Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus

Lager-style beers constitute the vast majority of the beer market, and yet, the genetic origin of the yeast strains that brew them has been shrouded in mystery and controversy. Unlike ale-style beers, which are generally brewed with Saccharomyces cerevisiae, lagers are brewed at colder temperatures...

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Autores: Peris Navarro, David, Langdon, Quinn K., Moriarty, Ryan V., Sylvester, Kayla, Bontrager, Martin, Charron, Guillaume, Leducq, Jean-Baptiste, Landry, Christian R., Libkind, Diego, Hittinger, Chris Todd
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2016
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/378165
Acceso en línea:http://hdl.handle.net/10261/378165
https://api.elsevier.com/content/abstract/scopus_id/84982847704
Access Level:acceso abierto
Palabra clave:Yeasts
Saccharomyces eubayanus
Lager brewing
Genetic variation
Phylogenetics
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oai_identifier_str oai:digital.csic.es:10261/378165
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus
title Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus
spellingShingle Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus
Peris Navarro, David
Yeasts
Saccharomyces eubayanus
Lager brewing
Genetic variation
Phylogenetics
title_short Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus
title_full Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus
title_fullStr Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus
title_full_unstemmed Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus
title_sort Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus
dc.creator.none.fl_str_mv Peris Navarro, David
Langdon, Quinn K.
Moriarty, Ryan V.
Sylvester, Kayla
Bontrager, Martin
Charron, Guillaume
Leducq, Jean-Baptiste
Landry, Christian R.
Libkind, Diego
Hittinger, Chris Todd
author Peris Navarro, David
author_facet Peris Navarro, David
Langdon, Quinn K.
Moriarty, Ryan V.
Sylvester, Kayla
Bontrager, Martin
Charron, Guillaume
Leducq, Jean-Baptiste
Landry, Christian R.
Libkind, Diego
Hittinger, Chris Todd
author_role author
author2 Langdon, Quinn K.
Moriarty, Ryan V.
Sylvester, Kayla
Bontrager, Martin
Charron, Guillaume
Leducq, Jean-Baptiste
Landry, Christian R.
Libkind, Diego
Hittinger, Chris Todd
author2_role author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv National Science Foundation (US)
Natural Sciences and Engineering Research Council of Canada
Agencia Nacional de Promoción Científica y Tecnológica (Argentina)
Consejo Nacional de Investigaciones Científicas y Técnicas (Argentina)
National Institute of Food and Agriculture (US)
Great Lakes Bioenergy Research Center (US)
Peris Navarro, David [0000-0001-9912-8802]
Moriarty, Ryan V. [0000-0001-7100-1906]
Bontrager, Martin [0000-0003-3013-6155]
dc.subject.none.fl_str_mv Yeasts
Saccharomyces eubayanus
Lager brewing
Genetic variation
Phylogenetics
topic Yeasts
Saccharomyces eubayanus
Lager brewing
Genetic variation
Phylogenetics
description Lager-style beers constitute the vast majority of the beer market, and yet, the genetic origin of the yeast strains that brew them has been shrouded in mystery and controversy. Unlike ale-style beers, which are generally brewed with Saccharomyces cerevisiae, lagers are brewed at colder temperatures with allopolyploid hybrids of Saccharomyces eubayanus x S. cerevisiae. Since the discovery of S. eubayanus in 2011, additional strains have been isolated from South America, North America, Australasia, and Asia, but only interspecies hybrids have been isolated in Europe. Here, using genome sequence data, we examine the relationships of these wild S. eubayanus strains to each other and to domesticated lager strains. Our results support the existence of a relatively low-diversity (π = 0.00197) lineage of S. eubayanus whose distribution stretches across the Holarctic ecozone and includes wild isolates from Tibet, new wild isolates from North America, and the S. eubayanus parents of lager yeasts. This Holarctic lineage is closely related to a population with higher diversity (π = 0.00275) that has been found primarily in South America but includes some widely distributed isolates. A second diverse South American population (π = 0.00354) and two early-diverging Asian subspecies are more distantly related. We further show that no single wild strain from the Holarctic lineage is the sole closest relative of lager yeasts. Instead, different parts of the genome portray different phylogenetic signals and ancestry, likely due to outcrossing and incomplete lineage sorting. Indeed, standing genetic variation within this wild Holarctic lineage of S. eubayanus is responsible for genetic variation still segregating among modern lager-brewing hybrids. We conclude that the relationships among wild strains of S. eubayanus and their domesticated hybrids reflect complex biogeographical and genetic processes.
publishDate 2016
dc.date.none.fl_str_mv 2016
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/378165
https://api.elsevier.com/content/abstract/scopus_id/84982847704
url http://hdl.handle.net/10261/378165
https://api.elsevier.com/content/abstract/scopus_id/84982847704
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv PLoS genetics
The underlying dataset has been published as supplementary material of the article in the publisher platform at https://doi.org/10.1371/journal.pgen.1006155
https://doi.org/10.1371/journal.pgen.1006155
No
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Public Library of Science
publisher.none.fl_str_mv Public Library of Science
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanusPeris Navarro, DavidLangdon, Quinn K.Moriarty, Ryan V.Sylvester, KaylaBontrager, MartinCharron, GuillaumeLeducq, Jean-BaptisteLandry, Christian R.Libkind, DiegoHittinger, Chris ToddYeastsSaccharomyces eubayanusLager brewingGenetic variationPhylogeneticsLager-style beers constitute the vast majority of the beer market, and yet, the genetic origin of the yeast strains that brew them has been shrouded in mystery and controversy. Unlike ale-style beers, which are generally brewed with Saccharomyces cerevisiae, lagers are brewed at colder temperatures with allopolyploid hybrids of Saccharomyces eubayanus x S. cerevisiae. Since the discovery of S. eubayanus in 2011, additional strains have been isolated from South America, North America, Australasia, and Asia, but only interspecies hybrids have been isolated in Europe. Here, using genome sequence data, we examine the relationships of these wild S. eubayanus strains to each other and to domesticated lager strains. Our results support the existence of a relatively low-diversity (π = 0.00197) lineage of S. eubayanus whose distribution stretches across the Holarctic ecozone and includes wild isolates from Tibet, new wild isolates from North America, and the S. eubayanus parents of lager yeasts. This Holarctic lineage is closely related to a population with higher diversity (π = 0.00275) that has been found primarily in South America but includes some widely distributed isolates. A second diverse South American population (π = 0.00354) and two early-diverging Asian subspecies are more distantly related. We further show that no single wild strain from the Holarctic lineage is the sole closest relative of lager yeasts. Instead, different parts of the genome portray different phylogenetic signals and ancestry, likely due to outcrossing and incomplete lineage sorting. Indeed, standing genetic variation within this wild Holarctic lineage of S. eubayanus is responsible for genetic variation still segregating among modern lager-brewing hybrids. We conclude that the relationships among wild strains of S. eubayanus and their domesticated hybrids reflect complex biogeographical and genetic processes.This material is based upon work supported by the National Science Foundation Graduate Research Fellowship under Grant No. DGE-1256259 to QKL and MB; QKL and MB were also supported by the Predoctoral Training Program in Genetics, funded by the National Institutes of Health (5 T32 GM007133-40). CRL was funded by a Discovery grant from the Natural Sciences and Engineering Research Council of Canada (NSERC). CRL holds the Canada Research Chair in Evolutionary Cell and Systems Biology. DL was funded by ANPCyT (PICT2011-1814, and PICT2014-2542), UNComahue (B171), CONICET (11220130100392CO), and NSF-CONICET Bilateral Cooperation Projects. This material is based upon work supported by the National Science Foundation under Grant No. DEB-1253634 to CTH, by USDA National Institute of Food and Agriculture Hatch Project 1003258, and funded in part by the DOE Great Lakes Bioenergy Research Center (DOE Office of Science BER DE-FC02-07ER64494).Peer reviewedPublic Library of ScienceNational Science Foundation (US)Natural Sciences and Engineering Research Council of CanadaAgencia Nacional de Promoción Científica y Tecnológica (Argentina)Consejo Nacional de Investigaciones Científicas y Técnicas (Argentina)National Institute of Food and Agriculture (US)Great Lakes Bioenergy Research Center (US)Peris Navarro, David [0000-0001-9912-8802]Moriarty, Ryan V. [0000-0001-7100-1906]Bontrager, Martin [0000-0003-3013-6155]202520252016info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/378165https://api.elsevier.com/content/abstract/scopus_id/84982847704reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)InglésPLoS geneticsThe underlying dataset has been published as supplementary material of the article in the publisher platform at https://doi.org/10.1371/journal.pgen.1006155https://doi.org/10.1371/journal.pgen.1006155Noinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3781652026-05-22T06:33:51Z
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