Domestication of different varieties in the cheese-making fungusGeotrichum candidum

Abstract

Domestication is an excellent model for studying adaptation processes, constituting recent adaptation and diversification, 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 hybridization. The genetic diversity in the cheese clade was the lowest but remained high compared to other domesticated fungi, indicating milder bottlenecks. Commercial starter strains were scattered across the cheese clade, not constituting a single clonal lineage. The cheese clade was 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, cheese populations displayed contrasted phenotypes, with one cheese population producing a typical blue cheese flavor and another one displaying denser and fluffier colonies, 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 three varieties with contrasted phenotypes. Some of the traits acquired by cheese strains indicate convergence with other, distantly related fungi used for cheese maturation.

Convergence in domesticated fungi used for cheese and dry-cured meat maturation: beneficial traits, genomic mechanisms, and degeneration

“…When grown as filamentous lawns on Petri dishes, they prevented the growth of fungal challengers. This was the case in the non-Roquefort P. roqueforti population, P. biforme, P. camemberti and G. candidum [36,41,43].…”

“…In contrast, the Roquefort population displayed slow lipolysis and proteolysis, which is desirable for Roquefort cheeses whose PDO (protected designation of origin) requires a long ripening period (at least 90 days). The dry-cured meat populations of P. nalgiovense and P. salamii, as well as the cheese populations of G. candidum also showed slower proteolysis and lipolysis than their wild-type conspecifics, which can be beneficial to avoid obtaining degraded products [38,41].…”

“…Phenotypic and genetic differentiation between strains collected in cheese and in other environments have been detected in P. roqueforti, G. candidum and S. cerevisiae [25,37,41] and their demographic history of domestication could be inferred. In P. roqueforti, two distinct populations have been domesticated independently, one occurring only in cheeses in the protected designation of origin (PDO) Roquefort, the other population being inoculated in all the other blue cheeses worldwide [37].…”

“…caseifulvum, found in different types of soft cheese [36]. In G. candidum, domestication has also occurred in several steps, the cheese clade being subdivided into three differentiated cheese populations displaying contrasting phenotypes [41]. In S. cerevisiae, the cheese population is genetically and phenotypically differentiated from populations domesticated for other usages [25].…”

“…Recent studies have revealed striking cases of convergent adaptation in cheese-making fungi. Indeed, the two fungi used as starters for soft cheese production, P. camemberti and G. candidum, evolved towards greater fluffiness and whiteness of filamentous colonies compared to their closely related lineages, at the expense of radial growth speed [36,41]. Penicillium nalgiovense and P. salamii strains isolated from dry-cured meat also evolved greater whiteness [38].…”