The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts
Abstract
The dramatic phenotypic changes that occur in organisms during domestication leave indelible imprints on their genomes. Although many domesticated plants and animals have been systematically compared with their wild genetic stocks, the molecular and genomic processes underlying fungal domestication have received less attention. Here, we present a nearly complete genome assembly for the recently described yeast species Saccharomyces eubayanus and compare it to the genomes of multiple domesticated alloploid hybrids of S. eubayanus × S. cerevisiae (S. pastorianus syn. S. carlsbergensis), which are used to brew lager-style beers. We find that the S. eubayanus subgenomes of lager-brewing yeasts have experienced increased rates of evolution since hybridization, and that certain genes involved in metabolism may have been particularly affected. Interestingly, the S. eubayanus subgenome underwent an especially strong shift in selection regimes, consistent with more extensive domestication of the S. cerevisiae parent prior to hybridization. In contrast to recent proposals that lager-brewing yeasts were domesticated following a single hybridization event, the radically different neutral site divergences between the subgenomes of the two major lager yeast lineages strongly favor at least two independent origins for the S. cerevisiae × S. eubayanus hybrids that brew lager beers. In conclusion, our findings demonstrate howmore »
- Authors:
-
- Univ. of Wisconsin, Madison, WI (United States)
- Univ. of Wisconsin, Madison, WI (United States); Univ. Nacional del Comahue-CONICET, Bariloche (Argentina)
- Univ. of Wisconsin, Madison, WI (United States). Biotechnology Center
- Univ. Nacional del Comahue-CONICET, Bariloche (Argentina)
- Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center
- 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); National Science Foundation (NSF)
- Contributing Org.:
- Univ. Nacional del Comahue-CONICET, Bariloche (Argentina)
- OSTI Identifier:
- 1343408
- Alternate Identifier(s):
- OSTI ID: 1438256
- Grant/Contract Number:
- FC02-07ER64494; DEB-1253634
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Molecular Biology and Evolution
- Additional Journal Information:
- Journal Volume: 32; Journal Issue: 11; Journal ID: ISSN 0737-4038
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Saccharomyces eubayanus; domestication; genome assembly; hybridization; lager brewing
Citation Formats
Baker, Emily Clare, Wang, Bing, Bellora, Nicolas, Peris, David, Hulfachor, Amanda Beth, Koshalek, Justin A., Adams, Marie, Libkind, Diego, and Hittinger, Chris Todd. The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts. United States: N. p., 2015.
Web. doi:10.1093/molbev/msv168.
Baker, Emily Clare, Wang, Bing, Bellora, Nicolas, Peris, David, Hulfachor, Amanda Beth, Koshalek, Justin A., Adams, Marie, Libkind, Diego, & Hittinger, Chris Todd. The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts. United States. https://doi.org/10.1093/molbev/msv168
Baker, Emily Clare, Wang, Bing, Bellora, Nicolas, Peris, David, Hulfachor, Amanda Beth, Koshalek, Justin A., Adams, Marie, Libkind, Diego, and Hittinger, Chris Todd. Tue .
"The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts". United States. https://doi.org/10.1093/molbev/msv168. https://www.osti.gov/servlets/purl/1343408.
@article{osti_1343408,
title = {The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts},
author = {Baker, Emily Clare and Wang, Bing and Bellora, Nicolas and Peris, David and Hulfachor, Amanda Beth and Koshalek, Justin A. and Adams, Marie and Libkind, Diego and Hittinger, Chris Todd},
abstractNote = {The dramatic phenotypic changes that occur in organisms during domestication leave indelible imprints on their genomes. Although many domesticated plants and animals have been systematically compared with their wild genetic stocks, the molecular and genomic processes underlying fungal domestication have received less attention. Here, we present a nearly complete genome assembly for the recently described yeast species Saccharomyces eubayanus and compare it to the genomes of multiple domesticated alloploid hybrids of S. eubayanus × S. cerevisiae (S. pastorianus syn. S. carlsbergensis), which are used to brew lager-style beers. We find that the S. eubayanus subgenomes of lager-brewing yeasts have experienced increased rates of evolution since hybridization, and that certain genes involved in metabolism may have been particularly affected. Interestingly, the S. eubayanus subgenome underwent an especially strong shift in selection regimes, consistent with more extensive domestication of the S. cerevisiae parent prior to hybridization. In contrast to recent proposals that lager-brewing yeasts were domesticated following a single hybridization event, the radically different neutral site divergences between the subgenomes of the two major lager yeast lineages strongly favor at least two independent origins for the S. cerevisiae × S. eubayanus hybrids that brew lager beers. In conclusion, our findings demonstrate how this industrially important hybrid has been domesticated along similar evolutionary trajectories on multiple occasions.},
doi = {10.1093/molbev/msv168},
journal = {Molecular Biology and Evolution},
number = 11,
volume = 32,
place = {United States},
year = {Tue Aug 11 00:00:00 EDT 2015},
month = {Tue Aug 11 00:00:00 EDT 2015}
}
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- Microbial Cell Factories, Vol. 16, Issue 1
Interspecific hybridization facilitates niche adaptation in beer yeast
journal, October 2019
- Gallone, Brigida; Steensels, Jan; Mertens, Stijn
- Nature Ecology & Evolution, Vol. 3, Issue 11
Horizontal transfer and proliferation of Tsu4 in Saccharomyces paradoxus
posted_content, March 2018
- Bergman, Casey M.
- bioRxiv
Exploring the potential of Saccharomyces eubayanus as a parent for new interspecies hybrid strains in winemaking
journal, July 2017
- Magalhães, Frederico; Krogerus, Kristoffer; Castillo, Sandra
- FEMS Yeast Research, Vol. 17, Issue 5
Interspecies Hybridisation and Genome Chimerisation in Saccharomyces: Combining of Gene Pools of Species and Its Biotechnological Perspectives
journal, December 2018
- Sipiczki, Matthias
- Frontiers in Microbiology, Vol. 9
Chromosome level assembly and comparative genome analysis confirm lager-brewing yeasts originated from a single hybridization
journal, December 2019
- Salazar, Alex N.; Gorter de Vries, Arthur R.; van den Broek, Marcel
- BMC Genomics, Vol. 20, Issue 1
Evolutionary biology through the lens of budding yeast comparative genomics
journal, July 2017
- Marsit, Souhir; Leducq, Jean-Baptiste; Durand, Éléonore
- Nature Reviews Genetics, Vol. 18, Issue 10
Evolution of a novel chimeric maltotriose transporter in Saccharomyces eubayanus from parent proteins unable to perform this function
journal, April 2019
- Baker, EmilyClare P.; Hittinger, Chris Todd
- PLOS Genetics, Vol. 15, Issue 4
A Unique Saccharomyces cerevisiae × Saccharomyces uvarum Hybrid Isolated From Norwegian Farmhouse Beer: Characterization and Reconstruction
journal, September 2018
- Krogerus, Kristoffer; Preiss, Richard; Gibson, Brian
- Frontiers in Microbiology, Vol. 9
Reducing phenolic off-flavors through CRISPR-based gene editing of the FDC1 gene in Saccharomyces cerevisiae x Saccharomyces eubayanus hybrid lager beer yeasts
journal, January 2019
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Social wasps promote social behavior in Saccharomyces spp.
journal, February 2016
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Diacetyl control during brewery fermentation via adaptive laboratory engineering of the lager yeast Saccharomyces pastorianus
journal, October 2018
- Gibson, Brian; Vidgren, Virve; Peddinti, Gopal
- Journal of Industrial Microbiology & Biotechnology, Vol. 45, Issue 12
Traditional Norwegian Kveik Are a Genetically Distinct Group of Domesticated Saccharomyces cerevisiae Brewing Yeasts
journal, September 2018
- Preiss, Richard; Tyrawa, Caroline; Krogerus, Kristoffer
- Frontiers in Microbiology, Vol. 9
Genome Analysis of the Yeast M14, an Industrial Brewing Yeast Strain Widely Used in China
journal, October 2018
- Liu, Chunfeng; Niu, Chengtuo; Zhao, Yun
- Journal of the American Society of Brewing Chemists, Vol. 76, Issue 4
Independent domestication events in the blue‐cheese fungus Penicillium roqueforti
journal, February 2020
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- Molecular Ecology, Vol. 29, Issue 14
Traditional Norwegian Kveik Yeasts: Underexplored Domesticated Saccharomyces cerevisiae Yeasts
posted_content, September 2017
- Preiss, Richard; Tyrawa, Caroline; van der Merwe, George
- BioRxiv
Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus
journal, July 2016
- Peris, David; Langdon, Quinn K.; Moriarty, Ryan V.
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Microbial acidification, alcoholization, and aroma production during spontaneous lambic beer production
journal, August 2018
- De Roos, Jonas; De Vuyst, Luc
- Journal of the Science of Food and Agriculture, Vol. 99, Issue 1