title: Adaptive Horizontal Gene Transfers between Multiple Cheese-Associated Fungi.
abstract: 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.
authors.affiliation: Ecologie, Systématique et Evolution, UMR8079, Univ. Paris-Sud, 91405 Orsay, France; Ecologie, Systématique et Evolution, UMR8079, CNRS, 91405 Orsay, France.
authors.forename: Jeanne
authors.initials: J
authors.lastname: Ropars
authors.affiliation: Ecologie, Systématique et Evolution, UMR8079, Univ. Paris-Sud, 91405 Orsay, France; Ecologie, Systématique et Evolution, UMR8079, CNRS, 91405 Orsay, France.
authors.forename: Ricardo C
authors.initials: RC
authors.lastname: Rodríguez de la Vega
authors.affiliation: Institut de Systématique, Evolution, Biodiversité, UMR 7205 CNRS-MNHN-UPMC-EPHE, Muséum national d'Histoire naturelle, Sorbonne Université, CP39, 57 Rue Cuvier, 75231 Paris Cedex 05, France.
authors.forename: Manuela
authors.initials: M
authors.lastname: López-Villavicencio
authors.affiliation: Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441, INRA, Castanet-Tolosan 31326, France; Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594, CNRS, Castanet-Tolosan 31326, France.
authors.forename: Jérôme
authors.initials: J
authors.lastname: Gouzy
authors.affiliation: Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441, INRA, Castanet-Tolosan 31326, France; Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594, CNRS, Castanet-Tolosan 31326, France.
authors.forename: Erika
authors.initials: E
authors.lastname: Sallet
authors.affiliation: Ecologie, Systématique et Evolution, UMR8079, Univ. Paris-Sud, 91405 Orsay, France; Ecologie, Systématique et Evolution, UMR8079, CNRS, 91405 Orsay, France.
authors.forename: Émilie
authors.initials: É
authors.lastname: Dumas
authors.affiliation: Institut de Systématique, Evolution, Biodiversité, UMR 7205 CNRS-MNHN-UPMC-EPHE, Muséum national d'Histoire naturelle, Sorbonne Université, CP39, 57 Rue Cuvier, 75231 Paris Cedex 05, France.
authors.forename: Sandrine
authors.initials: S
authors.lastname: Lacoste
authors.affiliation: Institut de Génétique et Microbiologie, UMR8621, Univ. Paris-Sud, 91405 Orsay, France; Institut de Génétique et Microbiologie, UMR8621, CNRS, 91405 Orsay, France.
authors.forename: Robert
authors.initials: R
authors.lastname: Debuchy
authors.affiliation: Institut de Systématique, Evolution, Biodiversité, UMR 7205 CNRS-MNHN-UPMC-EPHE, Muséum national d'Histoire naturelle, Sorbonne Université, CP39, 57 Rue Cuvier, 75231 Paris Cedex 05, France.
authors.forename: Joëlle
authors.initials: J
authors.lastname: Dupont
authors.affiliation: Ecologie, Systématique et Evolution, UMR8079, Univ. Paris-Sud, 91405 Orsay, France; Ecologie, Systématique et Evolution, UMR8079, CNRS, 91405 Orsay, France. Electronic address: antoine.branca@u-psud.fr.
authors.forename: Antoine
authors.initials: A
authors.lastname: Branca
authors.affiliation: Ecologie, Systématique et Evolution, UMR8079, Univ. Paris-Sud, 91405 Orsay, France; Ecologie, Systématique et Evolution, UMR8079, CNRS, 91405 Orsay, France. Electronic address: tatiana.giraud@u-psud.fr.
authors.forename: Tatiana
authors.initials: T
authors.lastname: Giraud
mesh_terms: D000220:Adaptation, Biological / Q000502:physiology; D002611:Cheese / Q000382:microbiology*; D004271:DNA, Fungal / Q000378:metabolism; D005516:Food Microbiology; D005658:Fungi / Q000235:genetics*; D022761:Gene Transfer, Horizontal; D010407:Penicillium / Q000378:metabolism; D010641:Phenotype
chemical_list: D004271:DNA, Fungal
keywords: CheesyTer; HGT; Penicillium; Wallaby; convergence; food spoiler; gene expression; parallel adaptation