Genomic and phenotypic imprints of microbial domestication on cheese starter cultures

Abstract

Domestication – the artificial selection of wild species to obtain variants with traits of human interest– was integral to the rise of civilization. During the neolithic, the oversupply of food enabled by the domestication of crop plants and farm animals was associated with the invention of food preservation strategies through microbial fermentation. However, it remains unclear whether fermented food microbes show similar signs of domestication by humans like plants or animals. Only a few eukaroytic have been studied so far in this respect (e.g., yeasts used in mantou or wine), whereas little is known for bacteria. Here, we tested if cheese starter cultures harbour typical hallmarks of domestication by characterising over 100 community samples and over 100 individual strains isolated from historical and modern traditional Swiss cheese starter cultures. We find that cheese starter cultures have low genetic diversity both at the species and strain-level and are taxonomically and phenotypically stable. Our analyses further suggest that the evolutionary origin of the bacteria in cheese starter cultures coincided with the start of cheesemaking as reported from archeological records. Finally, we find evidence for ongoing genome decay and pseudogenization via transposon insertion related to a reduction of their niche breadth. These characteristics suggest that cheese starter cultures were domesticated by humans before knowing about microbes, potentially starting as early as the neolithics. Future work documenting the prevalence of these hallmarks across diverse fermented food systems and geographic regions will be key to unveiling the joint history of humanity with fermented food microbes.