Domestication of different varieties in the cheese-making fungus Geotrichum candidum

Domestication is an excellent model for studying adaptation processes, involving recent adaptation and diversification, convergence following adaptation to similar conditions, as well as degeneration of unused functions. Geotrichum candidum is a fungus used for cheese making and is also found in oth...

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Main Authors: Bennetot, Bastien, Vernadet, Jean-Philippe, Perkins, Vincent, Hautefeuille, Sophie, Rodríguez de la Vega, Ricardo C., O’Donnell, Samuel, Snirc, Alodie, Grondin, Cécile, Lessard, Marie-Hélène, Peron, Anne-Claire, Labrie, Steve, Landaud, Sophie, Giraud, Tatiana, Ropars, Jeanne
Format: Article
Language:English
Published: Peer Community In 2023-05-01
Series:Peer Community Journal
Online Access:https://peercommunityjournal.org/articles/10.24072/pcjournal.266/
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author Bennetot, Bastien
Vernadet, Jean-Philippe
Perkins, Vincent
Hautefeuille, Sophie
Rodríguez de la Vega, Ricardo C.
O’Donnell, Samuel
Snirc, Alodie
Grondin, Cécile
Lessard, Marie-Hélène
Peron, Anne-Claire
Labrie, Steve
Landaud, Sophie
Giraud, Tatiana
Ropars, Jeanne
author_facet Bennetot, Bastien
Vernadet, Jean-Philippe
Perkins, Vincent
Hautefeuille, Sophie
Rodríguez de la Vega, Ricardo C.
O’Donnell, Samuel
Snirc, Alodie
Grondin, Cécile
Lessard, Marie-Hélène
Peron, Anne-Claire
Labrie, Steve
Landaud, Sophie
Giraud, Tatiana
Ropars, Jeanne
author_sort Bennetot, Bastien
collection DOAJ
description Domestication is an excellent model for studying adaptation processes, involving recent adaptation and diversification, convergence following adaptation to similar conditions, as well as degeneration of unused functions. Geotrichum candidum is a fungus used for cheese making and is also found in other environments such as soil and plants. By analyzing whole-genome data from 98 strains, we found that all strains isolated from cheese formed a monophyletic clade. Within the cheese clade, we identified three genetically differentiated populations and we detected footprints of recombination and admixture. The genetic diversity in the cheese clade was similar as that in the wild clade, suggesting the lack of strong bottlenecks. Commercial starter strains were scattered across the cheese clade, thus not constituting a single clonal lineage. The cheese populations were phenotypically differentiated from other populations, with a slower growth on all media, even cheese, a prominent production of typical cheese volatiles and a lower proteolytic activity. One of the cheese clusters encompassed all soft goat cheese strains, suggesting an effect of cheese-making practices on differentiation. Another of the cheese populations seemed to represent a more advanced stage of domestication, with stronger phenotypic differentiation from the wild clade, harboring much lower genetic diversity, and phenotypes more typical of cheese fungi, with denser and fluffier colonies and a greater ability of excluding cheese spoiler fungi. Cheese populations lacked two beta lactamase-like genes present in the wild clade, involved in xenobiotic clearance, and displayed higher contents of transposable elements, likely due to relaxed selection. Our findings suggest the existence of genuine domestication in G. candidum, which led to diversification into different varieties with contrasted phenotypes. Some of the traits acquired by cheese strains indicate convergence with other, distantly related fungi used for cheese maturation.
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spelling doaj-art-fb5883041acc4595b99c1c8fbb211cff2025-02-07T10:16:49ZengPeer Community InPeer Community Journal2804-38712023-05-01310.24072/pcjournal.26610.24072/pcjournal.266Domestication of different varieties in the cheese-making fungus Geotrichum candidum Bennetot, Bastien0https://orcid.org/0000-0002-8349-6894Vernadet, Jean-Philippe1Perkins, Vincent2Hautefeuille, Sophie3Rodríguez de la Vega, Ricardo C.4O’Donnell, Samuel5Snirc, Alodie6Grondin, Cécile7Lessard, Marie-Hélène8Peron, Anne-Claire9Labrie, Steve10Landaud, Sophie11Giraud, Tatiana12Ropars, Jeanne13Laboratoire Ecologie Systématique et Evolution, Université Paris-Saclay, CNRS, AgroParisTech, site IDEEV, Gif-sur-Yvette, FranceLaboratoire Ecologie Systématique et Evolution, Université Paris-Saclay, CNRS, AgroParisTech, site IDEEV, Gif-sur-Yvette, FranceDépartement des sciences des aliments, Centre de recherche STELA, INAF, Université Laval, Québec, CanadaLaboratoire Ecologie Systématique et Evolution, Université Paris-Saclay, CNRS, AgroParisTech, site IDEEV, Gif-sur-Yvette, FranceLaboratoire Ecologie Systématique et Evolution, Université Paris-Saclay, CNRS, AgroParisTech, site IDEEV, Gif-sur-Yvette, FranceLaboratoire Ecologie Systématique et Evolution, Université Paris-Saclay, CNRS, AgroParisTech, site IDEEV, Gif-sur-Yvette, FranceLaboratoire Ecologie Systématique et Evolution, Université Paris-Saclay, CNRS, AgroParisTech, site IDEEV, Gif-sur-Yvette, FranceSPO, Univ Montpellier, INRAE, Institut Agro, Montpellier, FranceDépartement des sciences des aliments, Centre de recherche STELA, INAF, Université Laval, Québec, CanadaUMR SayFood, Université Paris-Saclay, INRAe, AgroParisTech, Thiverval Grignon, FranceDépartement des sciences des aliments, Centre de recherche STELA, INAF, Université Laval, Québec, CanadaUMR SayFood, Université Paris-Saclay, INRAe, AgroParisTech, Thiverval Grignon, FranceLaboratoire Ecologie Systématique et Evolution, Université Paris-Saclay, CNRS, AgroParisTech, site IDEEV, Gif-sur-Yvette, FranceLaboratoire Ecologie Systématique et Evolution, Université Paris-Saclay, CNRS, AgroParisTech, site IDEEV, Gif-sur-Yvette, FranceDomestication is an excellent model for studying adaptation processes, involving recent adaptation and diversification, convergence following adaptation to similar conditions, as well as degeneration of unused functions. Geotrichum candidum is a fungus used for cheese making and is also found in other environments such as soil and plants. By analyzing whole-genome data from 98 strains, we found that all strains isolated from cheese formed a monophyletic clade. Within the cheese clade, we identified three genetically differentiated populations and we detected footprints of recombination and admixture. The genetic diversity in the cheese clade was similar as that in the wild clade, suggesting the lack of strong bottlenecks. Commercial starter strains were scattered across the cheese clade, thus not constituting a single clonal lineage. The cheese populations were phenotypically differentiated from other populations, with a slower growth on all media, even cheese, a prominent production of typical cheese volatiles and a lower proteolytic activity. One of the cheese clusters encompassed all soft goat cheese strains, suggesting an effect of cheese-making practices on differentiation. Another of the cheese populations seemed to represent a more advanced stage of domestication, with stronger phenotypic differentiation from the wild clade, harboring much lower genetic diversity, and phenotypes more typical of cheese fungi, with denser and fluffier colonies and a greater ability of excluding cheese spoiler fungi. Cheese populations lacked two beta lactamase-like genes present in the wild clade, involved in xenobiotic clearance, and displayed higher contents of transposable elements, likely due to relaxed selection. Our findings suggest the existence of genuine domestication in G. candidum, which led to diversification into different varieties with contrasted phenotypes. Some of the traits acquired by cheese strains indicate convergence with other, distantly related fungi used for cheese maturation. https://peercommunityjournal.org/articles/10.24072/pcjournal.266/
spellingShingle Bennetot, Bastien
Vernadet, Jean-Philippe
Perkins, Vincent
Hautefeuille, Sophie
Rodríguez de la Vega, Ricardo C.
O’Donnell, Samuel
Snirc, Alodie
Grondin, Cécile
Lessard, Marie-Hélène
Peron, Anne-Claire
Labrie, Steve
Landaud, Sophie
Giraud, Tatiana
Ropars, Jeanne
Domestication of different varieties in the cheese-making fungus Geotrichum candidum
Peer Community Journal
title Domestication of different varieties in the cheese-making fungus Geotrichum candidum
title_full Domestication of different varieties in the cheese-making fungus Geotrichum candidum
title_fullStr Domestication of different varieties in the cheese-making fungus Geotrichum candidum
title_full_unstemmed Domestication of different varieties in the cheese-making fungus Geotrichum candidum
title_short Domestication of different varieties in the cheese-making fungus Geotrichum candidum
title_sort domestication of different varieties in the cheese making fungus geotrichum candidum
url https://peercommunityjournal.org/articles/10.24072/pcjournal.266/
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