A new cheese population in Penicillium roqueforti and adaptation of the five populations to their ecological niche.

Domestication is an excellent case study for understanding adaptation and multiple fungal lineages have been domesticated for fermenting food products. Studying domestication in fungi has thus both fundamental and applied interest. Genomic studies have revealed the existence of four populations within the blue-cheese-making fungus Penicillium roqueforti. The two cheese populations show footprints of domestication, but the adaptation of the two non-cheese populations to their ecological niches (i.e., silage/spoiled food and lumber/spoiled food) has not been investigated yet. Here, we reveal the existence of a new P. roqueforti population, specific to French Termignon cheeses, produced using small-scale traditional practices, with spontaneous blue mould colonisation. This Termignon population is genetically differentiated from the four previously identified populations, providing a novel source of genetic diversity for cheese making. The Termignon population indeed displayed substantial genetic diversity, both mating types, horizontally transferred regions previously detected in the non-Roquefort population, and intermediate phenotypes between cheese and non-cheese populations. Phenotypically, the non-Roquefort cheese population was the most differentiated, with specific traits beneficial for cheese making, in particular higher tolerance to salt, to acidic pH and to lactic acid. Our results support the view that this clonal population, used for many cheese types in multiple countries, is a domesticated lineage on which humans exerted strong selection. The lumber/spoiled food and silage/spoiled food populations were not more tolerant to crop fungicides but showed faster growth in various carbon sources (e.g., dextrose, pectin, sucrose, xylose and/or lactose), which can be beneficial in their ecological niches. Such contrasted phenotypes between P. roqueforti populations, with beneficial traits for cheese-making in the cheese populations and enhanced ability to metabolise sugars in the lumber/spoiled food population, support the inference of domestication in cheese fungi and more generally of adaptation to anthropized environments.

Strong effect of Penicillium roqueforti populations on volatile and metabolic compounds responsible for aromas, flavor and texture in blue cheeses.

Studies of food microorganism domestication can provide important insight into adaptation mechanisms and lead to commercial applications. Penicillium roqueforti is a fungus with four genetically differentiated populations, two of which were independently domesticated for blue cheese-making, with the other two populations thriving in other environments. Most blue cheeses are made with strains from a single P. roqueforti population, whereas Roquefort cheeses are inoculated with strains from a second population. We made blue cheeses in accordance with the production specifications for Roquefort-type cheeses, inoculating each cheese with a single P. roqueforti strain, using a total of three strains from each of the four populations. We investigated differences between the cheeses made with the strains from the four P. roqueforti populations, in terms of the induced flora, the proportion of blue color, water activity and the identity and abundance of aqueous and organic metabolites as proxies for proteolysis and lipolysis as well as volatile compounds responsible for flavor and aroma. We found that the population-of-origin of the P. roqueforti strains used for inoculation had a minor impact on bacterial diversity and no effect on the abundance of the main microorganism. The cheeses produced with P. roqueforti strains from cheese populations had a higher percentage of blue area and a higher abundance of the volatile compounds typical of blue cheeses, such as methyl ketones and secondary alcohols. In particular, the Roquefort strains produced higher amounts of these aromatic compounds, partly due to more efficient proteolysis and lipolysis. The Roquefort strains also led to cheeses with a lower water availability, an important feature for preventing spoilage in blue cheeses, which is subject to controls for the sale of Roquefort cheese. The typical appearance and flavors of blue cheeses thus result from human selection on P. roqueforti, leading to the acquisition of specific features by the two cheese populations. These findings have important implications for our understanding of adaptation and domestication, and for cheese improvement.

[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.

Differential retention of transposable element-derived sequences in outcrossing Arabidopsis genomes.

BACKGROUND: Transposable elements (TEs) are genomic parasites with major impacts on host genome architecture and host adaptation. A proper evaluation of their evolutionary significance has been hampered by the paucity of short scale phylogenetic comparisons between closely related species. Here, we characterized the dynamics of TE accumulation at the micro-evolutionary scale by comparing two closely related plant species, Arabidopsis lyrata and A. halleri. RESULTS: Joint genome annotation in these two outcrossing species confirmed that both contain two distinct populations of TEs with either 'recent' or 'old' insertion histories. Identification of rare segregating insertions suggests that diverse TE families contribute to the ongoing dynamics of TE accumulation in the two species. Orthologous TE fragments (i.e. those that have been maintained in both species), tend to be located closer to genes than those that are retained in one species only. Compared to non-orthologous TE insertions, those that are orthologous tend to produce fewer short interfering RNAs, are less heavily methylated when found within or adjacent to genes and these tend to have lower expression levels. These findings suggest that long-term retention of TE insertions reflects their frequent acquisition of adaptive roles and/or the deleterious effects of removing nearly neutral TE insertions when they are close to genes. CONCLUSION: Our results indicate a rapid evolutionary dynamics of the TE landscape in these two outcrossing species, with an important input of a diverse set of new insertions with variable propensity to resist deletion.