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Microbe Domestication and the Identification of the Wild Genetic Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast Diego Libkinda,1, Chris Todd Hittingerb,c,1,2, Elisabete Valériod, Carla Gonçalvesd, Jim Doverb,c, Mark Johnstonb,c, Paula Gonçalvesd, and José Paulo Sampaiod,3 aLaboratorio de Microbiología Aplicada y Biotecnología, Instituto de Investigaciones en Biodiversidad y Medio-ambiente, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)-Universidad Nacional del Comahue, 8400 Bariloche, Argentina; bDepartment of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, CO 80045; cDepartment of Genetics, Center for Genome Sciences, Washington University in St. Louis School of Medicine, St. Louis, MO 63108; and dCentro de Recursos Microbiológicos, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, 2829-516 Caparica, Portugal Edited by John Doebley, University of Wisconsin, Madison, WI, and approved July 20, 2011 (received for review April 5, 2011) Domestication of plants and animals promoted humanity’s transi- Saccharomyces pastorianus (syn. Saccharomyces carlsbergensis) tion from nomadic to sedentary lifestyles, demographic expansion, strains (8); two other cryotolerant Saccharomyces spp. have been and the emergence of civilizations. In contrast to the well-docu- associated with beer as contaminants (Saccharomyces bayanus) mented successes of crop and livestock breeding, processes of mi- and with cider or wine fermented at low temperatures (Saccha- crobe domestication remain obscure, despite the importance of romyces uvarum) (9). S. pastorianus has never been isolated from microbes to the production of food, beverages, and biofuels. Lager- the wild, depends on humans for its propagation, and appears to beer, first brewed in the 15th century, employs an allotetraploid be an allotetraploid hybrid species of S. cerevisiae and an un- hybrid yeast, Saccharomyces pastorianus (syn. Saccharomyces identified species (10, 11). Several hypotheses have been ad- carlsbergensis), a domesticated species created by the fusion of vanced for the source of the non-S. cerevisiae genome present in a Saccharomyces cerevisiae ale-yeast with an unknown cryotoler- S. pastorianus, including the taxonomically and genetically com- – “ ” ant Saccharomyces species. We report the isolation of that species plex species S. bayanus (12 14) and an unknown lager lineage and designate it Saccharomyces eubayanus sp. nov. because of its distinct both from S. bayanus and S. uvarum (11, 15). Identifying resemblance to Saccharomyces bayanus (a complex hybrid of S. the wild genetic stock of the cryotolerant subgenome of S. pas- eubayanus, Saccharomyces uvarum, and S. cerevisiae found only torianus is necessary for resolving the taxonomy and systematics in the brewing environment). Individuals from populations of S. of this important species complex, and for understanding the key eubayanus and its sister species, S. uvarum, exist in apparent sym- events that led to the domestication of lager yeast. In contrast to extensive investigation into domestication of patry in Nothofagus (Southern beech) forests in Patagonia, but are crops and livestock (2, 16–19), studies of domestication of isolated genetically through intrinsic postzygotic barriers, and eco- eukaryotic microbes have been limited (20–24), perhaps because logically through host-preference. The draft genome sequence of of the inability to conduct direct field studies. Identifying the S. eubayanus is 99.5% identical to the non-S. cerevisiae portion of genetic basis of traits under selection during domestication may the S. pastorianus genome sequence and suggests specific changes fi clarify the emergence of new traits and show the way toward in sugar and sul te metabolism that were crucial for domestica- further improvement. Because domesticated lineages derive tion in the lager-brewing environment. This study shows that com- from a subset of the original populations, a genetic bottleneck is bining microbial ecology with comparative genomics facilitates likely to have caused the disappearance of some alleles (17), the discovery and preservation of wild genetic stocks of domesti- especially in microbes, which are often propagated clonally. In an cated microbes to trace their history, identify genetic changes, and age of accelerated habitat destruction and diminishing bio- suggest paths to further industrial improvement. diversity, discovery of wild genetic stocks of domesticated microbes will facilitate preservation of their genetic resources for beer yeast | next-generation sequencing | yeast ecology | yeast taxonomy strain improvement. he beginning of agriculture and the domestication of plants Results and Discussion Tand animals are among the most decisive events in human Discovery of Wild Populations of Cryotolerant Saccharomyces. Sac- history because they triggered the rise of civilizations and the charomyces spp. are associated with oak trees (Fagaceae) in the attendant demographic, technological, and cultural develop- Northern Hemisphere (25, 26). Because species of the genus ments (1). The domestication of barley in the Fertile Crescent Nothofagus (Southern beeches, also members of the Fagales) (2) led to the emergence of the forebear of modern beer in occupy the oak niche in temperate regions of the Southern Sumeria 6,000 y ago (3). Beer and other alcoholic beverages Hemisphere (27), our survey in Northwestern Patagonia for Sac- may have played a pivotal role in cementing human societies through the social act and rituals of drinking (4) and by pro- viding a source of nutrition, medicine, and uncontaminated Author contributions: D.L., C.T.H., M.J., P.G., and J.P.S. designed research; D.L., C.T.H., E.V., C.G., and J.D. performed research; D.L. and C.T.H. contributed new reagents/analytic water (5). Since the emergence of fermented beverages roughly tools; D.L., C.T.H., P.G., and J.P.S. analyzed data; and C.T.H., P.G., and J.P.S. wrote the matches the domestication of plants and animals, it is likely that paper. some yeast lineages with favored traits were also unwittingly The authors declare no conflict of interest. EVOLUTION domesticated. This article is a PNAS Direct Submission. In Europe, brewing gradually evolved during the Middle Ages Data deposition: Genome data have been deposited in the National Center for Biotech- to produce ale-type beer, a process conducted by Saccharomyces nology Information’s Sequence Read Archive (www.ncbi.nlm.nih.gov/sra) (sequence nos. cerevisiae, the same species involved in producing wine and SRP006155 of SRA030851); individual genes have been deposited in GenBank (accession leavened bread. Lager-brewing arose in 15th century Bavaria, nos. JF786614–JF786710). gained broad acceptance by the late 19th century (6), and has 1D.L. and C.T.H. contributed equally to this work. since become the most popular technique for producing alco- 2Present address: Laboratory of Genetics, University of Wisconsin, Madison, WI 53706. holic beverages, with over 250 billion dollars of global sales in 3To whom correspondence should be addressed. E-mail: [email protected]. 2008 (7). Unlike most ales and wines, lagers require slow, low- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. temperature fermentations that are carried out by cryotolerant 1073/pnas.1105430108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1105430108 PNAS | August 30, 2011 | vol. 108 | no. 35 | 14539–14544 Downloaded by guest on October 1, 2021 charomyces focused on woodlands containing populations of apparent coexistence of these two species. Detailed field and Nothofagus antarctica, Nothofagus dombeyi,andNothofagus pum- laboratory studies into the causes of isolation are called for. ilio, within and near Lanin and Nahuel Huapi National Parks (Argentina) (Fig. S1). We also surveyed stromata of Cyttaria har- Genome Sequences Resolve Saccharomyces Taxonomy and System- iotii (an obligate ascomycete parasite of Nothofagus spp.) because atics. The identification and taxonomy of S. bayanus, S. pastor- these fruiting structures are rich in simple sugars and provide ianus,andS. uvarum is problematic and controversial because a favorable yeast habitat (28). A total of 133 samples of Nothofagus S. bayanus and S. pastorianus have only been isolated from human- bark, soil from underneath the trees, and Cyttaria stromata, col- associated fermentations. Indeed, all known representatives of lected from 2006 to 2008, yielded 123 isolates of cryotolerant these two species have been suspected (S. bayanus) (13) or con- fi Saccharomyces and two isolates of S. cerevisiae (Table S1). rmed (S. pastorianus) (10) to be interspecies hybrids. One po- For a preliminary identification of the cryotolerant Saccharo- tential exception is the brewing contaminant NBRC 1948, which myces isolates, we determined the DNA sequence of individual was asserted to be a pure strain of S. bayanus based primarily on genes, performed PCR-fingerprinting, and examined restriction RFLP evidence from all 16 chromosomes (15). A broad survey of several strains previously assigned to S. bayanus, S. pastorianus, fragment length polymorphisms (RFLPs), using S. bayanus CBS “ ” 380T, S. uvarum CBS 395T, and S. uvarum CBS 7001 (referred to and S. uvarum led to the conclusion that an additional lager as S. bayanus in genomics literature) as references (Fig. S2). The lineage or species exists that contributed its genome to S. pastor- ianus (15). In contrast, the genome
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