Research Article |
Corresponding author: Feng-Li Hui ( fenglihui@yeah.net ) Academic editor: Thorsten Lumbsch
© 2021 Cheng-Feng Shi, Kai-Hong Zhang, Chun-Yue Chai, Zhen-Li Yan, Feng-Li Hui.
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:
Shi C-F, Zhang K-H, Chai C-Y, Yan Z-L, Hui F-L (2021) Diversity of the genus Sugiyamaella and description of two new species from rotting wood in China. MycoKeys 77: 27-39. https://doi.org/10.3897/mycokeys.77.60077
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Species of the genus Sugiyamaella (Trichomonascaceae, Saccharomycetales), found in rotting wood in China, were investigated using morphology and the molecular phylogeny of a combined ITS and nrLSU dataset. Nine taxa were collected in China: two were new species (viz. Sugiyamaella chuxiong sp. nov. and S. yunanensis sp. nov.) and seven were known species, S. americana, S. ayubii, S. novakii, S. paludigena, S. valenteae, S. valdiviana and S. xiaguanensis. The two new species are illustrated and their morphology and phylogenetic relationships with other Sugiyamaella species are discussed. Our results indicate a potentially great diversity of Sugiyamaella spp. inhabiting rotting wood in China just waiting to be discovered.
Phylogeny, rotted wood-inhabiting yeast, Sugiyamaella, taxonomy, Trichomonascaceae
Sugiyamaella Kurtzman & Robnett (2007) is typified by Sugiyamaella smithiae, which was initially classified in the genus Stephanoascus (
The members of Sugiyamaella have been described in association with insects. They were isolated either directly from wood-ingesting insects and insect frass or from common insect habitats, such as rotting wood, forest soil, mushrooms and peat (
Sugiyamaella has a worldwide distribution and most of its species were originally found in Europe, North America and South America (
Rotting wood samples were collected in two areas of Yunnan Province, China. The areas were located in the Xishuangbanna Primeval Forest Park of Jinghong (21°98'N, 100°88'E) and Zixi Mountain of Chuxiong (25°03'N, 101°41'E). The predominant vegetation is characterised as tropical and subtropical forest biome. The climate is hot and humid, with annual precipitation between 1,000 to 1,600 mm and an average temperature that ranges from 14.8 to 21.9 °C. Sixty decayed wood samples were collected during July to August in 2016–2018. The samples were stored in sterile plastic bags and transported under refrigeration to the laboratory over a period of no more than 24 h. The yeast strains were isolated from rotting wood samples in accordance with the methods described by
The morphological, physiological and biochemical properties were determined according to those used by
Genomic DNA was extracted from the yeast using an Ezup Column Yeast Genomic DNA Purification Kit, according to the manufacturer’s instructions (Sangon Biotech, Shanghai, China). The nuc rDNA ITS1-5.8S-ITS2 (ITS) region was amplified using primer pairs ITS1/ITS4 (
The sequences obtained from this study and the reference sequences downloaded from GenBank (Table
Sequences used in molecular phylogenetic analysis. Entries in bold are newly generated for this study.
Species | Strain | Locality | Sample | ITS | D1/D2 |
---|---|---|---|---|---|
Sugiyamaella americana | NRRL YB-2067T | USA | Frass | NR_137759 | DQ438193 |
S. americana | NYNU 17714 | China | Rotting wood | MT965698 | MT965699 |
S. ayubii |
|
Brazil | Rotting wood | NR_155796 | KR184132 |
S. ayubii | NYNU 177171 | China | Rotting wood | MT965704 | MT965705 |
S. bahiana |
|
Brazil | Rotting wood | NR_155810 | KC959941 |
S. bonitensis |
|
Brazil | Rotting wood | NR_155798 | KT006004 |
S. boreocaroliniensis | NRRL YB-1835T | USA | Frass | NR_165963 | DQ438221 |
S. bullrunensis |
|
USA | Insect | NR_111543 | HM208601 |
S. castrensis | NRRL Y-17329T | Chile | Rotting wood | NR_111229 | DQ438195 |
S. carassensis |
|
Brazil | Rotting wood | NR_155808 | KX550111 |
S. chiloensis | NRRL Y-17643T | Chile | Rotted wood | DQ911454 | DQ438217 |
S. floridensis | NRRL YB-3827T | USA | Frass | NR_111230 | DQ438222 |
S. grinbergsii | NRRL Y-27117T | Chile | Insect | KY102116 | DQ438199 |
S. japonica | NRRL YB-2798T | Japan | Frass | NR_111239 | DQ438202 |
S. ligni |
|
Brazil | Rotting wood | KX550112 | KX550112 |
S. lignohabitans | NRRL YB-1473T | USA | Decayed log | NR_119622 | DQ438198 |
S. marionensis | NRRL YB-1336T | USA | Decayed log | NR_111237 | DQ438197 |
S. marilandica | NRRL YB-1847T | USA | Frass | NR_165965 | DQ438219 |
S. mastotermitis |
|
Berlin | Termite | NR_156606 | KU883286 |
S. neomexicana |
|
USA | Frass | NR_165966 | DQ438201 |
S. novakii | NRRL Y-27346T | Hungary | Rotting wood | NR_111235 | DQ438196 |
S. novakii | NYNU 17778 | China | Rotting wood | MT965702 | MT965703 |
S. paludigena | NRRL Y-12697T | Russia | Peat | NR_111236 | DQ438194 |
S. paludigena | NYNU 1771 | China | Rotting wood | MT965696 | MT965697 |
S. paludigena | NYNU 177116 | China | Rotting wood | MT966075 | MT966074 |
S. pinicola |
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USA | Frass | NR_165967 | DQ438200 |
S. qingdaonensis |
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China | Rotting wood | NR_151806 | FJ613527 |
S. smithiae | NRRL Y-17850T | Brazil | Soil | DQ911455 | DQ438218 |
S. trypani |
|
Poland | Soil | MK388412 | MK387312 |
S. valdiviana | NRRL Y-7791T | Chile | Rotting wood | NR_111544 | DQ438220 |
S. valdiviana | NYNU17755 | China | Rotting wood | MT965700 | MT965701 |
S. valenteae |
|
Brazil | Rotting wood | NR_155797 | KT005999 |
S. valenteae | NYNU 17795 | China | Rotting wood | MT965706 | MT965707 |
S. xiaguanensis | NYNU 161041T | China | Rotting wood | KY213802 | KY213817 |
S. xiaguanensis | NYNU 17753 | China | Rotting wood | MT969346 | MT969344 |
S. xylanicola |
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Brazil | Rotting wood | KC493642 | KC493642 |
S. xylolytica |
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Brazil | Rotting wood | KU214874 | KF889433 |
S. yunanensis | NYNU 161059T | China | Rotting wood | MT257259 | MT257257 |
S. yunanensis | NYNU 16113 | China | Rotting wood | MT257256 | MT257261 |
Candida sp. | W370 | Taiwan | Forest soil | JN581120 | JN581115 |
Candida sp. | GA2M09 | Taiwan | Mushroom | FJ873591 | FJ873521 |
S. chuxiongensis | NYNU 181038T | China | Rotting wood | MK682800 | MK682795 |
S. chuxiongensis | NYNU 18521 | China | Rotting wood | MT257260 | MT257255 |
S. chuxiongensis | NYNU 18634 | China | Rotting wood | MT257258 | MT257262 |
Schizosaccharomyces pombe | NRRL Y-12796T | – | – | KY105378 | AY048171 |
Maximum Parsimony analysis was performed using a heuristic search option with tree-bisection reconnection (TBR) branch swapping (
The alignment was based on the combined nuclear dataset (ITS and nrLSU), included 31 taxa and one outgroup taxon (Schizosaccharomyces pombe NRRL Y-12796) and was comprised of 976 characters including gaps (385 for ITS and 591 for nrLSU) in the aligned matrix. Of these characters, 452 were constant, 164 variable characters were parsimony-uninformative and 360 characters were parsimony-informative. The heuristic search, using MP analysis, generated the most parsimonious tree (TL = 1627, CI = 0.457, RI = 0.766, RC = 0.394). The best model applied in the ML analysis was GTR+I+G. The ML analysis yielded a best scoring tree with a final optimisation likelihood value of –8651.84. Two methods for phylogenetic tree construction resulted in a similar topology. Therefore, only the best scoring PhyML tree is shown with BS and BT values simultaneously in Fig.
From the phylogenetic tree (Fig.
Maximum Likelihood phylogenetic tree of Sugiyamaella inferred from the combined ITS and nrLSU dataset and rooted with Schizosaccharomyces pombe NRRL Y-12796. The ML and MP bootstrap support values above 50% are shown at the first and second positions, respectively. Newly-sequenced collections are in black boldface.
China, Yunnan Province, Jinghong City, Mengyang Town, in rotting wood from a tropical rainforest, July 2016, K.F. Liu & L. Zhang (holotype NYNU 161059T, culture ex-type
The species name yunanensis (N.L. fem. adj.) refers to the geographical origin of the type strain of this species.
The cells are ovoid to elongate (2.5–5.5 × 3–7.5 μm) and occur singly or in pairs after being placed in YM broth for 3 days at 25 °C (Fig.
China, Yunnan Province, Jinghong City, Mengyang Town, in rotting wood from a tropical rainforest, July 2016, K.F. Liu & L. Zhang, NYNU 16113.
Two isolates, representing S. yunanensis, are retrieved in a well-supported clade and appear most closely related to S. valdiviana (Fig.
China, Yunnan Province, Chuxiong City, Zixi Town, in rotting wood from Zixi Mountain, August 2018, K.F. Liu & Z.W. Xi (holotype NYNU 181038T, culture ex-type
The cells are ovoid to elongate (2.5–4 × 3–4.5 μm) and occur singly or in pairs after growth in a YM broth for 3 days at 25 °C (Fig.
China, Yunnan Province, Chuxiong City, Zixi Town, in rotting wood from Zixi Mountain, August 2018, K.F. Liu & Z.W. Xi, NYNU 18521, NYNU 18634.
We generated sequences for three isolates of S. chuxiong, NYNU 18521, NYNU 181038 and NYNU 18634. This new species is phylogenetically most closely related to S. valenteae and S. ayubii (Fig.
In this study, nine Sugiyamaella species were identified, based on morphological and molecular phylogenetic analyses. All species were isolated from rotting wood collected in Yunnan Province, China. As a result, S. chuxiong and S. yunanensis are proposed as new species in Sugiyamaella for their distinct phylogenic positions and distinctive physiological traits. In addition, identification of seven known species of Sugiyamaella, S. americana, S. ayubii, S. novakii, S. paludigena, S. valenteae, S. valdiviana and S. xiaguanensis were clearly distinguished by both morphological and molecular approaches.
Molecular phylogeny studies on Sugiyamaella and related genera have been carried out recently (
Many new yeast species have been identified in the last ten years in China (
Sugiyamaella species have a worldwide distribution and are isolated from a wide range of substrates. Insect is their main habitat, but new species were also isolated from frass, rotting wood, decayed log, forest soil, mushrooms and peat (
We sincerely thank Dr. Lin Zhang, Dr. Kai-Fang Liu and Dr. Zhi-Wen Xi for their help with collecting specimens. This project was supported by Grant No. 31570021 from the National Natural Science Foundation of China, China, No. 2018001 from the State Key Laboratory of Motor Vehicle Biofuel Technology, Henan Tianguan Enterprise Group Co. Ltd., China.