Evolutionary Advantage Conferred by an Eukaryote-to-Eukaryote Gene Transfer Event in Wine Yeasts.
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.
INRA, UMR1083, SPO, F-34060 Montpellier, France Montpellier SupAgro, UMR1083, SPO, F-34060 Montpellier, France Montpellier University, UMR1083, SPO, F-34060 Montpellier, France.
Souhir
S
Marsit
Department of Genetics, University of Valencia, and Department of Biotechnology, Institute of Agrochemistry and Food Technology, CSIC, Valencia, Spain.
Adriana
A
Mena
INRA, UMR1083, SPO, F-34060 Montpellier, France Montpellier SupAgro, UMR1083, SPO, F-34060 Montpellier, France Montpellier University, UMR1083, SPO, F-34060 Montpellier, France.
Frédéric
F
Bigey
INRA, UMR1083, SPO, F-34060 Montpellier, France Montpellier SupAgro, UMR1083, SPO, F-34060 Montpellier, France Montpellier University, UMR1083, SPO, F-34060 Montpellier, France.
François-Xavier
FX
Sauvage
CEA, Institut de Génomique, Genoscope, Centre National de Séquençage, Evry, France.
Arnaud
A
Couloux
CEA, Institut de Génomique, Genoscope, Centre National de Séquençage, Evry, France.
Julie
J
Guy
INRA, UMR1083, SPO, F-34060 Montpellier, France Montpellier SupAgro, UMR1083, SPO, F-34060 Montpellier, France Montpellier University, UMR1083, SPO, F-34060 Montpellier, France.
Jean-Luc
JL
Legras
Department of Genetics, University of Valencia, and Department of Biotechnology, Institute of Agrochemistry and Food Technology, CSIC, Valencia, Spain.
Eladio
E
Barrio
INRA, UMR1083, SPO, F-34060 Montpellier, France Montpellier SupAgro, UMR1083, SPO, F-34060 Montpellier, France Montpellier University, UMR1083, SPO, F-34060 Montpellier, France.
Sylvie
S
Dequin
INRA, UMR1083, SPO, F-34060 Montpellier, France Montpellier SupAgro, UMR1083, SPO, F-34060 Montpellier, France Montpellier University, UMR1083, SPO, F-34060 Montpellier, France galeote@supagro.inra.fr.
Virginie
V
Galeote
D000596:Amino Acids / Q000378:metabolism; D001483:Base Sequence; D005075:Biological Evolution; D018533:Biomass; D005285:Fermentation; D022761:Gene Transfer, Horizontal / Q000235:genetics*; D005800:Genes, Fungal; D005978:Glutathione / Q000378:metabolism; D059765:Homologous Recombination / Q000235:genetics; D009842:Oligopeptides / Q000378:metabolism; D010641:Phenotype; D012441:Saccharomyces cerevisiae / Q000235:genetics*; D027843:Vitis / Q000378:metabolism; D014920:Wine / Q000382:microbiology*
D000596:Amino Acids; D009842:Oligopeptides; D005978:Glutathione
FOT genes; HGT; competition; domestication; nitrogen; oligopeptides