Title: A genome-informed higher rank classification of the biotechnologically important fungal subphylum Saccharomycotina

Abstract

The subphylum Saccharomycotina is a lineage in the fungal phylum Ascomycota that exhibits levels of genomic diversity similar to those of plants and animals. The Saccharomycotina consist of more than 1 200 known species currently divided into 16 families, one order, and one class. Species in this subphylum are ecologically and metabolically diverse and include important opportunistic human pathogens, as well as species important in biotechnological applications. Many traits of biotechnological interest are found in closely related species and often restricted to single phylogenetic clades. However, the biotechnological potential of most yeast species remains unexplored. Although the subphylum Saccharomycotina has much higher rates of genome sequence evolution than its sister subphylum, Pezizomycotina, it contains only one class compared to the 16 classes in Pezizomycotina. The third subphylum of Ascomycota, the Taphrinomycotina, consists of six classes and has approximately 10 times fewer species than the Saccharomycotina. These data indicate that the current classification of all these yeasts into a single class and a single order is an underappreciation of their diversity. Our previous genome-scale phylogenetic analyses showed that the Saccharomycotina contains 12 major and robustly supported phylogenetic clades; seven of these are current families (Lipomycetaceae, Trigonopsidaceae, Alloascoideaceae, Pichiaceae, Phaffomycetaceae, Saccharomycodaceae, andmore » Saccharomycetaceae), one comprises two current families (Dipodascaceae and Trichomonascaceae), one represents the genus Sporopachydermia, and three represent lineages that differ in their translation of the CUG codon (CUG-Ala, CUG-Ser1, and CUG-Ser2). Using these analyses in combination with relative evolutionary divergence and genome content analyses, we propose an updated classification for the Saccharomycotina, including seven classes and 12 orders that can be diagnosed by genome content. This updated classification is consistent with the high levels of genomic diversity within this subphylum and is necessary to make the higher rank classification of the Saccharomycotina more comparable to that of other fungi, as well as to communicate efficiently on lineages that are not yet formally named.« less

Authors:

Groenewald, M. ^[1]; Hittinger, C. T. ^[2]; Bensch, K. ^[1]; Opulente, D. A. ^[3]; Shen, X. -X. ^[4]; Li, Y. ^[5]; Liu, C. ^[4]; LaBella, A. L. ^[6]; Zhou, X. ^[7]; Limtong, S. ^[8]; Jindamorakot, S. ^[9]; Gonçalves, P. ^[10]; Robert, V. ^[1]; Wolfe, K. H. ^[11]; Rosa, C. A. ^[12]; Boekhout, T. ^[13]; Ĉadež, N. ^[14]; Péter, G. ^[15]; Sampaio, J. P. ^[10]; Lachance, M. -A. ^[16] more »; Yurkov, A. M. ^[17]; Daniel, H. -M. ^[18]; Takashima, M. ^[19]; Boundy-Mills, K. ^[20]; Libkind, D. ^[21]; Aoki, K. ^[19]; Sugita, T. ^[22]; Rokas, A. ^[23] « less

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+ Show Author Affiliations

1. Westerdijk Fungal Biodiversity Institute, Utrecht (Netherlands)
2. Univ. of Wisconsin, Madison, WI (United States)
3. Univ. of Wisconsin, Madison, WI (United States); Villanova Univ., PA (United States)
4. Zhejiang Univ., Hangzhou (China)
5. Shandong Univ., Qingdao, Shandong (China)
6. Univ. of North Carolina, Charlotte, NC (United States)
7. South China Agricultural University, Guangzhou (China)
8. Kasetsart University, Bangkok (Thailand)
9. National Science and Technology Development Agency, Pathum Thani (Thailand)
10. Universidade Nova de Lisboa, Caparica (Portugal)
11. University College Dublin (Ireland)
12. Universidade Federal de Minas Gerais, Belo Horizonte (Brazil)
13. King Saud Univ., Riyadh (Saudi Arabia)
14. Univ. of Ljubljana (Slovenia)
15. Hungarian University of Agriculture and Life Sciences, Budapest (Hungary)
16. Univ. of Western Ontario, London, ON (Canada)
17. Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Braunscheig (Germany)
18. Universite Catholique de Louvain, Louvain-la-Neuve (Belgium)
19. Tokyo University of Agriculture (Japan)
20. Univ. of California, Davis, CA (United States)
21. Universidad Nacional del Comahue, San Carlos de Bariloche (Argentina)
22. Meiji Pharmaceutical University, Tokyo (Japan)
23. Vanderbilt Univ., Nashville, TN (United States)

Publication Date:

Thu May 25 00:00:00 EDT 2023

Research Org.:

Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)

Sponsoring Org.:

USDOE Office of Science (SC), Biological and Environmental Research (BER); Institution for Fermentation, Osaka (IFO); Belgian Science Policy Office; National Science Foundation (NSF); USDA National Institute of Food and Agriculture; National Institutes of Health (NIH); National Institute of Allergy and Infectious Diseases (NIAID)

Contributing Org.:

NCBI Taxonomy Team

OSTI Identifier:

1992330

Grant/Contract Number:  

SC0018409; C5/00/BCCM; DEB-1442148; DEB-2110403; DEB-1442113; DEB2110404; R01 AI153356

Resource Type:

Accepted Manuscript

Journal Name:

Studies in Mycology

Additional Journal Information:

Journal Volume: 105; Journal Issue: 1; Journal ID: ISSN 0166-0616

Publisher:

Elsevier

Country of Publication:

United States

Language:

English

Subject:

59 BASIC BIOLOGICAL SCIENCES; higher rank classification; novel taxa; orthologous groups (OGs); saccharomycotina; taxonomy; yeasts