Evidence for loss and reacquisition of alcoholic fermentation in a fructophilic yeast lineage

Author:

Gonçalves Carla1,Wisecaver Jennifer H23,Kominek Jacek4567,Oom Madalena Salema18ORCID,Leandro Maria José910,Shen Xing-Xing2,Opulente Dana A4567,Zhou Xiaofan1112,Peris David456713ORCID,Kurtzman Cletus P14,Hittinger Chris Todd4567ORCID,Rokas Antonis2ORCID,Gonçalves Paula1ORCID

Affiliation:

1. UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal

2. Department of Biological Sciences, Vanderbilt University, Nashville, United States

3. Department of Biochemistry, Purdue Center for Plant Biology, Purdue University, West Lafayette, United States

4. Laboratory of Genetics, University of Wisconsin-Madison, Madison, United States

5. DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, United States

6. J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, United States

7. Wisconsin Energy Institute, University of Wisconsin-Madison, Madison, United States

8. Centro de Investigação Interdisciplinar Egas Moniz, Instituto Universitário Egas Moniz, Caparica, Portugal

9. Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Av. da República, Oeiras, Portugal

10. LNEG – Laboratório Nacional de Energia e Geologia, Unidade de Bioenergia (UB), Lisboa, Portugal

11. Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, China

12. Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China

13. Department of Food Biotechnology, Institute of Agrochemistry and Food Technology (IATA), CSIC, Valencia, Spain

14. Mycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, U.S. Department of Agriculture, Peoria, United States

Abstract

Fructophily is a rare trait that consists of the preference for fructose over other carbon sources. Here, we show that in a yeast lineage (the Wickerhamiella/Starmerella, W/S clade) comprised of fructophilic species thriving in the high-sugar floral niche, the acquisition of fructophily is concurrent with a wider remodeling of central carbon metabolism. Coupling comparative genomics with biochemical and genetic approaches, we gathered ample evidence for the loss of alcoholic fermentation in an ancestor of the W/S clade and subsequent reinstatement through either horizontal acquisition of homologous bacterial genes or modification of a pre-existing yeast gene. An enzyme required for sucrose assimilation was also acquired from bacteria, suggesting that the genetic novelties identified in the W/S clade may be related to adaptation to the high-sugar environment. This work shows how even central carbon metabolism can be remodeled by a surge of HGT events.

Funder

Fundação para a Ciência e a Tecnologia

National Science Foundation

National Institute of Food and Agriculture

Wisconsin Alumni Research Foundation

DOE Great Lakes Bioenergy Research Center

Pew Charitable Trusts

European Regional Development Fund

H2020 Marie Skłodowska-Curie Actions

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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