Abstract
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Social wasps promote social behavior in Saccharomyces spp.
Production of fermented beverages and bread making represents a multibillion dollar worldwide industry (1) with its origins linked to the Middle East nearly 10,000 y ago (2). Despite this long history, the cause of fermentation was not discovered until the pioneering work beginning in the middle of the 19th century when Louis Pasteur demonstrated that fermentation is yeast-mediated. The long-term questions have been which yeast and where did it come from? The name selected for the wine fermentation yeast was Saccharomyces cerevisiae, but based on phenotype, it appeared that there were related fermentative species. Early studies from DNA reassociation (3) and from gene sequencing (4) verified this premise and demonstrated that additional species of Saccharomyces were involved in fermentation, such as Saccharomyces uvarum for lager beers. DNA sequence evidence supports the use of S. cerevisiae in wine making in Egypt 5,000 y ago (5). Unresolved has been an understanding of the natural habitat of Saccharomyces species. It has been proposed that S. cerevisiae evolved into a domesticated species found only in wineries and associated vineyards, but the discovery of Saccharomyces species on tree bark has raised the intriguing possibility that S. cerevisiae and related species have a natural habitat associated with forest trees (6). More recent genome sequencing revealed a new species, Saccharomyces eubayanus and, further, that it shares homologous genes with S. cerevisiae, Saccharomyces paradoxus, and S. uvarum (7). This surprising discovery again raised the question of habitat for Saccharomyces and where might it be possible for the species to interact and form hybrids. The study by Stefanini et al. (8) in PNAS discovered Saccharomyces species to be common in the intestinal tract of social wasps (Fig. 1), such as Polistes dominula, which provide a “nest” for overwintering and outcrossing for S. cerevisiae and S. paradoxus.
In the search for the natural habitat of Saccharomyces spp. researchers have used media enriched with high glucose or even alcohol to isolate the yeasts from oak (Quercus spp.) (9, 10) and other members of the Fagaceae, oak-associated soils, and associated insects (e.g., 11, 12). In several of the studies, multiple species of Saccharomyces were sympatric, but hybrids were seldom found because of ecological isolation by factors such as growth temperature (e.g., S. cerevisiae and S. paradoxus) (10, 13). Based on these reports, it is clear that the wasps do more than provide a hibernaculum for yeasts to overwinter. The discovery of hybrids of S. cerevisiae and S. paradoxus within the intestine of Polistes is noteworthy, but the experimental finding that S. paradoxus strains did not survive gut passage except when rescued by hybridization is remarkable (8). In addition, gut passage promotes conditions favorable to outcrossing, explaining high rates of strain diversity in S. cerevisiae.
Insects, including wasps, have long been seen to damage grapes, and damaged grapes have much higher frequencies of S. cerevisiae, thus supporting the view that the natural habitat of the yeast is in an undiscovered habitat and alerting yeast specialists to look elsewhere for wild populations (14). About 300 taxa of Polistes are recognized worldwide, and about 20 are present in the United States. P. dominula, used by Stefanini et al. (8), was introduced to the United States from Europe in the late 1970s and has spread throughout most of the country to the West Coast, displacing several of native species along the way (15). Many social wasps, including P. dominula, construct nests of paper made of chewed wood fibers and bark, a potential source of wild yeasts. A correlation between the timing of S. cerevisae population buildup until midsummer could be correlated with the life cycle of a number of Polistes species. The use of wine and alcohol baits to attract pest wasps (16) suggests that baits could be used to conduct rapid broad surveys to test the universality of the S. cerevisiae–wasp association. Such surveys should be timed to the life cycle of the wasps and other suspect insects, with consideration of the known geographical and ecological limits of the organisms (17). In a commentary on a paper enumerating large numbers of potential undescribed yeasts from the gut of beetles (18), Boekhout (19) reported that insect sources accounted for only 6% of the isolates in the Centraalbureau voor Schmmelcultures (CBS) yeast collection, and the insect gut was a “highly promising route” to the discovery of hidden microbial diversity. It now is obvious not only that new species may exist in the gut of insects but that known yeasts rare in nature may regularly occupy insect habitats (Figs. 2 and and3),3), where they prosper.
Acknowledgments
The mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture (USDA). The USDA is an equal opportunity provider and employer. We thank Dr. Julia L. Kerrigan for providing the original high resolution image used in Fig. 2.
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Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences
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