Evolutionary advantage conferred by an eukaryote-to-eukaryote gene transfer event in wine yeasts
2015
Marsit, Souhir | Mena, Adriana | Bigey, Frederic | Sauvage, Francois Xavier | Couloux, Arnaud | Guy, Julie | Legras, Jean-Luc | Barrio, Eladio | Dequin, Sylvie | Galeote, Virginie | Sciences Pour l'Oenologie (SPO) ; Université Montpellier 1 (UM1)-Institut National de la Recherche Agronomique (INRA)-Université de Montpellier (UM)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro) | Department of Genetics ; Stanford University | Department of Biotechnology, Institute of Agrochemistry and Food Technology ; Consejo Superior de Investigaciones Cientificas [España] = Spanish National Research Council [Spain] (CSIC) | Genoscope - Centre national de séquençage [Evry] (GENOSCOPE) ; Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)) ; Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)
Although an increasing number of horizontal gene transfers have been reported in eukaryotes, experimental evidence for their adaptive value is lacking. Here, we report the recent transfer of a 158-kb genomic region between Torulaspora microellipsoides and Saccharomyces cerevisiae wine yeasts or closely related strains. This genomic region has undergone several rearrangements in S. cerevisiae strains, including gene loss and gene conversion between two tandemly duplicated FOT genes encoding oligopeptide transporters. We show that FOT genes confer a strong competitive advantage during grape must fermentation by increasing the number and diversity of oligopeptides that yeast can utilize as a source of nitrogen, thereby improving biomass formation, fermentation efficiency, and cell viability. Thus, the acquisition of FOT genes has favored yeast adaptation to the nitrogen-limited wine fermentation environment. This finding indicates that anthropic environments offer substantial ecological opportunity for evolutionary diversification through gene exchange between distant yeast species.
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