Domestication is an excellent model for studies of adaptation because it involves recent and strong selection on a few, identified traits. Few studies have focused on the domestication of fungi, despite their importance to bioindustry and to a general understanding of adaptation in eukaryotes. Penicillium fungi are ubiquitous molds among which two distantly related species have been independently selected for cheese-making, P. roqueforti for blue cheeses like Roquefort, and P. camemberti for soft cheeses like Camembert. The selected traits include morphology, aromatic profile, lipolytic and proteolytic activities, and ability to grow at low temperatures, in a matrix containing bacterial and fungal competitors. By comparing the genomes of ten Penicillium species, we show that adaptation to cheese was associated with multiple recent horizontal transfers of large genomic regions carrying crucial metabolic genes. We identified seven horizontally-transferred regions (HTRs) spanning more than 10 kb each, flanked by specific transposable elements, and displaying nearly 100% identity between distant Penicillium species. Two HTRs carried genes with functions involved in the utilization of cheese nutrients or competition and were found nearly identical in multiple strains and species of cheese-associated Penicillium fungi, indicating recent selective sweeps; they were experimentally associated with faster growth and greater competitiveness on cheese and contained genes highly expressed in the early stage of cheese maturation.
We also used population genomics to reconstruct the evolutionary history of Penicillium roqueforti. Four populations were identified, including two containing only cheese strains (one corresponding to the emblematic Roquefort “protected designation of origin” strains), and two non-cheese populations including silage and food-spoiling strains. Approximate Bayesian computation analyses indicated that the two cheese populations were derived from independent domestication events. The non-Roquefort population had experienced a stronger genetic bottleneck and displayed greater fitness for traits related to industrial cheese maturation, such as greater lipolysis, cheese cavity colonization and salt tolerance. It probably originated from the industrial selection of a single clonal lineage and is used worldwide for the production of all types of blue cheese other than Roquefort. The Roquefort population resulted from a softer domestication event, probably due to the ancient use of different strains across multiple farms, with possible selection for slower growth before the invention of refrigeration and for greater spore production on the traditional multiplication medium (bread). We detected genomic regions affected by recent positive selection and genomic islands specific to one of the cheese populations, some of which corresponded to putative horizontal gene transfer events. This study sheds light on the processes of adaptation to rapid environmental changes, has industrial implications and raises questions about the conservation of genetic resources.