Better explicating the strengths and shortcomings of these models will help refine projections and improve transparency in the years ahead.
Image credit: Witsawat.S.
Edited by Jeffrey P. Townsend, Yale University, New Haven, CT, and accepted by the Editorial Board December 9, 2015 (received for review August 18, 2015)
Significance
Despite the widespread interest on Saccharomyces cerevisiae, its wild lifestyle is far from being completely understood, with one of the most resounding examples being its sexual attitude. We show that the intestine of social wasps favors the mating of Saccharomyces strains by providing a succession of environmental conditions prompting sporulation and germination. We also demonstrate that the insect intestine favors hybridization of S. cerevisiae and Saccharomyces paradoxus. Although S. paradoxus survives in wild environments and rarely mates with S. cerevisiae, we discover that two European S. paradoxus strains cannot survive the wasp's intestinal environment but can be rescued through interspecific hybridization with S. cerevisiae. These findings are introducing insects as environmental alcoves in which yeast cells can meet and mate.
Abstract
The reproductive ecology of Saccharomyces cerevisiae is still largely unknown. Recent evidence of interspecific hybridization, high levels of strain heterozygosity, and prion transmission suggest that outbreeding occurs frequently in yeasts. Nevertheless, the place where yeasts mate and recombine in the wild has not been identified. We found that the intestine of social wasps hosts highly outbred S. cerevisiae strains as well as a rare S. cerevisiae×S. paradoxus hybrid. We show that the intestine of Polistes dominula social wasps favors the mating of S. cerevisiae strains among themselves and with S. paradoxus cells by providing a succession of environmental conditions prompting cell sporulation and spores germination. In addition, we prove that heterospecific mating is the only option for European S. paradoxus strains to survive in the gut. Taken together, these findings unveil the best hidden secret of yeast ecology, introducing the insect gut as an environmental alcove in which crosses occur, maintaining and generating the diversity of the ascomycetes.
Footnotes
↵1I.S. and L.D. contributed equally to this work.
- ↵2To whom correspondence should be addressed. Email: duccio.cavalieri{at}unifi.it.
Author contributions: I.S., L.D., M.P., S.T., and D.C. designed research; I.S. and L.D. performed research; I.S., L.D., L.B., and D.C. analyzed data; and I.S., L.D., L.B., M.P., S.T., and D.C. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. J.P.T. is a guest editor invited by the Editorial Board.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1516453113/-/DCSupplemental.
Freely available online through the PNAS open access option.
Saccharomyces mating occurs in wasps' intestine
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