Adaptive Horizontal Gene Transfers between Multiple Cheese-Associated Fungi

• Published in: Current biology Vol. 25; no. 19; pp. 2562 - 2569
• Main Authors: Ropars, Jeanne, Rodríguez de la Vega, Ricardo C., López-Villavicencio, Manuela, Gouzy, Jérôme, Sallet, Erika, Dumas, Émilie, Lacoste, Sandrine, Debuchy, Robert, Dupont, Joëlle, Branca, Antoine, Giraud, Tatiana
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 05.10.2015; Elsevier; Cell Press
• Subjects: Adaptation, Biological - physiology; Cheese - microbiology; CheesyTer; convergence; DNA, Fungal - metabolism; Food Microbiology; food spoiler; Fungi - genetics; gene expression; Gene Transfer, Horizontal; HGT; Life Sciences; parallel adaptation; Penicillium; Penicillium - metabolism; Phenotype; Wallaby; food spoiler; HGT; convergence; Penicillium; Wallaby; CheesyTer; parallel adaptation; gene expression; Domestication; Fromage; Bio-Industrie; Champignons Penicillium
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2015.08.025

Domestication is an excellent model for studies of adaptation because it involves recent and strong selection on a few, identified traits [1–5]. Few studies have focused on the domestication of fungi, with notable exceptions [6–11], despite their importance to bioindustry [12] and to a general understanding of adaptation in eukaryotes [5]. 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 [13–15]. 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. These findings have industrial and food safety implications and improve our understanding of the processes of adaptation to rapid environmental changes. •New HTRs are found in cheese fungi•HTRs are flanked by specific transposable elements•HTRs have spread in cheese-associated fungi through recent selective sweeps•Experiments link two HTRs to growth and competitive advantages on cheese Ropars et al. report newly discovered horizontally transferred regions, flanked by specific transposable elements that allow cheese-making fungi and food spoilers to grow faster and be better competitors on cheese. These findings have industrial and food safety implications and also improve our understanding of adaptation processes.