The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts

Baker, Emily Clare; Wang, Bing; Bellora, Nicolas; Peris, David; Hulfachor, Amanda Beth; Koshalek, Justin A.; Adams, Marie; Libkind, Diego; Hittinger, Chris Todd

doi:10.1093/molbev/msv168

Title: The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts

Journal Article · Tue Aug 11 00:00:00 EDT 2015 · Molecular Biology and Evolution

DOI:https://doi.org/10.1093/molbev/msv168· OSTI ID:1343408

Baker, Emily Clare ^[1]; Wang, Bing ^[1]; Bellora, Nicolas ^[2]; Peris, David ^[1]; Hulfachor, Amanda Beth ^[1]; Koshalek, Justin A. ^[3]; Adams, Marie ^[3]; Libkind, Diego ^[4]; Hittinger, Chris Todd ^[5]

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

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.

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Research Organization:: Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)

Contributing Organization:: Univ. Nacional del Comahue-CONICET, Bariloche (Argentina)

Grant/Contract Number:: FC02-07ER64494; DEB-1253634

OSTI ID:: 1343408

Alternate ID(s):: OSTI ID: 1438256

Journal Information:: Molecular Biology and Evolution, Vol. 32, Issue 11; ISSN 0737-4038

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 126 works

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Himalayan Saccharomyces eubayanus Genome Sequences Reveal Genetic Markers Explaining Heterotic Maltotriose Consumption by Saccharomyces pastorianus Hybrids Brouwers, Nick; Brickwedde, Anja; Gorter de Vries, Arthur R. Applied and Environmental Microbiology, Vol. 85, Issue 22 https://doi.org/10.1128/aem.01516-19	journal	September 2019
Novel brewing yeast hybrids: creation and application Krogerus, Kristoffer; Magalhães, Frederico; Vidgren, Virve Applied Microbiology and Biotechnology, Vol. 101, Issue 1 https://doi.org/10.1007/s00253-016-8007-5	journal	November 2016
Whole genome sequencing, de novo assembly and phenotypic profiling for the new budding yeast species Saccharomyces jurei Naseeb, Samina; Alsammar, Haya; Burgis, Tim G3: Genes\|Genomes\|Genetics https://doi.org/10.1101/339929	journal	June 2018
On the origins and industrial applications of Saccharomyces cerevisiae × Saccharomyces kudriavzevii hybrids : Origins and applications of S. cerevisiae x S. kudriavzevii hybrids Peris, David; Pérez-Torrado, Roberto; Hittinger, Chris Todd Yeast, Vol. 35, Issue 1 https://doi.org/10.1002/yea.3283	journal	December 2017
Genome Diversity and Evolution in the Budding Yeasts (Saccharomycotina) Dujon, Bernard A.; Louis, Edward J. Genetics, Vol. 206, Issue 2 https://doi.org/10.1534/genetics.116.199216	journal	June 2017
Structural, Physiological and Regulatory Analysis of Maltose Transporter Genes in Saccharomyces eubayanus CBS 12357T Brickwedde, Anja; Brouwers, Nick; van den Broek, Marcel Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01786	journal	August 2018
Chromosome level assembly and comparative genome analysis confirm lager-brewing yeasts originated from a single hybridization Salazar, Alex N.; Gorter de Vries, Arthur R.; van den Broek, Marcel BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-6263-3	journal	December 2019
Inheritance of brewing-relevant phenotypes in constructed Saccharomyces cerevisiae × Saccharomyces eubayanus hybrids Krogerus, Kristoffer; Seppänen-Laakso, Tuulikki; Castillo, Sandra Microbial Cell Factories, Vol. 16, Issue 1 https://doi.org/10.1186/s12934-017-0679-8	journal	April 2017
Interspecific hybridization facilitates niche adaptation in beer yeast Gallone, Brigida; Steensels, Jan; Mertens, Stijn Nature Ecology & Evolution, Vol. 3, Issue 11 https://doi.org/10.1038/s41559-019-0997-9	journal	October 2019
Horizontal transfer and proliferation of Tsu4 in Saccharomyces paradoxus Bergman, Casey M. bioRxiv https://doi.org/10.1101/287078	posted_content	March 2018
Exploring the potential of Saccharomyces eubayanus as a parent for new interspecies hybrid strains in winemaking Magalhães, Frederico; Krogerus, Kristoffer; Castillo, Sandra FEMS Yeast Research, Vol. 17, Issue 5 https://doi.org/10.1093/femsyr/fox049	journal	July 2017
Interspecies Hybridisation and Genome Chimerisation in Saccharomyces: Combining of Gene Pools of Species and Its Biotechnological Perspectives Sipiczki, Matthias Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.03071	journal	December 2018
Evolutionary biology through the lens of budding yeast comparative genomics Marsit, Souhir; Leducq, Jean-Baptiste; Durand, Éléonore Nature Reviews Genetics, Vol. 18, Issue 10 https://doi.org/10.1038/nrg.2017.49	journal	July 2017
Evolution of a novel chimeric maltotriose transporter in Saccharomyces eubayanus from parent proteins unable to perform this function Baker, EmilyClare P.; Hittinger, Chris Todd PLOS Genetics, Vol. 15, Issue 4 https://doi.org/10.1371/journal.pgen.1007786	journal	April 2019
A Unique Saccharomyces cerevisiae × Saccharomyces uvarum Hybrid Isolated From Norwegian Farmhouse Beer: Characterization and Reconstruction Krogerus, Kristoffer; Preiss, Richard; Gibson, Brian Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02253	journal	September 2018
Reducing phenolic off-flavors through CRISPR-based gene editing of the FDC1 gene in Saccharomyces cerevisiae x Saccharomyces eubayanus hybrid lager beer yeasts Mertens, Stijn; Gallone, Brigida; Steensels, Jan PLOS ONE, Vol. 14, Issue 1 https://doi.org/10.1371/journal.pone.0209124	journal	January 2019
Social wasps promote social behavior in Saccharomyces spp. Blackwell, Meredith; Kurtzman, Cletus P. Proceedings of the National Academy of Sciences, Vol. 113, Issue 8 https://doi.org/10.1073/pnas.1600173113	journal	February 2016
Diacetyl control during brewery fermentation via adaptive laboratory engineering of the lager yeast Saccharomyces pastorianus Gibson, Brian; Vidgren, Virve; Peddinti, Gopal Journal of Industrial Microbiology & Biotechnology, Vol. 45, Issue 12 https://doi.org/10.1007/s10295-018-2087-4	journal	October 2018
Traditional Norwegian Kveik Are a Genetically Distinct Group of Domesticated Saccharomyces cerevisiae Brewing Yeasts Preiss, Richard; Tyrawa, Caroline; Krogerus, Kristoffer Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02137	journal	September 2018
Genome Analysis of the Yeast M14, an Industrial Brewing Yeast Strain Widely Used in China Liu, Chunfeng; Niu, Chengtuo; Zhao, Yun Journal of the American Society of Brewing Chemists, Vol. 76, Issue 4 https://doi.org/10.1080/03610470.2018.1496633	journal	October 2018
Independent domestication events in the blue‐cheese fungus Penicillium roqueforti Dumas, Emilie; Feurtey, Alice; Rodríguez de la Vega, Ricardo C. Molecular Ecology, Vol. 29, Issue 14 https://doi.org/10.1111/mec.15359	journal	February 2020
Traditional Norwegian Kveik Yeasts: Underexplored Domesticated Saccharomyces cerevisiae Yeasts Preiss, Richard; Tyrawa, Caroline; van der Merwe, George BioRxiv https://doi.org/10.1101/194969	posted_content	September 2017
Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus Peris, David; Langdon, Quinn K.; Moriarty, Ryan V. PLOS Genetics, Vol. 12, Issue 7 https://doi.org/10.1371/journal.pgen.1006155	journal	July 2016
Microbial acidification, alcoholization, and aroma production during spontaneous lambic beer production De Roos, Jonas; De Vuyst, Luc Journal of the Science of Food and Agriculture, Vol. 99, Issue 1 https://doi.org/10.1002/jsfa.9291	journal	August 2018

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59 BASIC BIOLOGICAL SCIENCES
Saccharomyces eubayanus
domestication
genome assembly
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Title: The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts

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