Insights from sourdough redefine the domestication landscape of baker's yeast

Abstract

While the domestication of plants and animals is widely recognized for its role in the rise of human civilization, humans have also cultivated microbes over millennia to produce food and beverages. One microbe in particular, Saccharomyces cerevisiae, is associated with a wide variety of human-fermentation environments, including wine, beer, and notably bread, such that it is often referred to as "bakers yeast." To better illuminate the domestication history of baking associated yeast, we isolated 38 Saccharomyces cerevisiae strains from sourdough starters donated by bakers throughout North America and compared them to thousands of S. cerevisiae isolates from a variety of wild and human-fermentation environments. We identified 6 major clades with two primary domestication hubs, Mediterranean liquid-state fermentation and Asian solid-state fermentation, diverging across Eurasia that gave rise to human-associated lineages. Population genomic analyses demonstrate that S. cerevisiae strains found in sourdough starters are genetically distinct from commercial baking strains and do not come from the surrounding wild environment. Our results show that sourdough yeast strains are closely related to each other and have shared ancestry with strains isolated from various Asian solid state grain fermentations such Japanese sake, Asian rice wines, Chinese distilled spirits (baijiu), and Chinese steamed bread (mantou). We found evidence of significant admixture throughout S. cerevisiae populations, including baking-associated lineages, likely facilitated by human activity. Pangenome gene content largely captures S. cerevisiae traditional genomic sequence-based population structure and reflects human cultural practices, with differences in gene content and copy number between baking associated strains and other groups. Overall, we show that many generalized hallmarks of domestication, such as genome contraction, loss of genetic diversity, and lack of niche expansion, are not universal features of S. cerevisiae domestication, and that baking-associated yeasts have a complex evolutionary history heavily shaped by human culture.