Distinct Domestication Trajectories in Top-Fermenting Beer Yeasts and Wine Yeasts

Margarida Gonçalves, Ana Pontes, Pedro Almeida, Raquel Barbosa, Marta Serra, Diego Libkind, Mathias Hutzler, Paula Gonçalves, José Paulo Sampaio

Research output: Contribution to journalArticle

56 Citations (Scopus)

Abstract

Beer is one of the oldest alcoholic beverages and is produced by the fermentation of sugars derived from starches present in cereal grains. Contrary to lager beers, made by bottom-fermenting strains of Saccharomyces pastorianus, a hybrid yeast, ale beers are closer to the ancient beer type and are fermented by S. cerevisiae, a top-fermenting yeast. Here, we use population genomics to investigate (1) the closest relatives of top-fermenting beer yeasts; (2) whether top-fermenting yeasts represent an independent domestication event separate from those already described; (3) whether single or multiple beer yeast domestication events can be inferred; and (4) whether top-fermenting yeasts represent non-recombinant or recombinant lineages. Our results revealed that top-fermenting beer yeasts are polyphyletic, with a main clade composed of at least three subgroups, dominantly represented by the German, British, and wheat beer strains. Other beer strains were phylogenetically close to sake, wine, or bread yeasts. We detected genetic signatures of beer yeast domestication by investigating genes previously linked to brewing and using genome-wide scans. We propose that the emergence of the main clade of beer yeasts is related with a domestication event distinct from the previously known cases of wine and sake yeast domestication. The nucleotide diversity of the main beer clade more than doubled that of wine yeasts, which might be a consequence of fundamental differences in the modes of beer and wine yeast domestication. The higher diversity of beer strains could be due to the more intense and different selection regimes associated to brewing.

Original languageEnglish
Pages (from-to)2750-2761
Number of pages12
JournalCurrent Biology
Volume26
Issue number20
DOIs
Publication statusPublished - 24 Oct 2016

Fingerprint

wine yeasts
Beer
Wine
domestication
beers
Yeast
trajectories
Yeasts
Trajectories
yeasts
Brewing
sake
brewing
Domestication
Genes
Metagenomics
Alcoholic Beverages
Saccharomyces
alcoholic beverages
Bread

Keywords

  • beer
  • comparative genomics
  • domestication signatures
  • microbe domestication
  • phenolic off flavor (POF)
  • Saccharomyces cerevisiae
  • top-fermenting ale beer
  • wheat beer
  • yeast population genomics

Cite this

Gonçalves, M., Pontes, A., Almeida, P., Barbosa, R., Serra, M., Libkind, D., ... Sampaio, J. P. (2016). Distinct Domestication Trajectories in Top-Fermenting Beer Yeasts and Wine Yeasts. Current Biology, 26(20), 2750-2761. https://doi.org/10.1016/j.cub.2016.08.040
Gonçalves, Margarida ; Pontes, Ana ; Almeida, Pedro ; Barbosa, Raquel ; Serra, Marta ; Libkind, Diego ; Hutzler, Mathias ; Gonçalves, Paula ; Sampaio, José Paulo. / Distinct Domestication Trajectories in Top-Fermenting Beer Yeasts and Wine Yeasts. In: Current Biology. 2016 ; Vol. 26, No. 20. pp. 2750-2761.
@article{c295a214146a482e8d62e991b8cfe767,
title = "Distinct Domestication Trajectories in Top-Fermenting Beer Yeasts and Wine Yeasts",
abstract = "Beer is one of the oldest alcoholic beverages and is produced by the fermentation of sugars derived from starches present in cereal grains. Contrary to lager beers, made by bottom-fermenting strains of Saccharomyces pastorianus, a hybrid yeast, ale beers are closer to the ancient beer type and are fermented by S. cerevisiae, a top-fermenting yeast. Here, we use population genomics to investigate (1) the closest relatives of top-fermenting beer yeasts; (2) whether top-fermenting yeasts represent an independent domestication event separate from those already described; (3) whether single or multiple beer yeast domestication events can be inferred; and (4) whether top-fermenting yeasts represent non-recombinant or recombinant lineages. Our results revealed that top-fermenting beer yeasts are polyphyletic, with a main clade composed of at least three subgroups, dominantly represented by the German, British, and wheat beer strains. Other beer strains were phylogenetically close to sake, wine, or bread yeasts. We detected genetic signatures of beer yeast domestication by investigating genes previously linked to brewing and using genome-wide scans. We propose that the emergence of the main clade of beer yeasts is related with a domestication event distinct from the previously known cases of wine and sake yeast domestication. The nucleotide diversity of the main beer clade more than doubled that of wine yeasts, which might be a consequence of fundamental differences in the modes of beer and wine yeast domestication. The higher diversity of beer strains could be due to the more intense and different selection regimes associated to brewing.",
keywords = "beer , comparative genomics , domestication signatures , microbe domestication , phenolic off flavor (POF) , Saccharomyces cerevisiae , top-fermenting ale beer , wheat beer , yeast population genomics",
author = "Margarida Gon{\cc}alves and Ana Pontes and Pedro Almeida and Raquel Barbosa and Marta Serra and Diego Libkind and Mathias Hutzler and Paula Gon{\cc}alves and Sampaio, {Jos{\'e} Paulo}",
note = "Sem PDF. info:eu-repo/grantAgreement/FCT/3599-PPCDT/118618/PT# info:eu-repo/grantAgreement/FCT/3599-PPCDT/118590/PT# info:eu-repo/grantAgreement/FCT/5876/147258/PT# We thank Chris Hittinger for critical comments on the manuscript. This work was supported by FCT Portugal grants PTDC/BIA-EVF/118618/2010 (J.P.S., M.G., and P.G.), PTDC/AGR-ALI/118590/2010 (J.P.S., P.A., P.G., and R.B.), UID/Multi/04378/2013 (J.P.S. and P.G.), and SFRH/BD/77390/2011 (P.A.). D.L. was supported by grant B171 (Universidad Nacional del Comahue) and by grants PICT2014-2542 and PICT2014-3677 (ANPCyT, Argentina).",
year = "2016",
month = "10",
day = "24",
doi = "10.1016/j.cub.2016.08.040",
language = "English",
volume = "26",
pages = "2750--2761",
journal = "Current Biology",
issn = "0960-9822",
publisher = "Elsevier Science B.V., Amsterdam.",
number = "20",

}

Gonçalves, M, Pontes, A, Almeida, P, Barbosa, R, Serra, M, Libkind, D, Hutzler, M, Gonçalves, P & Sampaio, JP 2016, 'Distinct Domestication Trajectories in Top-Fermenting Beer Yeasts and Wine Yeasts', Current Biology, vol. 26, no. 20, pp. 2750-2761. https://doi.org/10.1016/j.cub.2016.08.040

Distinct Domestication Trajectories in Top-Fermenting Beer Yeasts and Wine Yeasts. / Gonçalves, Margarida; Pontes, Ana; Almeida, Pedro; Barbosa, Raquel; Serra, Marta; Libkind, Diego; Hutzler, Mathias; Gonçalves, Paula; Sampaio, José Paulo.

In: Current Biology, Vol. 26, No. 20, 24.10.2016, p. 2750-2761.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Distinct Domestication Trajectories in Top-Fermenting Beer Yeasts and Wine Yeasts

AU - Gonçalves, Margarida

AU - Pontes, Ana

AU - Almeida, Pedro

AU - Barbosa, Raquel

AU - Serra, Marta

AU - Libkind, Diego

AU - Hutzler, Mathias

AU - Gonçalves, Paula

AU - Sampaio, José Paulo

N1 - Sem PDF. info:eu-repo/grantAgreement/FCT/3599-PPCDT/118618/PT# info:eu-repo/grantAgreement/FCT/3599-PPCDT/118590/PT# info:eu-repo/grantAgreement/FCT/5876/147258/PT# We thank Chris Hittinger for critical comments on the manuscript. This work was supported by FCT Portugal grants PTDC/BIA-EVF/118618/2010 (J.P.S., M.G., and P.G.), PTDC/AGR-ALI/118590/2010 (J.P.S., P.A., P.G., and R.B.), UID/Multi/04378/2013 (J.P.S. and P.G.), and SFRH/BD/77390/2011 (P.A.). D.L. was supported by grant B171 (Universidad Nacional del Comahue) and by grants PICT2014-2542 and PICT2014-3677 (ANPCyT, Argentina).

PY - 2016/10/24

Y1 - 2016/10/24

N2 - Beer is one of the oldest alcoholic beverages and is produced by the fermentation of sugars derived from starches present in cereal grains. Contrary to lager beers, made by bottom-fermenting strains of Saccharomyces pastorianus, a hybrid yeast, ale beers are closer to the ancient beer type and are fermented by S. cerevisiae, a top-fermenting yeast. Here, we use population genomics to investigate (1) the closest relatives of top-fermenting beer yeasts; (2) whether top-fermenting yeasts represent an independent domestication event separate from those already described; (3) whether single or multiple beer yeast domestication events can be inferred; and (4) whether top-fermenting yeasts represent non-recombinant or recombinant lineages. Our results revealed that top-fermenting beer yeasts are polyphyletic, with a main clade composed of at least three subgroups, dominantly represented by the German, British, and wheat beer strains. Other beer strains were phylogenetically close to sake, wine, or bread yeasts. We detected genetic signatures of beer yeast domestication by investigating genes previously linked to brewing and using genome-wide scans. We propose that the emergence of the main clade of beer yeasts is related with a domestication event distinct from the previously known cases of wine and sake yeast domestication. The nucleotide diversity of the main beer clade more than doubled that of wine yeasts, which might be a consequence of fundamental differences in the modes of beer and wine yeast domestication. The higher diversity of beer strains could be due to the more intense and different selection regimes associated to brewing.

AB - Beer is one of the oldest alcoholic beverages and is produced by the fermentation of sugars derived from starches present in cereal grains. Contrary to lager beers, made by bottom-fermenting strains of Saccharomyces pastorianus, a hybrid yeast, ale beers are closer to the ancient beer type and are fermented by S. cerevisiae, a top-fermenting yeast. Here, we use population genomics to investigate (1) the closest relatives of top-fermenting beer yeasts; (2) whether top-fermenting yeasts represent an independent domestication event separate from those already described; (3) whether single or multiple beer yeast domestication events can be inferred; and (4) whether top-fermenting yeasts represent non-recombinant or recombinant lineages. Our results revealed that top-fermenting beer yeasts are polyphyletic, with a main clade composed of at least three subgroups, dominantly represented by the German, British, and wheat beer strains. Other beer strains were phylogenetically close to sake, wine, or bread yeasts. We detected genetic signatures of beer yeast domestication by investigating genes previously linked to brewing and using genome-wide scans. We propose that the emergence of the main clade of beer yeasts is related with a domestication event distinct from the previously known cases of wine and sake yeast domestication. The nucleotide diversity of the main beer clade more than doubled that of wine yeasts, which might be a consequence of fundamental differences in the modes of beer and wine yeast domestication. The higher diversity of beer strains could be due to the more intense and different selection regimes associated to brewing.

KW - beer

KW - comparative genomics

KW - domestication signatures

KW - microbe domestication

KW - phenolic off flavor (POF)

KW - Saccharomyces cerevisiae

KW - top-fermenting ale beer

KW - wheat beer

KW - yeast population genomics

U2 - 10.1016/j.cub.2016.08.040

DO - 10.1016/j.cub.2016.08.040

M3 - Article

VL - 26

SP - 2750

EP - 2761

JO - Current Biology

JF - Current Biology

SN - 0960-9822

IS - 20

ER -

Gonçalves M, Pontes A, Almeida P, Barbosa R, Serra M, Libkind D et al. Distinct Domestication Trajectories in Top-Fermenting Beer Yeasts and Wine Yeasts. Current Biology. 2016 Oct 24;26(20):2750-2761. https://doi.org/10.1016/j.cub.2016.08.040