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

Lo, Ying‐Chu; Bruxaux, Jade; Rodríguez de la Vega, Ricardo C.; O'Donnell, Samuel; Snirc, Alodie; Coton, Monika; Le Piver, Mélanie; Le Prieur, Stéphanie; Roueyre, Daniel; Dupont, Joëlle; Houbraken, Jos; Debuchy, Robert; Ropars, Jeanne; Giraud, Tatiana; Branca, Antoine

doi:10.1111/eva.13591

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

Journal Article · 07 September 2023 · Evolutionary Applications

DOI: https://doi.org/10.1111/eva.13591 · OSTI ID:2422810

Lo, Ying‐Chu ^[1];

^[2];

^[1]; O'Donnell, Samuel ^[1]; Snirc, Alodie ^[1]; Coton, Monika ^[3]; Le Piver, Mélanie ^[4]; Le Prieur, Stéphanie ^[1]; Roueyre, Daniel ^[4]; Dupont, Joëlle ^[5]; Houbraken, Jos ^[6]; Debuchy, Robert ^[7]; Ropars, Jeanne ^[1];

^[1];

^[1]

Univ. Paris-Saclay, Gif-sur-Yvette (France). Institute for the Diversity, Ecology and Evolution of the Living World (IDEEV)
Univ. Paris-Saclay, Gif-sur-Yvette (France). Institute for the Diversity, Ecology and Evolution of the Living World (IDEEV); Umea Univ. (Sweden)
Université de Bretagne Occidentale (France). University Laboratory of Biodiversity and Microbial Ecology (LUBEM)
Interprofessional Production Laboratory, Aurillac (France)
National Museum of Natural History, Paris (France)
Westerdijk Fungal Biodiversity Institute, Utrecht (Netherlands)
Univ. Paris-Saclay, Gif-sur-Yvette (France). Institute for Integrative Biology of the Cell (I2BC)

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.

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Research Organization:: USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2422810

Journal Information:: Evolutionary Applications, Journal Name: Evolutionary Applications Journal Issue: 9 Vol. 16; ISSN 1752-4571

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

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