The Genome Sequence of Saccharomyces eubayanus and the Domestication of Lager-Brewing Yeasts

Molecular Biology and Evolution
EmilyClare P BakerChris Todd Hittinger

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 m...Continue Reading

References

Sep 1, 1991·Molecular Microbiology·R Needleman
Jan 1, 1987·Antonie van Leeuwenhoek·A V Martini, A Martini
Dec 1, 1966·Genetical Research·W G Hill, A Robertson
Sep 1, 1997·Nucleic Acids Research·S F AltschulD J Lipman
Jun 6, 2000·Nature·G FischerEdward J Louis
Aug 9, 2001·International Journal of Systematic and Evolutionary Microbiology·S CasaregolaClaude Gaillardin
Nov 26, 2002·Proceedings of the National Academy of Sciences of the United States of America·Maitreya J DunhamDavid Botstein
Apr 5, 2003·The Journal of Biological Chemistry·Elton T YoungTrey Ideker
May 1, 1964·Mutation Research·H J MULLER
Mar 23, 2004·Nucleic Acids Research·Robert C Edgar
Sep 24, 2004·Proceedings of the National Academy of Sciences of the United States of America·Chris Todd HittingerSean B Carroll
Dec 28, 2006·Cell·John F DoebleyBruce D Smith
Feb 17, 2007·FEMS Yeast Research·Christine Le JeuneIsabelle Masneuf-Pomarède
Apr 14, 2007·Science·Rhesus Macaque Genome Sequencing and Analysis ConsortiumAnn S Zwieg
Apr 25, 2007·Nucleic Acids Research·Karin LagesenDavid W Ussery
May 8, 2007·Molecular Biology and Evolution·Ziheng Yang
Aug 12, 2008·Molecular Biology and Evolution·Fernando CruzMatthew T Webster
Dec 17, 2008·Trends in Genetics : TIG·Antonis Rokas
Jan 30, 2009·FEMS Microbiology Letters·Amparo Querol, Ursula Bond
Feb 13, 2009·Nature·Gianni LitiEdward J Louis
Mar 6, 2009·DNA Research : an International Journal for Rapid Publication of Reports on Genes and Genomes·Yoshihiro NakaoToshihiko Ashikari
Mar 21, 2009·Proceedings of the National Academy of Sciences of the United States of America·Gregory I LangDavid Botstein
Oct 7, 2009·Proceedings of the National Academy of Sciences of the United States of America·Maite NovoSylvie Dequin
Feb 19, 2010·Nature·Chris Todd HittingerAntonis Rokas
Apr 21, 2010·FEMS Yeast Research·Virve VidgrenJohn Londesborough
May 18, 2010·Current Biology : CB·Chris A BrownKevin J Verstrepen
Jun 22, 2010·The Journal of Biological Chemistry·Marie-Ange TesteJean-Luc Parrou
Aug 30, 2011·Proceedings of the National Academy of Sciences of the United States of America·Diego LibkindJosé Paulo Sampaio
Nov 24, 2011·Nucleic Acids Research·J Michael CherryEdith D Wong
Apr 18, 2012·Journal of Computational Biology : a Journal of Computational Molecular Cell Biology·Anton BankevichPavel A Pevzner
Jul 26, 2012·Genome Research·Filipe J RibeiroDavid B Jaffe
Sep 19, 2012·BMC Bioinformatics·Estelle Proux-WéraKenneth H Wolfe
Feb 2, 2013·BMC Genomics·Gianni LitiConrad A Nieduszynski
Oct 18, 2013·Molecular Biology and Evolution·Koichiro TamuraSudhir Kumar
Oct 22, 2013·Trends in Ecology & Evolution·Hans Ellegren
Oct 31, 2013·Methods in Molecular Biology·Ari Löytynoja
Jan 1, 2014·G3 : Genes - Genomes - Genetics·Stacia R EngelJ Michael Cherry
Jan 16, 2014·Molecular Biology and Evolution·Anders BergströmGianni Liti
Mar 1, 2014·G3 : Genes - Genomes - Genetics·Andrea WaltherJürgen Wendland
May 23, 2014·Current Biology : CB·Jian BingFeng-Yan Bai
Jun 3, 2014·Nature Communications·Pedro AlmeidaJosé Paulo Sampaio
Aug 3, 2014·Eukaryotic Cell·Jürgen Wendland
Nov 11, 2014·Annual Review of Animal Biosciences·Guo-Dong WangYa-Ping Zhang
Mar 7, 2015·FEMS Yeast Research·Marit HeblyPascale Daran-Lapujade

Citations

Feb 18, 2016·Proceedings of the National Academy of Sciences of the United States of America·Meredith Blackwell, Cletus P Kurtzman
Nov 28, 2015·Molecular Biology and Evolution·Joseph Caspermeyer
Dec 10, 2015·Current Opinion in Genetics & Development·Chris Todd HittingerCletus P Kurtzman
Nov 12, 2015·Fungal Genetics and Biology : FG & B·William G AlexanderChris Todd Hittinger
Oct 16, 2015·FEMS Yeast Research·Pooja K StropeJohn H McCusker
May 18, 2016·Applied Microbiology and Biotechnology·Kristoffer KrogerusBrian R Gibson
Jul 13, 2016·FEMS Yeast Research·Barry van BergenArmando Jardim
Oct 28, 2016·Applied Microbiology and Biotechnology·Cristian Varela
Apr 4, 2017·Molecular Biology and Evolution·Caiti Smukowski HeilMaitreya J Dunham
Apr 27, 2017·Molecular Biology and Evolution·Jean-Baptiste LeducqChristian R Landry
Jun 6, 2017·FEMS Yeast Research·Brian R GibsonJosé Paulo Sampaio
Jul 18, 2017·Nature Reviews. Genetics·Souhir MarsitChristian R Landry
Apr 13, 2018·Nature·Jackson PeterJoseph Schacherer
Dec 3, 2017·Applied and Environmental Microbiology·Kristoffer KrogerusBrian R Gibson
Oct 11, 2017·DNA Research : an International Journal for Rapid Publication of Reports on Genes and Genomes·Pavol SuloTomáš Szemes
Aug 9, 2017·Yeast·Chandre Monerawela, Ursula Bond
Mar 28, 2017·Applied and Environmental Microbiology·Arthur R Gorter de VriesJean-Marc Daran
Sep 27, 2015·Applied and Environmental Microbiology·Stijn MertensKevin J Verstrepen
Sep 25, 2018·Journal of the Science of Food and Agriculture·Jonas De Roos, Luc De Vuyst
Sep 6, 2018·Molecular Biology and Evolution·Quinn K LangdonChris Todd Hittinger
Aug 15, 2018·Environmental Microbiology·Juan Ignacio EizaguirreDiego Libkind
Aug 17, 2017·PloS One·Jiangxing RuanHuifeng Jiang
Sep 26, 2019·FEMS Yeast Research·Arthur R Gorter de VriesJean-Marc Daran
Jan 22, 2020·Molecular Ecology·Emilie DumasTatiana Giraud
Jan 24, 2020·Yeast·Thomas PerliJean-Marc Daran
Feb 5, 2020·FEMS Yeast Research·Diego LibkindChris Todd Hittinger
Jan 18, 2020·Annual Review of Food Science and Technology·Brian R GibsonVirve Vidgren
Sep 17, 2019·PLoS Genetics·Caiti Smukowski HeilMaitreya J Dunham
Feb 26, 2020·Microbial Biotechnology·Wladimir MardonesFrancisco A Cubillos
Nov 26, 2016·Applied Microbiology and Biotechnology·Kristoffer KrogerusBrian R Gibson
May 17, 2017·Doklady Biological Sciences : Proceedings of the Academy of Sciences of the USSR, Biological Sciences Sections·Gennadi I Naumov
Apr 20, 2019·Frontiers in Genetics·Arthur R Gorter de VriesJean-Marc Daran
Feb 8, 2019·Science Advances·EmilyClare P BakerChris Todd Hittinger
Apr 1, 2017·Biotechnology for Biofuels·David PerisChris Todd Hittinger
Oct 12, 2018·Journal of Industrial Microbiology & Biotechnology·Brian R GibsonKristoffer Krogerus
Oct 23, 2019·Nature Ecology & Evolution·Quinn K LangdonChris Todd Hittinger
Jun 9, 2017·Genetics·Bernard A Dujon, Edward J Louis
Mar 21, 2020·FEMS Yeast Research·Haya Alsammar, Daniela Delneri
Oct 23, 2019·Nature Ecology & Evolution·Brigida GalloneKevin J Verstrepen
May 1, 2020·Nature Communications·David PerisChris Todd Hittinger
Mar 7, 2021·Revista Argentina de microbiología·Julieta Amalia BuriniDiego Libkind
Nov 6, 2017·Current Opinion in Biotechnology·Chris Todd HittingerDavid S Ryder
Mar 27, 2021·Nature Reviews. Microbiology·Jan SteenselsKevin J Verstrepen
Feb 13, 2017·Molecular Phylogenetics and Evolution·David PerisEladio Barrio

Datasets Mentioned

BETA
AZCJ01000000

Methods Mentioned

BETA
Illumina sequencing
454 sequencing
Chip
PCR

Related Concepts

Trending Feeds

COVID-19

Coronaviruses encompass a large family of viruses that cause the common cold as well as more serious diseases, such as the ongoing outbreak of coronavirus disease 2019 (COVID-19; formally known as 2019-nCoV). Coronaviruses can spread from animals to humans; symptoms include fever, cough, shortness of breath, and breathing difficulties; in more severe cases, infection can lead to death. This feed covers recent research on COVID-19.

STING Receptor Agonists

Stimulator of IFN genes (STING) are a group of transmembrane proteins that are involved in the induction of type I interferon that is important in the innate immune response. The stimulation of STING has been an active area of research in the treatment of cancer and infectious diseases. Here is the latest research on STING receptor agonists.

Chronic Fatigue Syndrome

Chronic fatigue syndrome is a disease characterized by unexplained disabling fatigue; the pathology of which is incompletely understood. Discover the latest research on chronic fatigue syndrome here.

Spatio-Temporal Regulation of DNA Repair

DNA repair is a complex process regulated by several different classes of enzymes, including ligases, endonucleases, and polymerases. This feed focuses on the spatial and temporal regulation that accompanies DNA damage signaling and repair enzymes and processes.

Glut1 Deficiency

Glut1 deficiency, an autosomal dominant, genetic metabolic disorder associated with a deficiency of GLUT1, the protein that transports glucose across the blood brain barrier, is characterized by mental and motor developmental delays and infantile seizures. Follow the latest research on Glut1 deficiency with this feed.

Hereditary Sensory Autonomic Neuropathy

Hereditary Sensory Autonomic Neuropathies are a group of inherited neurodegenerative disorders characterized clinically by loss of sensation and autonomic dysfunction. Here is the latest research on these neuropathies.

Separation Anxiety

Separation anxiety is a type of anxiety disorder that involves excessive distress and anxiety with separation. This may include separation from places or people to which they have a strong emotional connection with. It often affects children more than adults. Here is the latest research on separation anxiety.

Neural Activity: Imaging

Imaging of neural activity in vivo has developed rapidly recently with the advancement of fluorescence microscopy, including new applications using miniaturized microscopes (miniscopes). This feed follows the progress in this growing field.

Applications of Molecular Barcoding

The concept of molecular barcoding is that each original DNA or RNA molecule is attached to a unique sequence barcode. Sequence reads having different barcodes represent different original molecules, while sequence reads having the same barcode are results of PCR duplication from one original molecule. Discover the latest research on molecular barcoding here.