Domestication of different varieties in the cheese-making fungus Geotrichum candidum

Domestication is an excellent model for studying adaptation processes, involving recent adaptation and diversification, convergence following adaptation to similar conditions, as well as degeneration of unused functions. Geotrichum candidum is a fungus used for cheese-making and is also found in other environments such as soil and plants. By analyzing whole-genome data from 98 strains, we found that all strains isolated from cheese formed a monophyletic clade. Within the cheese clade, we identified three differentiated populations and we detected footprints of recombination and admixture. The genetic diversity in the cheese clade was high, indicating a lack of strong bottleneck. Commercial starter strains were scattered across the cheese clade, thus not constituting a single clonal lineage. The cheese populations were phenotypically differentiated from other populations, with a slower growth on all media, even cheese, a prominent production of attractive cheese flavors and a lower proteolytic activity. Furthermore, one of the cheese populations displayed footprints of a more advanced state of domestication, with much lower genetic diversity, denser and fluffier colones and excluding more efficiently cheese spoiler fungi. Cheese populations lost two beta lactamase-like genes, involved in xenobiotic clearance, and displayed transposable element expansion, likely due to relaxed selection. Our findings suggest the existence of genuine domestication in G. candidum, which led to diversification into different varieties with contrasted phenotypes. Some of the traits acquired by cheese strains indicate convergence with other, distantly related fungi used for cheese maturation.