Adaptive Horizontal Gene Transfers between Multiple Cheese-Associated Fungi

Description

Domestication is an excellent model for studies ofadaptation because it involves recent and strong selectionon a few, identified traits [1–5]. Few studieshave focused on the domestication of fungi, withnotable exceptions [6–11], despite their importanceto bioindustry [12] and to a general understandingof adaptation in eukaryotes [5]. Penicillium fungi areubiquitous molds among which two distantly relatedspecies have been independently selected forcheese making—P. roqueforti for blue cheeses likeRoquefort and P. camemberti for soft cheeses likeCamembert. The selected traits include morphology,aromatic profile, lipolytic and proteolytic activities,and ability to grow at low temperatures, in a matrixcontaining bacterial and fungal competitors [13–15].By comparing the genomes of ten Penicillium species,we show that adaptation to cheese was associatedwith multiple recent horizontal transfers of largegenomic regions carrying crucial metabolic genes.We identified seven horizontally transferred regions(HTRs) spanning more than 10 kb each, flankedby specific transposable elements, and displayingnearly 100% identity between distant Penicilliumspecies. Two HTRs carried genes with functionsinvolved in the utilization of cheese nutrients orcompetition and were found nearly identical in multiplestrains and species of cheese-associated Penicilliumfungi, indicating recent selective sweeps; theywere experimentally associated with faster growthand greater competitiveness on cheese and containedgenes highly expressed in the early stage ofcheese maturation. These findings have industrialand food safety implications and improve our understanding of the processes of adaptation to rapidenvironmental changes.

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