Adaptation of s. Cerevisiae to fermented food environments reveals remarkable genome plasticity and the footprints of domestication

Jean Luc Legras, Virginie Galeote, Frederic Bigey, Carole Camarasa, Souhir Marsit, Thibault Nidelet, Isabelle Sanchez, Arnaud Couloux, Julie Guy, Ricardo Franco-Duarte, Marina Marcet-Houben, Toni Gabaldon, Dorit Schuller, Jose Paulo Sampaio, Sylvie Dequin

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

The budding yeast Saccharomyces cerevisiae can be found in the wild and is also frequently associated with human activities. 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.

Original languageEnglish
Pages (from-to)1712-1727
Number of pages16
JournalMolecular Biology And Evolution
Volume35
Issue number7
DOIs
Publication statusPublished - 1 Jan 2018

Fingerprint

fermented foods
domestication
footprint
plasticity
genome
Genome
Food
Saccharomyces cerevisiae
food
niches
yeast
niche
Population
Wine
genomics
Yeasts
rum
yeasts
Quercus
wine yeasts

Keywords

  • Adaptation
  • Domestication
  • Horizontal gene transfer
  • Saccharomyces cerevisiae
  • Sweep

Cite this

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, Jose Paulo ; Dequin, Sylvie. / Adaptation of s. Cerevisiae to fermented food environments reveals remarkable genome plasticity and the footprints of domestication. In: Molecular Biology And Evolution. 2018 ; Vol. 35, No. 7. pp. 1712-1727.
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abstract = "The budding yeast Saccharomyces cerevisiae can be found in the wild and is also frequently associated with human activities. 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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Legras, JL, Galeote, V, Bigey, F, Camarasa, C, Marsit, S, Nidelet, T, Sanchez, I, Couloux, A, Guy, J, Franco-Duarte, R, Marcet-Houben, M, Gabaldon, T, Schuller, D, Sampaio, JP & Dequin, S 2018, 'Adaptation of s. Cerevisiae to fermented food environments reveals remarkable genome plasticity and the footprints of domestication' Molecular Biology And Evolution, vol. 35, no. 7, pp. 1712-1727. https://doi.org/10.1093/molbev/msy066

Adaptation of s. Cerevisiae to fermented food environments reveals remarkable genome plasticity and the footprints of domestication. / 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, Jose Paulo; Dequin, Sylvie.

In: Molecular Biology And Evolution, Vol. 35, No. 7, 01.01.2018, p. 1712-1727.

Research output: Contribution to journalArticle

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AU - Legras, Jean Luc

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AU - Marsit, Souhir

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AU - Sanchez, Isabelle

AU - Couloux, Arnaud

AU - Guy, Julie

AU - Franco-Duarte, Ricardo

AU - Marcet-Houben, Marina

AU - Gabaldon, Toni

AU - Schuller, Dorit

AU - Sampaio, Jose Paulo

AU - Dequin, Sylvie

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