[The domestication of Penicillium cheese fungi]. / La domestication des champignons Penicillium du fromage.

Domestication is the process of organism evolution under selection by humans, and as such has been a model for studying adaptation since Charles Darwin. Here we review recent studies on the genomics of adaptation and domestication syndrome in two cheese-making fungal lineages, Penicillium roqueforti used for maturing blue cheeses, and the Penicillium camemberti species complex used for making soft cheeses such as Camembert and Brie. Comparative genomics have revealed horizontal gene transfers involved in convergent adaptation to cheese. Population genomics have identified differentiated populations with contrasted traits, several populations having independently been domesticated for cheese making in both P. roqueforti and the Penicillium camemberti species complex, and having undergone bottlenecks. The different cheese populations have acquired traits beneficial for cheese making in comparison to non-cheese populations, regarding color, spore production, growth rates on cheese, salt tolerance, lipolysis, proteolysis, volatile compound or toxin production and/or competitive ability. The cheese populations also show degeneration for some unused functions such as decreased ability of sexual reproduction or of growth under harsh conditions. These recent findings have fundamental importance for our understanding of adaptation and have applied interest for strain improvement.

La domestication est le processus d'évolution d'un organisme en cours de sélection par l'homme et, à ce titre, elle a servi de modèle pour l'étude de l'adaptation depuis Charles Darwin. Nous passons ici en revue les études récentes sur la génomique de l'adaptation et le syndrome de domestication dans deux lignées de champignons fromagers, Penicillium roqueforti utilisé pour l'affinage des fromages bleus, et le complexe d'espèces Penicillium camemberti utilisé pour la fabrication de fromages à pâte molle comme le camembert et le brie. La génomique comparative a révélé des transferts de gènes horizontaux impliqués dans l'adaptation convergente du fromage. La génomique des populations a identifié des populations différenciées aux caractères contrastés, plusieurs populations ayant été indépendamment domestiquées pour la fabrication de fromage à la fois chez P. roqueforti et le complexe d'espèces Penicillium camemberti, et ayant subi de forts goulots d'étranglement. Les différentes populations fromagères ont acquis des caractères avantageux pour la fabrication du fromage par rapport aux populations non fromagères, en ce qui concerne la couleur, la production de spores, les taux de croissance sur le fromage, la tolérance au sel, la lipolyse, la protéolyse, la production de composés volatils ou de toxines et/ou la capacité d'exclusion compétitive. Les populations fromagères présentent également une dégénérescence de certaines fonctions non utilisées, telles que la capacité réduite de reproduction sexuée ou de croissance dans des conditions difficiles. Ces récentes découvertes ont une importance fondamentale pour notre compréhension de l'adaptation et ont un intérêt appliqué pour l'amélioration des souches.

Domestication of the Emblematic White Cheese-Making Fungus Penicillium camemberti and Its Diversification into Two Varieties.

Domestication involves recent adaptation under strong human selection and rapid diversification and therefore constitutes a good model for studies of these processes. We studied the domestication of the emblematic white mold Penicillium camemberti, used for the maturation of soft cheeses, such as Camembert and Brie, about which surprisingly little was known, despite its economic and cultural importance. Whole-genome-based analyses of genetic relationships and diversity revealed that an ancient domestication event led to the emergence of the gray-green P. biforme mold used in cheese making, by divergence from the blue-green wild P. fuscoglaucum fungus. Another much more recent domestication event led to the generation of the P. camemberti clonal lineage as a sister group to P. biforme. Penicillium biforme displayed signs of phenotypic adaptation to cheese making relative to P. fuscoglaucum, in terms of whiter color, faster growth on cheese medium under cave conditions, lower amounts of toxin production, and greater ability to prevent the growth of other fungi. The P. camemberti lineage displayed even stronger signs of domestication for all these phenotypic features. We also identified two differentiated P. camemberti varieties, apparently associated with different kinds of cheeses and with contrasted phenotypic features in terms of color, growth, toxin production, and competitive ability. We have thus identified footprints of domestication in these fungi, with genetic differentiation between cheese and wild populations, bottlenecks, and specific phenotypic traits beneficial for cheese making. This study has not only fundamental implications for our understanding of domestication but can also have important effects on cheese making.

A Behavior-Manipulating Virus Relative as a Source of Adaptive Genes for Drosophila Parasitoids.

Some species of parasitic wasps have domesticated viral machineries to deliver immunosuppressive factors to their hosts. Up to now, all described cases fall into the Ichneumonoidea superfamily, which only represents around 10% of hymenoptera diversity, raising the question of whether such domestication occurred outside this clade. Furthermore, the biology of the ancestral donor viruses is completely unknown. Since the 1980s, we know that Drosophila parasitoids belonging to the Leptopilina genus, which diverged from the Ichneumonoidea superfamily 225 Ma, do produce immunosuppressive virus-like structure in their reproductive apparatus. However, the viral origin of these structures has been the subject of debate. In this article, we provide genomic and experimental evidence that those structures do derive from an ancestral virus endogenization event. Interestingly, its close relatives induce a behavior manipulation in present-day wasps. Thus, we conclude that virus domestication is more prevalent than previously thought and that behavior manipulation may have been instrumental in the birth of such associations.