Domestication in dry-cured meat Penicillium fungi: Convergent specific phenotypes and horizontal gene transfers without strong genetic subdivision

TY - JOUR

T1 - Domestication in dry-cured meat Penicillium fungi

T2 - Convergent specific phenotypes and horizontal gene transfers without strong genetic subdivision

AU - Lo, Ying Chu

AU - Bruxaux, Jade

AU - Rodríguez de la Vega, Ricardo C.

AU - O'Donnell, Samuel

AU - Snirc, Alodie

AU - Coton, Monika

AU - Le Piver, Mélanie

AU - Le Prieur, Stéphanie

AU - Roueyre, Daniel

AU - Dupont, Joëlle

AU - Houbraken, Jos

AU - Debuchy, Robert

AU - Ropars, Jeanne

AU - Giraud, Tatiana

AU - Branca, Antoine

N1 - Funding Information: This work was supported by the ERC starting grant GenomeFun 309403 and Louis D foundation award to TG, a CNRS PEPS adaptation grant to AB and the FUNGADAPT ANR-19-CE20-0002 ANR grant to TG, AB and MC. YCL acknowledges a PhD grant from the France–Taiwan joint program Campus France. We thank Alice Feurtey, Fanny Hartmann and Fantin Carpentier for help with genome analyses. We thank MNHN for granting access to strains with the help of Manuela Lopez-Villavicencio and Sandrine Lacoste. We thank all the people who sent dry-cured meat casings from around the world. We thank the GenoToul platform for sequencing. We are also grateful to the GenoToul bioinformatics platform Toulouse Occitanie (Bioinfo Genotoul, doi: 10.15454/1.5572369328961167E12) for providing some computing resources. PacBio sequencing was conducted at the IGM Genomics Center, University of California, San Diego, La Jolla, CA. We thank Federico Laich and Giancarlo Perrone for providing P. salamii strains. Some sequence data (Table S2) were produced by the US Department of Energy Joint Genome Institute http://www.jgi.doe.gov/ in collaboration with the user community. Funding Information: This work was supported by the ERC starting grant GenomeFun 309403 and Louis D foundation award to TG, a CNRS PEPS adaptation grant to AB and the FUNGADAPT ANR‐19‐CE20‐0002 ANR grant to TG, AB and MC. YCL acknowledges a PhD grant from the France–Taiwan joint program Campus France. We thank Alice Feurtey, Fanny Hartmann and Fantin Carpentier for help with genome analyses. We thank MNHN for granting access to strains with the help of Manuela Lopez‐Villavicencio and Sandrine Lacoste. We thank all the people who sent dry‐cured meat casings from around the world. We thank the GenoToul platform for sequencing. We are also grateful to the GenoToul bioinformatics platform Toulouse Occitanie (Bioinfo Genotoul, doi: 10.15454/1.5572369328961167E12 ) for providing some computing resources. PacBio sequencing was conducted at the IGM Genomics Center, University of California, San Diego, La Jolla, CA. We thank Federico Laich and Giancarlo Perrone for providing strains. Some sequence data (Table S2 ) were produced by the US Department of Energy Joint Genome Institute http://www.jgi.doe.gov/ in collaboration with the user community. P. salamii Publisher Copyright: © 2023 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd.

PY - 2023/9

Y1 - 2023/9

N2 - Some 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 is 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 related Penicillium species used for dry-cured meat production, P. nalgiovense, the most common species in the dry-cured meat food industry, and P. 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 of P. nalgiovense were 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 available Penicillium genomes from various environments revealed HGTs, particularly between P. nalgiovense and P. salamii (representing almost 1.5 Mb of cumulative length). HGTs additionally involved P. 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 the P. salamii and P. nalgiovense populations used for dry-cured meat production, which constitutes domestication. Several genetic and phenotypic changes were similar in P. salamii, P. nalgiovense and P. 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.

AB - Some 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 is 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 related Penicillium species used for dry-cured meat production, P. nalgiovense, the most common species in the dry-cured meat food industry, and P. 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 of P. nalgiovense were 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 available Penicillium genomes from various environments revealed HGTs, particularly between P. nalgiovense and P. salamii (representing almost 1.5 Mb of cumulative length). HGTs additionally involved P. 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 the P. salamii and P. nalgiovense populations used for dry-cured meat production, which constitutes domestication. Several genetic and phenotypic changes were similar in P. salamii, P. nalgiovense and P. 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.

KW - convergence

KW - domestication

KW - fungi

KW - parallel adaptation

KW - sausage

UR - http://www.scopus.com/inward/record.url?scp=85170403750&partnerID=8YFLogxK

U2 - 10.1111/eva.13591

DO - 10.1111/eva.13591

M3 - Article

AN - SCOPUS:85170403750

SN - 1752-4563

VL - 16

SP - 1637

EP - 1660

JO - Evolutionary Applications

JF - Evolutionary Applications

IS - 9

ER -