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

Abstract

AbstractSome 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 (HGTs). Studying their adaptation to human-made substrates are of fundamental and applied importance, for understanding adaptation processes and for further strain improvement. We studied here the population structures and phenotypes of two distantly relatedPenicilliumspecies used for dry-cured meat production,P. nalgiovense, the most common species in the dry-cured meat food industry, andP. salamii, used locally by farms. Both species displayed low genetic diversity, lacking 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 conspecifics, and those ofP. nalgiovensewere whiter. Phenotypically, 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 availablePenicilliumgenomes from various environments revealed HGTs, particularly betweenP. nalgiovenseandP. salamii(representing almost 1.5 Mb of cumulative length). HGTs additionally involvedP. biforme, also found in dry-cured meat products. We further detected positive selection based on amino-acid changes. Our findings suggest that selection by humans has shaped theP. salamiiandP. nalgiovensepopulations used for dry-cured meat production, which constitutes domestication. Several genetic and phenotypic changes were similar inP. salamii,P. nalgiovense,andP. biforme, indicating convergent adaptation to the same human-made environment. Our findings have implications for fundamental knowledge on adaptation and for the food industry: the discovery of different phenotypes and of two mating types paves the way for strain improvement by conventional breeding, to elucidate the genomic bases of beneficial phenotypes and to generate diversity.