Adaptation of S. cerevisiae to Fermented Food Environments Reveals Remarkable Genome Plasticity and the Footprints of Domestication
2018
Legras, Jean-Luc | Galeote, Virginie | Bigey, Frederic | Camarasa, Carole | Marsit, Souhir | Nidelet, Thibault | Sanchez, Isabelle | Couloux, Arnaud | Guy, Julie | Franco-Duarte, Ricardo | Marcet-Houben, Marina | Gabaldon, Toni | Schuller, Dorit | Sampaio, José Paulo | Dequin, Sylvie | 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) | Mathématiques, Informatique et STatistique pour l'Environnement et l'Agronomie (MISTEA) ; Institut National de la Recherche Agronomique (INRA)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro) | 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) | CBMA, Department of Biology ; Universidade do Minho = University of Minho [Braga] | Centre for Genomic Regulation (CRG) | Universitat Pompeu Fabra [Barcelona] (UPF) | Unidade de Ciencias Biomoleculares Aplicadas (UCIBIO) ; Requimte ; Universidade do Porto = University of Porto-Departamento de Química (DQ) ; Faculdade de Ciências e Tecnologia = School of Science & Technology (FCT NOVA) ; Universidade Nova de Lisboa = NOVA University Lisbon (NOVA)-Universidade Nova de Lisboa = NOVA University Lisbon (NOVA)-Faculdade de Ciências e Tecnologia = School of Science & Technology (FCT NOVA) ; Universidade Nova de Lisboa = NOVA University Lisbon (NOVA)-Universidade Nova de Lisboa = NOVA University Lisbon (NOVA)-Universidade do Porto = University of Porto-Departamento de Química (DQ) ; Faculdade de Ciências e Tecnologia = School of Science & Technology (FCT NOVA) ; Universidade Nova de Lisboa = NOVA University Lisbon (NOVA)-Universidade Nova de Lisboa = NOVA University Lisbon (NOVA)-Faculdade de Ciências e Tecnologia = School of Science & Technology (FCT NOVA) ; Universidade Nova de Lisboa = NOVA University Lisbon (NOVA)-Universidade Nova de Lisboa = NOVA University Lisbon (NOVA) | GIS IBiSA-AO 2010-2011, France ; AIP Bioressources from the National Institute for Agricultural Research, Franc
The budding yeast Saccharomyces cerevisiae can be found in the wild and is also frequently associated with humanactivities. Despite recent insights into the phylogeny of this species, much is still unknown about how evolutionary processes related to anthropogenic niches have shaped the genomes and phenotypes of S. cerevisiae.To address this question, we performed population-level sequencing of 82 S. cerevisiae strains from wine, flor, rum, dairy products, bakeries, and the natural environment (oak trees). These genomic data enabled us to delineate specific genetic groups corresponding to the different ecological niches and revealed high genome content variation across the groups. Most of these strains, compared with the reference genome, possessed additional genetic elements acquired by introgression or horizontal transfer, several of which were population-specific. In addition, several genomic regions in each population showed evidence of nonneutral evolution, as shown by high differentiation, or of selective sweeps including genes with key functions in these environments (e.g., amino acid transport for wine yeast). Linking genetics to lifestyle differences and metabolite traits has enabled us to elucidate the genetic basis of several niche-specific population traits, such as growth on galactose for cheese strains. These data indicate that yeast has been subjected to various divergent selective pressures depending on its niche, requiring the development of customized genomes for better survival in these environments. These striking genome dynamics associated with local adaptation and domestication reveal the remarkable plasticity of the S. cerevisiae genome, revealing this species to be an amazing complex of specialized populations.
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