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Social Wasps Promote Social Behavior in Saccharomyces Spp

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Social Wasps Promote Social Behavior in Saccharomyces Spp COMMENTARY Social wasps promote social behavior in Saccharomyces spp. COMMENTARY Meredith Blackwella,b,1 and Cletus P. Kurtzmanc Production of fermented beverages and bread mak- ing 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 pioneer- ing 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 Saccha- romyces cerevisiae, but based on phenotype, it appeared that there were related fermentative spe- cies. Early studies from DNA reassociation (3) and from gene sequencing (4) verified this premise and demon- strated that additional species of Saccharomyces were involved in fermentation, such as Saccharomyces uva- rum for lager beers. DNA sequence evidence sup- ports the use of S. cerevisiae in wine making in Egypt 5,000 y ago (5). Unresolved has been an under- standing of the natural habitat of Saccharomyces spe- cies. It has been proposed that S. cerevisiae evolved into a domesticated species found only in wineries and associated vineyards, but the discovery of Saccha- romyces species on tree bark has raised the intriguing possibility that S. cerevisiae and related species have a Fig. 1. Several studies surveyed yeasts present in the gut or on the surface of natural habitat associated with forest trees (6). More various insects. The work of Stefanini et al. (8) discusses the importance of gut recent genome sequencing revealed a new species, passage in the social wasp, P. dominula,toS. cerevisiae and survival of Saccharomyces eubayanus and, further, that it shares S. paradoxus in the gut. It draws on previous studies that provided detailed knowledge of the natural history of the wasp gut conditions and yeast genetics. homologous genes with S. cerevisiae, Saccharomyces A wasp in the same genus, Polistes fuscatus, is shown adding pulp to the “paper” paradoxus, and S. uvarum (7). This surprising discovery nest made from masticated wood and bark fibers. Image courtesy of M. J. West- again raised the question of habitat for Saccharomy- Eberhard (Smithsonian Tropical Research Institute). ces and where might it be possible for the species to interact and form hybrids. The study by Stefanini et al. the Fagaceae, oak-associated soils, and associated in- (8) in PNAS discovered Saccharomyces species to be sects (e.g., 11, 12). In several of the studies, multiple common in the intestinal tract of social wasps (Fig. 1), species of Saccharomyces were sympatric, but hybrids such as Polistes dominula, which provide a “nest” for were seldom found because of ecological isolation by overwintering and outcrossing for S. cerevisiae and factors such as growth temperature (e.g., S. cerevisiae S. paradoxus. and S. paradoxus) (10, 13). Based on these reports, it is In the search for the natural habitat of Saccharomyces clear that the wasps do more than provide a hibernac- spp. researchers have used media enriched with ulum for yeasts to overwinter. The discovery of hybrids high glucose or even alcohol to isolate the yeasts from of S. cerevisiae and S. paradoxus within the intestine oak (Quercus spp.) (9, 10) and other members of of wasps is noteworthy, but the experimental finding aDepartment of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803; bDepartment of Biological Sciences, University of South Carolina, Columbia, SC 29208; and cMycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, Peoria, IL 61604 Author contributions: M.B. and C.P.K. wrote the paper. The authors declare no conflict of interest. See companion article on page 2247. 1To whom correspondence should be addressed. Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1600173113 PNAS | February 23, 2016 | vol. 113 | no. 8 | 1971–1973 Downloaded by guest on September 27, 2021 Fig. 3. Ascoidea asiatica was isolated from a beetle larva infesting wood, and it is probably an ambrosia fungus disseminated by insect vectors. “Yeast” is a growth form exhibited by many terrestrial fungi, but it also may be used to refer to a specific subphylum of ascomycetes (Saccharomycotina) that reproduce asexually by Fig. 2. Yeasts are usually studied from isolations made in Petri budding and may produce sexual spores in asci that are not covered dishes, and their life histories in nature are largely unknown. by a fruiting body. Asci with hat-shaped ascospores are shown to Ascobotryozyma americana and the nematode Panagrellus dubius have developed after 15 d of growth on 5% (wt/vol) malt extract agar μ have a unique commensal relationship that would go unobserved in at 17 °C. (Scale bar, 10 m.) Although budding cells are produced pure culture. The yeast uses its bifurcate basal cell as a holdfast to in the life cycle of the yeast, abundant hyphae are also produced attach to the nematode, and it uses the invertebrate animal as a under the growth conditions used. Reprinted from ref. 20. staging platform to get nutrition from the nematode’s environment. Scanning electron micrograph. (Scale bar, 0.4 mm.) Reprinted from ref. 21, with permission from Mycologia, ©The Mycological Society wasps (16) suggests that baits could be used to conduct rapid of America. broad surveys to test the universality of the S. cerevisiae–wasp association. Such surveys should be timed to the life cycle of that S. paradoxus strains did not survive gut passage except when the wasps and other suspect insects, with consideration of the rescued by hybridization is remarkable (8). In addition, gut passage known geographical and ecological limits of the organisms (17). promotes conditions favorable to outcrossing, explaining high In a commentary on a paper enumerating large numbers of po- rates of strain diversity in S. cerevisiae. tential undescribed yeasts from the gut of beetles (18), Boekhout Insects, including wasps, have long been seen to damage (19) reported that insect sources accounted for only 6% of the grapes, and damaged grapes have much higher frequencies of S. isolates in the Centraalbureau voor Schmmelcultures (CBS) yeast cerevisiae, thus supporting the view that the natural habitat of the collection, and the insect gut was a “highly promising route” to yeast is undiscovered and alerting yeast specialists to look else- the discovery of hidden microbial diversity. It now is obvious not where for wild populations (14). About 300 taxa of Polistes are only that new species may exist in the gut of insects but that recognized worldwide, and about 20 are present in the United known yeasts rare in nature may regularly occupy insect habitats States. P. dominula, used by Stefanini et al. (8), was introduced (Figs. 2 and 3), where they prosper. to the United States from Europe in the late 1970s and has spread throughout most of the country to the West Coast, displacing Acknowledgments several of native species along the way (15). Many social wasps, The mention of trade names or commercial products in this including P. dominula, construct nests of paper made of chewed publication is solely for the purpose of providing specific in- wood fibers and bark, a potential source of wild yeasts. A corre- formation and does not imply recommendation or endorsement lation between the timing of S. cerevisae population buildup until by the US Department of Agriculture (USDA). The USDA is an equal midsummer could be correlated with the life cycle of a number of opportunity provider and employer. We thank Dr. Julia L. Kerrigan Polistes species. The use of wine and alcohol baits to attract pest for providing the original high resolution image used in Fig. 2. 1 Johnson EA, Echavarri-Erasun C (2011) Yeast biotechnology. The Yeasts, a Taxonomic Study, eds Kurtzman CP, Fell JW, Boekhout T (Elsevier, Amsterdam), 5th Ed, pp 21–44. 2 McGovern PE (2003) Ancient Wine: The Search for the Origins of Viniculture (Princeton Univ Press, Princeton). 3 Vaughan-Martini A, Kurtzman CP (1985) Deoxyribonucleic acid relatedness among species of the genus Saccharomyces sensu stricto. Int J Syst Bacteriol 35(4): 508–511. 4 Kurtzman CP, Robnett CJ (1998) Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie van Leeuwenhoek 73(4):331–371. 5 Cavalieri D, McGovern PE, Hartl DL, Mortimer R, Polsinelli M (2003) Evidence for S. cerevisiae fermentation in ancient wine. J Mol Evol 57(Suppl 1):S226–S232. 6 Naumov GI (2013) Ecological and biogeographical features of Saccharomyces paradoxus Batschinskaya yeast and related species: I. The early studies. Microbiology 82(4):397–403. 7 Baker EC, et al. (2015) The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts. Mol Biol Evol 32(11):2818–2831. 8 Stefanini I, et al. (2016) Social wasps are a Saccharomyces mating nest. Proc Natl Acad Sci USA 113:2247–2251. 1972 | www.pnas.org/cgi/doi/10.1073/pnas.1600173113 Blackwell and Kurtzman Downloaded by guest on September 27, 2021 9 Sniegowski PD, Dombrowski PG, Fingerman E (2002) Saccharomyces cerevisiae and Saccharomyces paradoxus coexist in a natural woodland site in North America and display different levels of reproductive isolation from European conspecifics. FEMS Yeast Res 1(4):299–306. 10 Sampaio JP, Gonçalves P (2008) Natural populations of Saccharomyces kudriavzevii in Portugal are associated with oak bark and are sympatric with S. cerevisiae and S. paradoxus. Appl Environ Microbiol 74(7):2144–2152. 11 Liti G, et al. (2009) Population genomics of domestic and wild yeasts. Nature 458(7236):337–341. 12 Sylvester K, et al. (2015) Temperature and host preferences drive the diversification of Saccharomyces and other yeasts: A survey and the discovery of eight new yeast species.
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