Genomic factors shape carbon and nitrogen metabolic niche breadth across Saccharomycotina yeasts

Author:

Opulente Dana A.123ORCID,LaBella Abigail Leavitt456ORCID,Harrison Marie-Claire45ORCID,Wolters John F.12ORCID,Liu Chao7ORCID,Li Yonglin8ORCID,Kominek Jacek129ORCID,Steenwyk Jacob L.4510ORCID,Stoneman Hayley R.1211,VanDenAvond Jenna12ORCID,Miller Caroline R.12ORCID,Langdon Quinn K.1ORCID,Silva Margarida1213,Gonçalves Carla1451213,Ubbelohde Emily J.12ORCID,Li Yuanning41415ORCID,Buh Kelly V.1,Jarzyna Martin116ORCID,Haase Max A. B.121718ORCID,Rosa Carlos A.19ORCID,ČCadež Neža20ORCID,Libkind Diego21ORCID,DeVirgilio Jeremy H.22ORCID,Hulfachor Amanda Beth12ORCID,Kurtzman Cletus P.22,Sampaio José Paulo1213,Gonçalves Paula1213,Zhou Xiaofan48ORCID,Shen Xing-Xing47ORCID,Groenewald Marizeth23ORCID,Rokas Antonis45ORCID,Hittinger Chris Todd12ORCID

Affiliation:

1. Laboratory of Genetics, Wisconsin Energy Institute, Center for Genomic Science Innovation, J. F. Crow Institute for the Study of Evolution, University of Wisconsin–Madison, Madison, WI 53726, USA.

2. DOE Great Lakes Bioenergy Research Center, University of Wisconsin–Madison, Madison, WI 53726, USA.

3. Biology Department, Villanova University, Villanova, PA 19085, USA.

4. Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA.

5. Evolutionary Studies Initiative, Vanderbilt University, Nashville, TN 37235, USA.

6. North Carolina Research Center (NCRC), Department of Bioinformatics and Genomics, The University of North Carolina at Charlotte, Kannapolis, NC 28081, USA.

7. College of Agriculture and Biotechnology and Centre for Evolutionary and Organismal Biology, Zhejiang University, Hangzhou 310058, China.

8. Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou 510642, China.

9. LifeMine Therapeutics, Inc., Cambridge, MA 02140, USA.

10. Howard Hughes Medical Institute and the Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA.

11. University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA.

12. UCIBIO, Department of Life Sciences, NOVA School of Science and Technology, Universidade NOVA de Lisboa, Caparica, Portugal.

13. Associate Laboratory i4HB, NOVA School of Science and Technology, Universidade NOVA de Lisboa, Caparica, Portugal.

14. Institute of Marine Science and Technology, Shandong University, Qingdao 266237, China.

15. Laboratory for Marine Biology and Biotechnology, Qingdao Marine Science and Technology Center, Qingdao 266237, China.

16. Graduate Program in Neuroscience and Department of Biology, Washington University School of Medicine, St. Louis, MO 63130, USA.

17. Vilcek Institute of Graduate Biomedical Sciences and Institute for Systems Genetics, NYU Langone Health, New York, NY 10016, USA.

18. Department of Mechanistic Cell Biology, Max Planck Institute of Molecular Physiology, 44227 Dortmund, Germany.

19. Departamento de Microbiologia, ICB, C.P. 486, Universidade Federal de Minas Gerais, Belo Horizonte, MG, 31270-901, Brazil.

20. Food Science and Technology Department, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.

21. Centro de Referencia en Levaduras y Tecnología Cervecera (CRELTEC), Instituto Andino Patagónico de Tecnologías Biológicas y Geoambientales (IPATEC), Universidad Nacional del Comahue, CONICET, CRUB, Quintral 1250, San Carlos de Bariloche, 8400, Río Negro, Argentina.

22. Mycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, Peoria, IL 61604, USA.

23. Westerdijk Fungal Biodiversity Institute, 3584 CT Utrecht, Netherlands.

Abstract

Organisms exhibit extensive variation in ecological niche breadth, from very narrow (specialists) to very broad (generalists). Two general paradigms have been proposed to explain this variation: (i) trade-offs between performance efficiency and breadth and (ii) the joint influence of extrinsic (environmental) and intrinsic (genomic) factors. We assembled genomic, metabolic, and ecological data from nearly all known species of the ancient fungal subphylum Saccharomycotina (1154 yeast strains from 1051 species), grown in 24 different environmental conditions, to examine niche breadth evolution. We found that large differences in the breadth of carbon utilization traits between yeasts stem from intrinsic differences in genes encoding specific metabolic pathways, but we found limited evidence for trade-offs. These comprehensive data argue that intrinsic factors shape niche breadth variation in microbes.

Publisher

American Association for the Advancement of Science (AAAS)

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