis always grouped with T. minioluteus, T. minnesotensis, and T. udagawae, having strong statistic supports. In the BenA and CaM analyses (Figure 1 and Figure 2), T. minioluteus was the closest sister of the new species; while T. minioluteus and T. minnesotensis were both closely related to T. chongqingensis in the RPB2 tree (Figure 3). In the phylogenetic analysis of section Talaromyces based on the BenA dataset, T. wushanicus clustered with T. siamensis (Figure 4); while T. cnidii and T. siamensis were closely related to the new species in the CaM and RPB2 analyses (Figure 5 and Figure 6).

Table 4.

Detailed characteristics of the datasets.

Section Loci No. of Seq. Length of Alignment Model for BI
Trachyspermi BenA 35 533 TVM+I+G
CaM 34 656 SYM+I+G
RPB2 34 920 GTR+I+G
Talaromyces BenA 79 490 TrN+I+G
CaM 79 565 SYM+I+G
RPB2 78 978 TVM+I+G
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Full names of the used models: GTR+I+G (General Time Reversible with Invariant sites and Gamma distribution); SYM+I+G (Symmetrical model with Invariant sites and Gamma distribution); TrN+I+G (Tamura–Nei model with Invariant sites and Gamma distribution); TVM+I+G (Transversion model with Invariant sites and Gamma distribution).

Figure 1.

Figure 1

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Maximum likelihood phylogeny of Talaromyces sect. Trachyspermi inferred from the BenA dataset. Bootstrap values ≥ 70% (left) or posterior probability values ≥ 0.95 (right) are indicated at nodes. Asterisk denotes 100% bootstrap or 1.00 posterior probability.

Figure 2.

Figure 2

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Maximum likelihood phylogeny of Talaromyces sect. Trachyspermi inferred from the CaM dataset. Bootstrap values ≥ 70% (left) or posterior probability values ≥ 0.95 (right) are indicated at nodes. Asterisk denotes 100% bootstrap or 1.00 posterior probability.

Figure 3.

Figure 3

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Maximum likelihood phylogeny of Talaromyces sect. Trachyspermi inferred from the RPB2 dataset. Bootstrap values ≥ 70% (left) or posterior probability values ≥ 0.95 (right) are indicated at nodes. Asterisk denotes 100% bootstrap or 1.00 posterior probability.

Figure 4.

Figure 4

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Maximum likelihood phylogeny of Talaromyces sect. Talaromyces inferred from the BenA dataset. Bootstrap values ≥ 70% (left) or posterior probability values ≥ 0.95 (right) are indicated at nodes. Asterisk denotes 100% bootstrap or 1.00 posterior probability.

Figure 5.

Figure 5

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Maximum likelihood phylogeny of Talaromyces sect. Talaromyces inferred from the CaM dataset. Bootstrap values ≥ 70% (left) or posterior probability values ≥ 0.95 (right) are indicated at nodes. Asterisk denotes 100% bootstrap or 1.00 posterior probability.

Figure 6.

Figure 6

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Maximum likelihood phylogeny of Talaromyces sect. Talaromyces inferred from the RPB2 dataset. Bootstrap values ≥ 70% (left) or posterior probability values ≥ 0.95 (right) are indicated at nodes. Asterisk denotes 100% bootstrap or 1.00 posterior probability.

3.2. Taxonomy

Talaromyces chongqingensis X.C. Wang and W.Y. Zhuang, sp. nov., Figure 7.

Figure 7.

Figure 7

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Talaromyces chongqingensis (CS26-67). (A) Colonies: top row left to right, obverse CYA, MEA, YES, and PDA; bottom row left to right, reverse CYA, MEA, YES, and PDA; (B–F) Conidiophores; (G) Conidia. Bars: (D) 15 µm, applies also to (B,C); (G) 10 µm, applies also to (E,F).

Fungal Names: FN570851

Etymology: The specific epithet refers to the type locality.

in Talaromyces sect. Trachyspermi

Typification: China, Chongqing City, Chengkou County, Daba Mountain National Nature Reserve, Gaoguan Town, at the riverside of River Ren, 31°49′40′′ N 109°0′24′′ E, in soil under a palm tree, 30 October 2020, Xin-Cun Wang, Huan-Di Zheng and Chang Liu, culture, Zhi-Kang Zhang, CS26-67 (holotype HMAS 247849, ex-type strain CGMCC 3.20482).

DNA barcodes: ITS MZ358001, BenA MZ361343, CaM MZ361350, RPB2 MZ361357.

Colony diam: after 7 days at 25 °C (unless stated otherwise): on CYA, 12–13 mm; on CYA at 37 °C, no growth; on CYA at 5 °C, no growth; on MEA, 17–18 mm; on YES 18–19 mm; on PDA, 18–19 mm.

Colony characteristics:

On CYA at 25 °C, after 7 days: colonies nearly circular, protuberant in centers; margins moderately wide, entire; mycelia white and yellow; texture velutinous; sporulation dense; conidia en masse yellowish green to dull green; soluble pigments light brown; exudates small, clear; reverse orange, buff at the margins but dark orange at centers.

On MEA at 25 °C, after 7 days: Colonies irregular, protuberant in centers, pink hyphae growing at centers; margins moderately wide, irregular; mycelia white and yellow; texture floccose; sporulation dense; conidia en masse greyish green; soluble pigments absent; exudates absent; reverse buff.

On YES at 25 °C, after 7 days: Colonies nearly circular, strongly protuberant in centers; margins moderately wide, entire; mycelia white and yellow; texture velutinous; sporulation moderately dense; conidia en masse pale green; soluble pigments light brown; exudates absent; reverse orange, yellow brown at the margins but dark orange at centers.

On PDA at 25 °C, after 7 days: Colonies nearly circular, plain, slightly protuberant in centers; margins moderately wide, irregular; mycelia white and yellow; texture velutinous; sporulation very dense; conidia en masse yellowish green; soluble pigments absent; exudates absent; reverse yellow brown, buff at the margins but orange at centers.

Micromorphology: Conidiophores biverticillate; stipes smooth-walled, 90–250 × 2.5–3.0 μm; metulae 4–5, 10–13 × 2.5–3.5 μm; phialides acerose, tapering into very thin neck, 3–5 per metula, 10–13.5 × 2.0–2.5 μm; conidia ellipsoidal to broad fusiform, smooth-walled, 2.5–3.5 × 2.0–2.5 μm.

Additional strains examined: China, Chongqing City, Chengkou County, Daba Mountain National Nature Reserve, Gaoguan Town, at the riverside of River Ren, 31°49′40″ N 109°0′24″ E, in soil under a palm tree, 30 October 2020, Xin-Cun Wang, Huan-Di Zheng and Chang Liu, culture, Zhi-Kang Zhang, CS26-63; ibid., CS26-73; ibid., CS26-75.

Notes: This species is phylogenetically close to T. minioluteus and T. minnesotensis, but differs from them in growth rate on CYA and MEA at 25 °C (Table 5) and pink hyphae present at the centers of colonies on MEA. The sequence data of the four cultures of this fungus are completely identical.

Table 5.

Cultural and morphological comparisons of new species and their closely related species.

Species CYA 25 °C (mm) CYA 37 °C (mm) MEA (mm) YES (mm) Conidia Shape Conidia Wall Conidia Size (μm) Reference
T. chongqingensis 12–13 no growth 17–18 18–19 ellipsoidal to broad fusiform smooth 2.5–3.5 × 2–2.5 This study
T. minioluteus 17–18 no growth 21–22 18 ellipsoidal smooth 2.5–4 × 1.5–2.5 [24]
T. minnesotensis 24–26 no growth 13–15 21–24 ellipsoidal smooth 2.5–3.5 × 2–3 [5]
T. udagawae 6–8 no growth 10–11 8–9 subglobose to ellipsoidal smooth 3–4 × 2–3 [24]
T. cnidii 30–35 17–20 38–43 40–45 ellipsodial smooth to finely rough 3–4 × 2–2.5 [25]
T. siamensis 20–22 15 32–33 27–28 ellipsoidal to fusiform smooth to finely rough 3–4 × 2–3 [24]
T. wushanicus 21–24 17–19 40–44 24–28 ellipsoidal to broad fusiform smooth to finely rough 3–4 × 2.5–3 This study
Open in a new tab

Talaromyces wushanicus X.C. Wang and W.Y. Zhuang, sp. nov., Figure 8.

Figure 8.

Figure 8

Open in a new tab

Talaromyces wushanicus (CS17-05). (A) Colonies: top row left to right, obverse CYA, MEA, YES, and PDA; bottom row left to right, reverse CYA, MEA, YES, and PDA; (B–F) Conidiophores; (G) Conidia. Bars: (D) 15 µm, applies also to (B,C); (G) 10 µm, applies also to (E,F).

Fungal Names: FN570852

Etymology: The specific epithet refers to the type locality.

in Talaromyces sect. Talaromyces

Typification: China, Chongqing City, Wushan County, Dachang Town, Yanghe Village, 31°17′33′′ N 109°50′44′′ E, in soil, 29 October 2020, Xin-Cun Wang, Huan-Di Zheng and Chang Liu, culture, Zhi-Kang Zhang, CS17-05 (holotype HMAS 247848, ex-type strain CGMCC 3.20481).

DNA barcodes: ITS MZ356356, BenA MZ361347, CaM MZ361354, RPB2 MZ361361.

Colony diam: after 7 days at 25 °C (unless stated otherwise): on CYA, 21–24 mm; on CYA at 37 °C, 17–19 mm; on CYA at 5 °C, no growth; on MEA, 40–44 mm; on YES, 24–28 mm; on PDA, 37–38 mm.

Colony characteristics: On CYA 25 °C, 7 days: Colonies nearly circular, protuberant in centers; margins narrow to moderately wide, nearly entire; mycelia white; texture velutinous; sporulation moderately dense; conidia en masse yellowish green; soluble pigments absent; exudates almost absent, sometimes very tiny, red, clear; reverse buff, orange to light brown at centers, but white and pink at periphery.

On CYA at 37 °C, after 7 days: Colonies irregular or nearly circular, protuberant in centers; margins moderately wide, nearly entire; mycelia white; texture velutinous; sporulation moderately dense; conidia en masse dull green to greyish green; soluble pigments absent; exudates absent; reverse buff.

On MEA at 25 °C, after 7 days: Colonies nearly circular, plain; margins wide, entire; mycelia yellow; texture velutinous; sporulation dense; conidia en masse yellowish green; soluble pigments absent; exudates almost absent, sometimes very tiny, hyaline, clear; reverse buff, but yellow to orange in centers.

On YES at 25 °C, after 7 days: Colonies nearly circular, deep, wrinkled, highly protuberant in centers; margins narrow to moderately wide, entire; mycelia white; texture velutinous; sporulation dense; conidia en masse yellowish green to dark green; soluble pigments absent; exudates absent, rarely red and clear; reverse white, yellow brown to light brown, rimose, or deeply concave in centers.

On PDA at 25 °C, after 7 days: Colonies nearly circular, plain, slightly protuberant in centers; margins moderately wide, entire; mycelia white; texture velutinous; sporulation dense; conidia en masse yellowish green; soluble pigments absent; exudates hyaline, clear, present at centers; reverse greyish white to greenish white, reddish brown at centers.

Micromorphology: Conidiophores biverticillate, rarely terverticillate; stipes smooth-walled, 85–225 × 2.0–3.0 μm; metulae 5, 9.5–11.5 × 2.5–3.0 μm; phialides acerose, tapering into very thin neck, 3–4 per metula, 10–11 × 2.0–2.5 μm; conidia ellipsoidal to broad fusiform, smooth to finely rough, 3–4 × 2.5–3 μm.

Additional strains examined: China, Chongqing City, Wushan County, Dachang Town, Yanghe Village, 31°17′33′′ N 109°50′44′′ E, in soil, 29 October 2020, Xin-Cun Wang, Huan-Di Zheng and Chang Liu, culture, Zhi-Kang Zhang, CS17-04; ibid., CS17-06.

Notes: This species is closely related to T. cnidii and T. siamensis in the phylogenetic trees (Figure 4, Figure 5 and Figure 6), but it differs from T. cnidii in obviously slower growth rate on CYA and YES at 25 °C and from T. siamensis by an obviously faster growth on MEA at 25 °C (Table 5). Sequence comparisons indicate that the isolate CS17-04 has a one-base difference in ITS and a two-base difference in BenA from the other two strains. No morphological diversification was found among the strains.

4. Discussion

Of the 35 global biodiversity hotspots, 3 are located in southwestern China, consisting of Chongqing, Guizhou, Sichuan, Tibet, and Yunnan provinces [26]. Eight hotspot regions in the southwest of China were identified as priority conservation areas, including the Daba Mountains [27] where materials used for this study were gathered. Soil samples for floristic studies of fungi were collected from Chengkou, Wushan, and Wuxi counties in Chongqing and Wanyuan City in Sichuan. Although Talaromyces is a widespread genus and distributed in more than 27 provinces, cities, or regions of China [14], it has never been reported from the above areas.

In recent years, the number of new species of Talaromyces increased dramatically. There were 12 species recorded in Talaromyces sect. Trachyspermi and 36 ones in Talaromyces sect. Talaromyces in 2014 [24]. From 2018 to 2021, 13 additional species were discovered in the former section, and 20 new members were described in the latter. We are witnessing a trend: new fungal species are described at an accelerated rate.

Talaromyces species occur in diversified environments. When the information about the extype strains of more than 100 species in these two sections is gathered (Table 1 and Table 2), it is found that soil is commonly the substrate. Fifty or so species were isolated from different kinds of soil, e.g., forest, cultivated, and swamp soil. Plant debris appears to be the second frequent source, which nearly 20 species inhabited. Four species were from humans and one, the well-known T. marneffei, from bamboo rat. Surprisingly, T. pinophilus was discovered on PVC, the third widely used plastic in the world, which is hard to biodegrade.

Among the 30 species accepted in Talaromyces sect. Trachyspermi, 6 were originally reported from China (Table 1). Moreover, 18 of the 75 species known in Talaromyces sect. Talaromyces were described based on the Chinese samples or specimens (Table 2). These data surely demonstrate that China has a high fungal diversity. With more investigations conducted, we expect to discover more new species of this group of fungi.

5. Conclusions

The present work provides a better understanding of biodiversity and phylogeny of the genus. The results make the concepts of the two sections of Talaromyces well-established and more sophisticated. The discovery will be beneficial for future evaluation of the potential usages and functions of the new species.

Acknowledgments

The authors would like to thank Huan-Di Zheng, Zhao-Qing Zeng, and Chang Liu of Institute of Microbiology, Chinese Academy of Sciences for collecting jointly the samples for this study.

Author Contributions

Conceptualization, W.-Y.Z. and P.Z.; methodology, Z.-K.Z. and X.-C.W.; software, X.-C.W.; validation, X.-C.W.; formal analysis, X.-C.W. and Z.-K.Z.; investigation, X.-C.W.; resources, W.-Y.Z., P.Z. and X.-H.C.; data curation, X.-C.W.; writing—original draft preparation, X.-C.W.; writing—review and editing, W.-Y.Z. and X.-C.W.; visualization, X.-C.W.; supervision, X.-C.W., P.Z. and W.-Y.Z.; project administration, W.-Y.Z.; funding acquisition, P.Z., W.-Y.Z. and X.-C.W. All authors have read and agreed to the published version of the manuscript.

Funding

This project was supported by the National Natural Science Foundation of China (31750001) and Key Research Program of Frontier Science, Chinese Academy of Sciences (QYZDY-SSW-SMC029).

Conflicts of Interest

The authors declare no conflict of interest.

Footnotes

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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