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Interspecific hybridization facilitates niche adaptation in beer yeast

Nature Ecology & Evolution volume 3, pages 1562–1575 (2019)Cite this article

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Abstract

Hybridization between species often leads to non-viable or infertile offspring, yet examples of evolutionarily successful interspecific hybrids have been reported in all kingdoms of life. However, many questions on the ecological circumstances and evolutionary aftermath of interspecific hybridization remain unanswered. In this study, we sequenced and phenotyped a large set of interspecific yeast hybrids isolated from brewing environments to uncover the influence of interspecific hybridization in yeast adaptation and domestication. Our analyses demonstrate that several hybrids between Saccharomyces species originated and diversified in industrial environments by combining key traits of each parental species. Furthermore, posthybridization evolution within each hybrid lineage reflects subspecialization and adaptation to specific beer styles, a process that was accompanied by extensive chimerization between subgenomes. Our results reveal how interspecific hybridization provides an important evolutionary route that allows swift adaptation to novel environments.

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Fig. 1: Tanglegram depicting the relationships between Saccharomyces pure species and interspecific hybrids.
Fig. 2: Genome structure of Saccharomyces interspecific hybrids.
Fig. 3: Distribution of chimeric breakpoints across interspecific hybrids.
Fig. 4: Trait variation and niche adaptation of interspecific hybrids.
Fig. 5: The genetic basis of loss of 4-VG production in S.cer × S.eub hybrids.
Fig. 6: Time-calibrated phylogeny of S.cer Beer 1 clade.

Data availability

All raw sequencing reads generated in this study have been deposited to the NCBI Short Read Archive (BioProject accession: PRJNA516557).

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Acknowledgements

We thank all K.J.V. and S.Maere laboratory members for their help and suggestions. We thank AB InBev, White Labs Inc. and R. S. Wagner (Central Washington University) for isolating and sharing various hybrid yeasts from the beer environment. We thank M. Zarnkow (Research Center Weihenstephan for Brewing and Food Quality) for sharing historical facts on lager brewing. B.G. acknowledges funding from the VIB International PhD Program in Life Sciences. J.S. acknowledges funding from Research Foundation-Flanders (FWO) (grant no. 12W3918N). Research in the laboratory of K.J.V. is supported by KU Leuven Program Financing, European Research Council Consolidator Grant (no. CoG682009), Human Frontier Science program grant (no. RGP0050/2013), VIB, FWO (grant no. G.0C59.14N) and Vlaams Agentschap Innoveren en Ondernemen (grant no. HBC.2018.0097). Research in the laboratory of S.Maere is supported by VIB, Ghent University and FWO (grant no. G018915N).

Author information

Author notes

  1. These authors contributed equally: Brigida Gallone, Jan Steensels.

  2. Deceased: Franz Meußdoerffer.

Authors and Affiliations

  1. VIB–KU Leuven Center for Microbiology, Leuven, Belgium

    Brigida Gallone, Jan Steensels, Stijn Mertens, Maria C. Dzialo, Jonathan L. Gordon, Ruben Wauters, Florian A. Theßeling, Francesca Bellinazzo, Veerle Saels, Beatriz Herrera-Malaver & Kevin J. Verstrepen

  2. CMPG Laboratory of Genetics and Genomics, Department M2S, KU Leuven, Leuven, Belgium

    Brigida Gallone, Jan Steensels, Stijn Mertens, Maria C. Dzialo, Jonathan L. Gordon, Ruben Wauters, Florian A. Theßeling, Francesca Bellinazzo, Veerle Saels, Beatriz Herrera-Malaver & Kevin J. Verstrepen

  3. Leuven Institute for Beer Research, Leuven, Belgium

    Brigida Gallone, Jan Steensels, Stijn Mertens, Maria C. Dzialo, Jonathan L. Gordon, Ruben Wauters, Florian A. Theßeling, Francesca Bellinazzo, Veerle Saels, Beatriz Herrera-Malaver & Kevin J. Verstrepen

  4. Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium

    Brigida Gallone & Steven Maere

  5. VIB Center for Plant Systems Biology, Ghent, Belgium

    Brigida Gallone & Steven Maere

  6. White Labs Inc., San Diego, CA, USA

    Troels Prahl & Christopher White

  7. Research Center Weihenstephan for Brewing and Food Quality, TU München, Freising, Germany

    Mathias Hutzler & Franz Meußdoerffer

  8. ABInBev SA/NV, Leuven, Belgium

    Philippe Malcorps, Ben Souffriau & Luk Daenen

  9. Department of Microbiology, Immunology and Transplantation, Rega Institute, KU Leuven, Leuven, Belgium

    Guy Baele

Authors
  1. Brigida Gallone
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  2. Jan Steensels
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  3. Stijn Mertens
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  4. Maria C. Dzialo
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  5. Jonathan L. Gordon
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  6. Ruben Wauters
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  7. Florian A. Theßeling
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  8. Francesca Bellinazzo
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  9. Veerle Saels
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  10. Beatriz Herrera-Malaver
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  11. Troels Prahl
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  12. Christopher White
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  13. Mathias Hutzler
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  14. Franz Meußdoerffer
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  15. Philippe Malcorps
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  16. Ben Souffriau
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  17. Luk Daenen
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  18. Guy Baele
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  19. Steven Maere
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  20. Kevin J. Verstrepen
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Contributions

B.G., J.S., S.Maere and K.J.V. conceived the project. B.G. and J.S. performed the data collection. B.G., J.S. and G.B. carried out the formal analysis. B.G., J.S., S.Mertens, J.L.G., R.W., F.A.T., F.B., V.S., B.H.-M. and G.B. carried out the investigations. B.G. and J.S. performed data visualization. M.H., F.M., P.M., B.S., L.D., T.P., C.W. and K.J.V. provided resources. B.G., J.S., M.C.D., S.Maere and K.J.V. wrote the paper. S.Maere and K.J.V. supervised the project.

Corresponding authors

Correspondence to Steven Maere or Kevin J. Verstrepen.

Ethics declarations

Competing interests

AB InBev partially funded the experiments performed in this study. AB InBev had no role in conceptualization, design, data collection, analysis, decision to publish or preparation of the manuscript. B.S., P.M. and L.D. are employed by AB InBev.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–5, Tables 1–3, Note 1 and Dataset 1.

Reporting Summary

Supplementary Table 1

List of strains included in this study.

Supplementary Table 2

Chimeric breakpoints identified in Saccharomyces interspecific hybrids.

Supplementary Table 3

Phenotypic variation of Saccharomyces interspecific hybrids and Saccharomyces pure species.

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Gallone, B., Steensels, J., Mertens, S. et al. Interspecific hybridization facilitates niche adaptation in beer yeast. Nat Ecol Evol 3, 1562–1575 (2019). https://doi.org/10.1038/s41559-019-0997-9

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  • DOI: https://doi.org/10.1038/s41559-019-0997-9

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