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Title: Complex ancestries of lager-brewing hybrids were shaped by standing variation in the wild yeast Saccharomyces eubayanus

Journal Article · · PLoS Genetics

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 alestyle 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. Furthermore, we conclude that the relationships among wild strains of S. eubayanus and their domesticated hybrids reflect complex biogeographical and genetic processes.

Research Organization:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Organization:
USDOE
Grant/Contract Number:
FC02-07ER64494
OSTI ID:
1363953
Journal Information:
PLoS Genetics, Vol. 12, Issue 7; ISSN 1553-7404
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 67 works
Citation information provided by
Web of Science

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Cited By (36)

Characterization of Saccharomyces uvarum (Beijerinck, 1898) and related hybrids: assessment of molecular markers that predict the parent and hybrid genomes and a proposal to name yeast hybrids journal March 2017
Loss of Heterozygosity Drives Adaptation in Hybrid Yeast journal March 2017
Designing New Yeasts for Craft Brewing: When Natural Biodiversity Meets Biotechnology journal January 2020
Saccharomyces interspecies hybrids as model organisms for studying yeast adaptation to stressful environments: Adaptation of Saccharomyces hybrids to stressful environments journal January 2018
Temperature preference can bias parental genome retention during hybrid evolution journal September 2019
Structural, Physiological and Regulatory Analysis of Maltose Transporter Genes in Saccharomyces eubayanus CBS 12357T journal August 2018
Genome Diversity and Evolution in the Budding Yeasts (Saccharomycotina) journal June 2017
sppIDer: A Species Identification Tool to Investigate Hybrid Genomes with High-Throughput Sequencing journal September 2018
sppIDer: a species identification tool to investigate hybrid genomes with high-throughput sequencing journal May 2018
Mitochondrial DNA and temperature tolerance in lager yeasts journal January 2019
Horizontal transfer and proliferation of Tsu4 in Saccharomyces paradoxus journal June 2018
Natural Variation in the Multidrug Efflux Pump SGE1 Underlies Ionic Liquid Tolerance in Yeast journal July 2018
Discordant evolution of mitochondrial and nuclear yeast genomes at population level posted_content November 2019
New yeasts—new brews: modern approaches to brewing yeast design and development journal June 2017
Comparative genomics provides new insights into the diversity, physiology, and sexuality of the only industrially exploited tremellomycete: Phaffia rhodozyma journal November 2016
Discordant evolution of mitochondrial and nuclear yeast genomes at population level journal May 2020
Fermentation innovation through complex hybridization of wild and domesticated yeasts journal October 2019
Himalayan Saccharomyces eubayanus Genome Sequences Reveal Genetic Markers Explaining Heterotic Maltotriose Consumption by Saccharomyces pastorianus Hybrids journal September 2019
Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production journal March 2017
Novel brewing yeast hybrids: creation and application journal November 2016
On the origins and industrial applications of Saccharomyces cerevisiae × Saccharomyces kudriavzevii hybrids : Origins and applications of S. cerevisiae x S. kudriavzevii hybrids journal December 2017
Saccharomyces arboricola and Its Hybrids’ Propensity for Sake Production: Interspecific Hybrids Reveal Increased Fermentation Abilities and a Mosaic Metabolic Profile journal January 2020
A polyploid admixed origin of beer yeasts derived from European and Asian wine populations journal March 2019
Chromosome level assembly and comparative genome analysis confirm lager-brewing yeasts originated from a single hybridization journal December 2019
Interspecific hybridization facilitates niche adaptation in beer yeast journal October 2019
Horizontal transfer and proliferation of Tsu4 in Saccharomyces paradoxus posted_content March 2018
Phylogeography of the wild Lager-brewing ancestor ( Saccharomyces eubayanus ) in Patagonia journal October 2018
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A polyploid admixed origin of beer yeasts derived from European and Asian wine populations posted_content November 2018
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Evolution of a novel chimeric maltotriose transporter in Saccharomyces eubayanus from parent proteins unable to perform this function journal April 2019
Bioprospecting for brewers: Exploiting natural diversity for naturally diverse beers journal February 2019
Aneuploidy in yeast: Segregation error or adaptation mechanism? journal August 2019
Tolerance to winemaking stress conditions of Patagonian strains of Saccharomyces eubayanus and Saccharomyces uvarum journal July 2017
Hybridization is a recurrent evolutionary stimulus in wild yeast speciation journal February 2019
Mitochondrial‐encoded endonucleases drive recombination of protein‐coding genes in yeast journal September 2019

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