Domestication in dry-cured meatPenicilliumfungi: convergent specific phenotypes and horizontal gene transfers without strong genetic subdivision

Abstract

Many fungi have been domesticated for food production, with genetic differentiation between populations from food and wild environments, and food populations often acquiring beneficial traits through horizontal gene transfers. We studied the population structures and phenotypes of two distantly related Penicillium species used for dry-cured meat production, P. nalgiovense, the most common species in the dry-cured meat food industry, and P. salamii, used locally by farms. Both species displayed low genetic diversity, with no differentiation between strains isolated from dry-cured meat and those from other environments. Nevertheless, the strains collected from dry-cured meat within each species displayed slower proteolysis and lipolysis than their wild-type conspecifics, and those of P. nalgiovense were whiter. The phenotypes of the non-dry-cured meat strains were more similar to their sister species than to their conspecific dry-cured meat strains, indicating an evolution of specific phenotypes in dry-cured meat strains. A comparison of available Penicillium genomes from various environments revealed evidence of multiple horizontal gene transfers, particularly between P. nalgiovense and P. salamii. Some horizontal gene transfers involving P. biforme, also found in dry-cured meat products, were also detected. We also detected positive and purifying selection based on amino-acid changes. Our genetic and phenotypic findings suggest that human selection has shaped the P. salamii and P. nalgiovense populations used for dry-cured meat production, which constitutes domestication. Several genetic and phenotypic changes were similar in P. salamii, P. nalgiovense, and P. biforme, providing an interesting case of convergent adaptation to the same human-made environment.

Domestication of different varieties in the cheese-making fungusGeotrichum candidum

“…The slower growth and proteolysis activity may allow to prevent a too fast degradation of products during maturation, as found in the Roquefort P. roqueforti population (Dumas et al 2020). The lack of adaptation to salt was also found in the Roquefort P. roqueforti population and in dry-cured meat Penicillium fungi and may be due to evolutionary constraints (Lo et al, 2022). We also found genomic footprints of adaptation to cheese, with the presence of genomic islands of differentiation in cheese populations and the loss of genes no longer required in the human-made environment, i.e.…”

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

“…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].…”

“…Two Penicillium fungi are used for dry-cured meat production, P. nalgiovense and P. salamii, that are also phylogenetically very distant to each other [38]. In contrast to cheese fungi, no genetic subdivision was found within each of these species, between strains from dry-cured meat and other environments, although phenotypic differentiation was found (see below).…”

“…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]. The two cheese populations of P. roqueforti also changed color compared to non-cheese populations, both having independently evolved to produce bluer cheeses than non-cheese populations [37,42].…”

“…Only more recently the domestication of filamentous fungi which are used for fermenting food has begun to be studied [35]. For example, Penicillium camemberti is inoculated for the ripening of soft cheeses [36] and P. roqueforti for blue cheeses [37], whereas P. salamii and P. nalgiovense are used for dry-cured meat production [38]. Furthermore, humans have domesticated genetically distant filamentous fungi for similar uses, i.e.…”