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

Gonçalves, Carla; Wisecaver, Jennifer H.; Kominek, Jacek; Oom, Madalena Salema; Leandro, Maria José; Shen, Xing-Xing; Opulente, Dana A.; Zhou, Xiaofan; Peris, David; Kurtzman, Cletus P.; Hittinger, Chris Todd; Rokas, Antonis; Gonçalves, Paula

doi:10.7554/elife.33034

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

Journal Article · Thu Apr 12 00:00:00 EDT 2018 · eLife

DOI:https://doi.org/10.7554/elife.33034· OSTI ID:1628879

Gonçalves, Carla ^[1]; Wisecaver, Jennifer H. ^[2]; Kominek, Jacek ^[3]; ^[4]; Leandro, Maria José ^[5]; Shen, Xing-Xing ^[6]; Opulente, Dana A. ^[7]; Zhou, Xiaofan ^[8]; ^[9]; Kurtzman, Cletus P. ^[10]; ^[7]; ^[11]; ^[12]

Universidade Nova de Lisboa, Caparica (Portugal). UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia; DOE/OSTI
Vanderbilt Univ., Nashville, TN (United States). Dept. of Biological Sciences Purdue Univ., West Lafayette, IN (United States). Dept. of Biochemistry, Purdue Center for Plant Biology
Univ. of Wisconsin, Madison, WI (United States). Laboratory of Genetics; Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center; Univ. of Wisconsin, Madison, WI (United States). J. F. Crow Institute for the Study of Evolution; Univ. of Wisconsin, Madison, WI (United States). Wisconsin Energy Institute
UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal; Centro de Investigação Interdisciplinar Egas Moniz, Instituto Universitário Egas Moniz, Caparica, Portugal
Universidade Nova de Lisboa, Av. da República, Oeiras (Portuga). Instituto de Tecnologia Química e Biológica António Xavier; LNEG – Laboratório Nacional de Energia e Geologia, Unidade de Bioenergia (UB), Lisboa ( Portugal)
Vanderbilt Univ., Nashville, TN (United States). Dept. of Biological Sciences
Univ. of Wisconsin, Madison, WI (United States). Laboratory of Genetics; Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center; Univ. of Wisconsin, Madison, WI (United States). J. F. Crow Institute for the Study of Evolution; Univ. of Wisconsin, Madison, WI (United States). Wisconsin Energy Institute
South China Agricultural Univ., Guangzhou (China). Integrative Microbiology Research Centre; South China Agricultural Univ., Guangzhou (China). Guangdong Province Key Laboratory of Microbial Signals and Disease Control
Univ. of Wisconsin, Madison, WI (United States). Laboratory of Genetics; Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center; Univ. of Wisconsin, Madison, WI (United States). J. F. Crow Institute for the Study of Evolution; Univ. of Wisconsin, Madison, WI (United States). Wisconsin Energy Institute; Institute of Agrochemistry and Food Technology (IATA), CSIC, Valencia (Spain). Dept. of Food Biotechnology
National Center for Agricultural Utilization Research, Agricultural Research Service, U.S. Department of Agriculture, Peoria (United States). Mycotoxin Prevention and Applied Microbiology Research Unit
Vanderbilt Univ., Nashville, TN (United States). Dept. of Biological Sciences
Universidade Nova de Lisboa, Caparica (Portugal). UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia

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.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: FC02-07ER64494

OSTI ID:: 1628879

Journal Information:: eLife, Journal Name: eLife Vol. 7; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

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Environment-dependent fitness gains can be driven by horizontal gene transfer of transporter-encoding genes Milner, David S.; Attah, Victoria; Cook, Emily Proceedings of the National Academy of Sciences, Vol. 116, Issue 12 https://doi.org/10.1073/pnas.1815994116	journal	March 2019
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