The Genome Sequence ofSaccharomyces eubayanusand the Domestication of Lager-Brewing Yeasts

Abstract

The dramatic phenotypic changes that occur in organisms during domestication leave indelible imprints on their genomes. Although many domesticated plants and animals have been systematically compared with their wild genetic stocks, the molecular and genomic processes underlying fungal domestication have received less attention. Here, we present a nearly complete genome assembly for the recently described yeast species Saccharomyces eubayanus and compare it to the genomes of multiple domesticated alloploid hybrids of S. eubayanus × S. cerevisiae (S. pastorianus syn. S. carlsbergensis), which are used to brew lager-style beers. We find that the S. eubayanus subgenomes of lager-brewing yeasts have experienced increased rates of evolution since hybridization, and that certain genes involved in metabolism may have been particularly affected. Interestingly, the S. eubayanus subgenome underwent an especially strong shift in selection regimes, consistent with more extensive domestication of the S. cerevisiae parent prior to hybridization. In contrast to recent proposals that lager-brewing yeasts were domesticated following a single hybridization event, the radically different neutral site divergences between the subgenomes of the two major lager yeast lineages strongly favor at least two independent origins for the S. cerevisiae × S. eubayanus hybrids that brew lager beers. Our findings demonstrate how this industrially important hybrid has been domesticated along similar evolutionary trajectories on multiple occasions.

Multiple Origins of the Pathogenic Yeast Candida orthopsilosis by Separate Hybridizations between Two Parental Species

“…Natural hybrids between many of the members of the Saccharomyces species complex have been identified [10, 11]. For example, Saccharomyces pastorianus formed at least twice from recent hybridizations between Saccharomyces cerevisiae and Saccharomyces eubayanus , and this event has been associated with the acquisition of cold tolerance in the lager yeast [12–14]. …”

A Large Set of Newly Created Interspecific Saccharomyces Hybrids Increases Aromatic Diversity in Lager Beers

“…Whereas it was generally assumed that lager yeasts were hybrids between S. cerevisiae and S. bayanus, Libkind et al (11) showed that the second parent is actually S. eubayanus, a species originally discovered in Patagonia but later also isolated in other regions, such as North America and China (11)(12)(13). Although conclusive molecular evidence is not available (14), it is currently believed that the S. cerevisiae/S. eubayanus hybridization event took place 500 to 600 years ago, when German laws forced brewers to use lower fermentation temperatures, promoting the selection of rare natural hybrids between the common brewer's yeast S. cerevisiae and the more cold-tolerant S. eubayanus (11,15).…”

Ongoing resolution of duplicate gene functions shapes the diversification of a metabolic network

“…The first additional duplicate gene is GAL80B , which is a paralog of GAL80 ; this pair of paralogs was created by the whole genome duplication (WGD) event roughly 100 million years ago (Wolfe and Shields, 1997; Marcet-Houben and Gabaldón, 2015). GAL80B has been retained in the S. uvarum-Saccharomyces eubayanus clade, but it was lost in the S. cerevisiae - Saccharomyces arboricola clade (Hittinger et al, 2010, 2004; Scannell et al, 2011; Caudy et al, 2013; Hittinger, 2013; Liti et al, 2013; Baker et al, 2015). The second one is GAL2B , which was created by a recent tandem duplication in S. uvarum-S. eubayanus clade.…”

“…After the S. uvarum-S. eubayanus clade diverged from the S. arboricola-S. cerevisiae clade, these genes met distinct fates in different lineages (Figure 8). GAL80B was lost in the S. cerevisiae-S. arboricola clade, while it was retained in S. uvarum and S. eubayanus (Hittinger et al, 2010, 2004; Scannell et al, 2011; Caudy et al, 2013; Hittinger, 2013; Liti et al, 2013; Baker et al, 2015). The fates of GAL1 and GAL3 were still more varied.…”