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 clos...

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Main Authors:	Marsit, Souhir, Mena, Adriana, Bigey, Frédéric, Sauvage, François-Xavier, Couloux, Arnaud, Guy, Julie, Legras, Jean-Luc, Barrio, Eladio, Dequin, Sylvie, Galeote, Virginie
Format:	Online
Language:	English
Published:	Oxford University Press 2015
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4476156/

id	pubmed-4476156
recordtype	oai_dc
spelling	pubmed-44761562015-06-24 Evolutionary Advantage Conferred by an Eukaryote-to-Eukaryote Gene Transfer Event in Wine Yeasts Marsit, Souhir Mena, Adriana Bigey, Frédéric Sauvage, François-Xavier Couloux, Arnaud Guy, Julie Legras, Jean-Luc Barrio, Eladio Dequin, Sylvie Galeote, Virginie Discoveries 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. Oxford University Press 2015-07 2015-03-06 /pmc/articles/PMC4476156/ /pubmed/25750179 http://dx.doi.org/10.1093/molbev/msv057 Text en © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Marsit, Souhir Mena, Adriana Bigey, Frédéric Sauvage, François-Xavier Couloux, Arnaud Guy, Julie Legras, Jean-Luc Barrio, Eladio Dequin, Sylvie Galeote, Virginie
spellingShingle	Marsit, Souhir Mena, Adriana Bigey, Frédéric Sauvage, François-Xavier Couloux, Arnaud Guy, Julie Legras, Jean-Luc Barrio, Eladio Dequin, Sylvie Galeote, Virginie Evolutionary Advantage Conferred by an Eukaryote-to-Eukaryote Gene Transfer Event in Wine Yeasts
author_facet	Marsit, Souhir Mena, Adriana Bigey, Frédéric Sauvage, François-Xavier Couloux, Arnaud Guy, Julie Legras, Jean-Luc Barrio, Eladio Dequin, Sylvie Galeote, Virginie
author_sort	Marsit, Souhir
title	Evolutionary Advantage Conferred by an Eukaryote-to-Eukaryote Gene Transfer Event in Wine Yeasts
title_short	Evolutionary Advantage Conferred by an Eukaryote-to-Eukaryote Gene Transfer Event in Wine Yeasts
title_full	Evolutionary Advantage Conferred by an Eukaryote-to-Eukaryote Gene Transfer Event in Wine Yeasts
title_fullStr	Evolutionary Advantage Conferred by an Eukaryote-to-Eukaryote Gene Transfer Event in Wine Yeasts
title_full_unstemmed	Evolutionary Advantage Conferred by an Eukaryote-to-Eukaryote Gene Transfer Event in Wine Yeasts
title_sort	evolutionary advantage conferred by an eukaryote-to-eukaryote gene transfer event in wine yeasts
description	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.
publisher	Oxford University Press
publishDate	2015
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4476156/
_version_	1613238628658446336

Evolutionary Advantage Conferred by an Eukaryote-to-Eukaryote Gene Transfer Event in Wine Yeasts

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