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

A new cheese population in Penicillium roqueforti and adaptation of the five populations to their ecological niche

“…We found no particular tolerance for biologically relevant low temperature in the cheese populations, as in previous studies on other Penicillium cheese-making fungi (Ropars et al, 2020) or in other fungi used for cheese making, such as Bisifusarium domesticum and Geotrichum candidum (Bennetot et al, 2023;Savary et al, 2022).…”

“…The non-Roquefort population also had the lowest genetic diversity, likely due to strong bottlenecks, which was not the case of the Roquefort population, certainly due to PDO requirements. Such gradual domestication syndromes have previously been reported in the soft-cheese making fungi from the P. camemberti clade (Ropars et al, 2020) and in the cheesemaking fungus Geotrichum candidum (Bennetot et al, 2023). This suggests a protracted domestication process, with ancient, mild domestication, followed by more intensive selection in industrial times, as reported for example in maize (Allaby et al, 2008;Janzen & Hufford, 2016).…”

A new cheese population inPenicillium roquefortiand adaptation of the five populations to their ecological niche

“…camemberti clade (Ropars et al, 2020) and in the cheese-making fungus Geotrichum candidum (Bennetot et al, 2023). This suggests a protracted domestication process, with ancient, mild domestication, followed by more intensive selection in industrial times, as reported for example in maize (Allaby et al, 2008;Janzen & Hufford, 2016).…”

“…We found no particular tolerance for biologically relevant low temperature in the cheese populations, as in previous studies on other Penicillium cheese-making fungi (Ropars et al ., 2020) or in other fungi used for cheese making, such as Bisifusarium domesticum and Geotrichum candidum (Savary et al ., 2022; Bennetot et al ., 2023). In the S. cerevisiae yeast, different modes of fermentation, at high versus low temperature, have yielded distinct lineages with different optimal temperatures (Baker et al ., 2019).…”

“…The non-Roquefort population also had the lowest genetic diversity, likely due to strong bottlenecks, which was not the case of the Roquefort population, certainly due to PDO requirements. Such gradual domestication syndromes have previously been reported in the soft-cheese making fungi from the P. camemberti clade (Ropars et al ., 2020) and in the cheese-making fungus Geotrichum candidum (Bennetot et al ., 2023). This suggests a protracted domestication process, with ancient, mild domestication, followed by more intensive selection in industrial times, as reported for example in maize (Allaby et al ., 2008; Janzen & Hufford, 2016).…”