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Edited by Nancy A. Moran, Yale University, West Haven, CT, and approved July 5, 2012 (received for review May 18, 2012)
Abstract
Saccharomyces cerevisiae is one of the most important model organisms and has been a valuable asset to human civilization. However, despite its extensive use in the last 9,000 y, the existence of a seasonal cycle outside human-made environments has not yet been described. We demonstrate the role of social wasps as vector and natural reservoir of S. cerevisiae during all seasons. We provide experimental evidence that queens of social wasps overwintering as adults (Vespa crabro and Polistes spp.) can harbor yeast cells from autumn to spring and transmit them to their progeny. This result is mirrored by field surveys of the genetic variability of natural strains of yeast. Microsatellites and sequences of a selected set of loci able to recapitulate the yeast strain’s evolutionary history were used to compare 17 environmental wasp isolates with a collection of strains from grapes from the same region and more than 230 strains representing worldwide yeast variation. The wasp isolates fall into subclusters representing the overall ecological and industrial yeast diversity of their geographic origin. Our findings indicate that wasps are a key environmental niche for the evolution of natural S. cerevisiae populations, the dispersion of yeast cells in the environment, and the maintenance of their diversity. The close relatedness of several wasp isolates with grape and wine isolates reflects the crucial role of human activities on yeast population structure, through clonal expansion and selection of specific strains during the biotransformation of fermented foods, followed by dispersal mediated by insects and other animals.
Footnotes
↵1I.S. and L.D. contributed equally to this work.
- ↵2To whom correspondence should be addressed. E-mail: duccio.cavalieri{at}fmach.it.
Author contributions: M.P., S.T., and D.C. designed research; I.S., L.D., J.-L.L., A.C., M.D.P., C.D.F., and D.C. performed research; I.S., L.D., J.-L.L., A.C., M.D.P., C.D.F., R.V., P.C., M.P., S.T., and D.C. analyzed data; and I.S., L.D., and D.C. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession no. JQ946429–JQ946518).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1208362109/-/DCSupplemental.
Freely available online through the PNAS open access option.
- Irene Stefaninia,1,
- Leonardo Dapportob,c,1,
- Jean-Luc Legrasd,e,f,
- Antonio Calabrettaa,b,
- Monica Di Paolag,
- Carlotta De Filippoh,
- Roberto Violah,
- Paolo Caprettic,
- Mario Polsinellib,
- Stefano Turillazzib,i, and
- Duccio Cavalieria,h,2
- aDipartimento di Farmacologia, University of Florence, 50139, Florence, Italy;
- bDipartimento di Biologia Evoluzionistica, University of Florence, 50125, Florence, Italy;
- cDipartimento di Biotecnologie Agrarie, University of Florence, 50144, Florence, Italy;
- dINRA (Institut National de la Recherche Agronomique), UMR1083 (Unité Mixte de Recherche Sciences pour l'Oenologie), F-34060 Montpellier, France;
- eMontpellier SupAgro, UMR1083 (Unité Mixte de Recherche Sciences pour l'Oenologie), F-34060 Montpellier, France;
- fUniversité Montpellier I, UMR1083 (Unité Mixte de Recherche Sciences pour l'Oenologie), F-34060 Montpellier, France;
- gDipartimento di Scienze per la Salute della Donna e del Bambino, Ospedale Pediatrico Meyer, University of Florence, 50139, Florence, Italy;
- hCentre for Research and Innovation, Fondazione Edmund Mach, Via E. Mach 1, 38010 San Michele all'Adige, Trento, Italy; and
- iCentro di Servizi di Spettromeria di Massa, University of Florence, Florence, Italy
Edited by Nancy A. Moran, Yale University, West Haven, CT, and approved July 5, 2012 (received for review May 18, 2012)
Abstract
Saccharomyces cerevisiae is one of the most important model organisms and has been a valuable asset to human civilization. However, despite its extensive use in the last 9,000 y, the existence of a seasonal cycle outside human-made environments has not yet been described. We demonstrate the role of social wasps as vector and natural reservoir of S. cerevisiae during all seasons. We provide experimental evidence that queens of social wasps overwintering as adults (Vespa crabro and Polistes spp.) can harbor yeast cells from autumn to spring and transmit them to their progeny. This result is mirrored by field surveys of the genetic variability of natural strains of yeast. Microsatellites and sequences of a selected set of loci able to recapitulate the yeast strain’s evolutionary history were used to compare 17 environmental wasp isolates with a collection of strains from grapes from the same region and more than 230 strains representing worldwide yeast variation. The wasp isolates fall into subclusters representing the overall ecological and industrial yeast diversity of their geographic origin. Our findings indicate that wasps are a key environmental niche for the evolution of natural S. cerevisiae populations, the dispersion of yeast cells in the environment, and the maintenance of their diversity. The close relatedness of several wasp isolates with grape and wine isolates reflects the crucial role of human activities on yeast population structure, through clonal expansion and selection of specific strains during the biotransformation of fermented foods, followed by dispersal mediated by insects and other animals.
- evolutionary biology
- genomics
Footnotes
↵1I.S. and L.D. contributed equally to this work.
- ↵2To whom correspondence should be addressed. E-mail: duccio.cavalieri{at}fmach.it.
Author contributions: M.P., S.T., and D.C. designed research; I.S., L.D., J.-L.L., A.C., M.D.P., C.D.F., and D.C. performed research; I.S., L.D., J.-L.L., A.C., M.D.P., C.D.F., R.V., P.C., M.P., S.T., and D.C. analyzed data; and I.S., L.D., and D.C. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession no. JQ946429–JQ946518).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1208362109/-/DCSupplemental.
Freely available online through the PNAS open access option.
Saccharomyces cerevisiae and social wasps
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