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Title: Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids

Abstract

The wild, cold-adapted parent of hybrid lager-brewing yeasts, Saccharomyces eubayanus, has a complex and understudied natural history. The exploration of this diversity can be used both to develop new brewing applications and to enlighten our understanding of the dynamics of yeast evolution in the wild. Here, we integrate whole genome sequence and phenotypic data of 200 S. eubayanus strains, the largest collection known to date. S. eubayanus has a multilayered population structure, consisting of two major populations that are further structured into six subpopulations. Four of these subpopulations are found exclusively in the Patagonian region of South America; one is found predominantly in Patagonia and sparsely in Oceania and North America; and one is specific to the Holarctic ecozone. Plant host associations differed between subpopulations and between S. eubayanus and its sister species, Saccharomyces uvarum. S. eubayanus is most abundant and genetically diverse in northern Patagonia, where some locations harbor more genetic diversity than is found outside of South America, suggesting that northern Patagonia east of the Andes was a glacial refugium for this species. All but one subpopulation shows isolation-by-distance, and gene flow between subpopulations is low. However, there are strong signals of ancient and recent outcrossing, including twomore » admixed lineages, one that is sympatric with and one that is mostly isolated from its parental populations. Using our extensive biogeographical data, we build a robust model that predicts all known and a handful of additional regions of the globe that are climatically suitable for S. eubayanus, including Europe where host accessibility and competitive exclusion by other Saccharomyces species may explain its continued elusiveness. We conclude that this industrially relevant species has rich natural diversity with many factors contributing to its complex distribution and natural history.« less

Authors:
 [1]; ORCiD logo [2];  [3]; ORCiD logo [1];  [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [4]; ORCiD logo [4]; ORCiD logo [3]; ORCiD logo [1];  [5]
  1. Univ. of Wisconsin, Madison, WI (United States)
  2. Univ. of Wisconsin, Madison, WI (United States); Inst. of Agrochemistry and Food Technology (IATA), Valencia (Spain)
  3. Univ. Nacional del Comahue, Bariloche (Argentina)
  4. Inst. de Investigacion y Desarrollo enIngenierıa de Procesos, Neuquen (Argentina)
  5. Univ. of North Carolina, Chapel Hill, NC (United States)
Publication Date:
Research Org.:
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Contributing Org.:
University of Wisconsin Biotechnology Center DNA Sequencing Facility; Agricultural Research Service (ARS) NRRL collection
OSTI Identifier:
1637493
Grant/Contract Number:  
SC0018409; FC02-07ER64494
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Genetics
Additional Journal Information:
Journal Volume: 16; Journal Issue: 4; Journal ID: ISSN 1553-7404
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; phylogeography; species diversity; South America; Saccharomyces cerevisiae; Europe; biogeography; nucleotide sequencing; Saccharomyces

Citation Formats

Langdon, Quinn K., Peris, David, Eizaguirre, Juan I., Opulente, Dana A., Buh, Kelly V., Sylvester, Kayla, Jarzyna, Martin, Rodríguez, María E., Lopes, Christian A., Libkind, Diego, Hittinger, Chris Todd, and Copenhaver, Gregory P. Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids. United States: N. p., 2020. Web. doi:10.1371/journal.pgen.1008680.
Langdon, Quinn K., Peris, David, Eizaguirre, Juan I., Opulente, Dana A., Buh, Kelly V., Sylvester, Kayla, Jarzyna, Martin, Rodríguez, María E., Lopes, Christian A., Libkind, Diego, Hittinger, Chris Todd, & Copenhaver, Gregory P. Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids. United States. https://doi.org/10.1371/journal.pgen.1008680
Langdon, Quinn K., Peris, David, Eizaguirre, Juan I., Opulente, Dana A., Buh, Kelly V., Sylvester, Kayla, Jarzyna, Martin, Rodríguez, María E., Lopes, Christian A., Libkind, Diego, Hittinger, Chris Todd, and Copenhaver, Gregory P. Mon . "Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids". United States. https://doi.org/10.1371/journal.pgen.1008680. https://www.osti.gov/servlets/purl/1637493.
@article{osti_1637493,
title = {Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids},
author = {Langdon, Quinn K. and Peris, David and Eizaguirre, Juan I. and Opulente, Dana A. and Buh, Kelly V. and Sylvester, Kayla and Jarzyna, Martin and Rodríguez, María E. and Lopes, Christian A. and Libkind, Diego and Hittinger, Chris Todd and Copenhaver, Gregory P.},
abstractNote = {The wild, cold-adapted parent of hybrid lager-brewing yeasts, Saccharomyces eubayanus, has a complex and understudied natural history. The exploration of this diversity can be used both to develop new brewing applications and to enlighten our understanding of the dynamics of yeast evolution in the wild. Here, we integrate whole genome sequence and phenotypic data of 200 S. eubayanus strains, the largest collection known to date. S. eubayanus has a multilayered population structure, consisting of two major populations that are further structured into six subpopulations. Four of these subpopulations are found exclusively in the Patagonian region of South America; one is found predominantly in Patagonia and sparsely in Oceania and North America; and one is specific to the Holarctic ecozone. Plant host associations differed between subpopulations and between S. eubayanus and its sister species, Saccharomyces uvarum. S. eubayanus is most abundant and genetically diverse in northern Patagonia, where some locations harbor more genetic diversity than is found outside of South America, suggesting that northern Patagonia east of the Andes was a glacial refugium for this species. All but one subpopulation shows isolation-by-distance, and gene flow between subpopulations is low. However, there are strong signals of ancient and recent outcrossing, including two admixed lineages, one that is sympatric with and one that is mostly isolated from its parental populations. Using our extensive biogeographical data, we build a robust model that predicts all known and a handful of additional regions of the globe that are climatically suitable for S. eubayanus, including Europe where host accessibility and competitive exclusion by other Saccharomyces species may explain its continued elusiveness. We conclude that this industrially relevant species has rich natural diversity with many factors contributing to its complex distribution and natural history.},
doi = {10.1371/journal.pgen.1008680},
journal = {PLoS Genetics},
number = 4,
volume = 16,
place = {United States},
year = {Mon Apr 06 00:00:00 EDT 2020},
month = {Mon Apr 06 00:00:00 EDT 2020}
}

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Cited by: 17 works
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Figures / Tables:

Fig 1 Fig 1: S. eubayanus distribution and population structure. S. eubayanus has a global distribution and two major populations with six subpopulations. (A) World map showing isolation locations of S. eubayanus strains not from North or South America. Points represent one strain colored by subpopulation. Details of sites and subpopulations foundmore » in North America (B) and South America (C) with circle size scaled by the number of strains. (D) Whole genome PCA of S. eubayanus strains and five hybrids with large contributions from S. eubayanus. (E) PCA of just PA. (F) PCA of just PB and hybrid S. eubayanus sub-genomes. Color legends in A and D apply to this and all other figures.« less

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Works referencing / citing this record:

An Out-of-Patagonia migration explains the worldwide diversity and distribution of Saccharomyces eubayanus lineages
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Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.