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

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Bennetot, Bastien | Vernadet, Jean-Philippe | Perkins, Vincent | Hautefeuille, Sophie | Rodríguez de La Vega, Ricardo C. | O’donnell, Samuel | Snirc, Alodie | Grondin, Cécile | Lessard, Marie-Hélène | Peron, Anne-Claire | Labrie, Steve | Landaud, Sophie | Giraud, Tatiana, E | Ropars, Jeanne

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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.

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