Evidence for loss and reacquisition of alcoholic fermentation in a fructophilic yeast lineage
Carla Gonçalves,
Jennifer H Wisecaver,
Jacek Kominek,
Madalena Salema Oom,
Maria José Leandro,
Xing-Xing Shen,
Dana A Opulente,
Xiaofan Zhou,
David Peris,
Cletus P Kurtzman,
Chris Todd Hittinger,
Antonis Rokas,
Paula Gonçalves
Affiliations
Carla Gonçalves
UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal
Jennifer H Wisecaver
Department of Biological Sciences, Vanderbilt University, Nashville, United States; Department of Biochemistry, Purdue Center for Plant Biology, Purdue University, West Lafayette, United States
Jacek Kominek
Laboratory of Genetics, University of Wisconsin-Madison, Madison, United States; DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, United States; J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, United States; Wisconsin Energy Institute, University of Wisconsin-Madison, Madison, United States
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
Maria José Leandro
Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Av. da República, Oeiras, Portugal; LNEG – Laboratório Nacional de Energia e Geologia, Unidade de Bioenergia (UB), Lisboa, Portugal
Xing-Xing Shen
Department of Biological Sciences, Vanderbilt University, Nashville, United States
Dana A Opulente
Laboratory of Genetics, University of Wisconsin-Madison, Madison, United States; DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, United States; J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, United States; Wisconsin Energy Institute, University of Wisconsin-Madison, Madison, United States
Xiaofan Zhou
Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, China; Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China
Laboratory of Genetics, University of Wisconsin-Madison, Madison, United States; DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, United States; J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, United States; Wisconsin Energy Institute, University of Wisconsin-Madison, Madison, United States; Department of Food Biotechnology, Institute of Agrochemistry and Food Technology (IATA), CSIC, Valencia, Spain
Cletus P Kurtzman
Mycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, U.S. Department of Agriculture, Peoria, United States
Laboratory of Genetics, University of Wisconsin-Madison, Madison, United States; DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, United States; J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, United States; Wisconsin Energy Institute, University of Wisconsin-Madison, Madison, United States
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.
