Biology subjects

Coton, M.

Publications and source records attributed to Coton, M..

8 recordsLinked to original sources

bioRxiv2026

Cheese adaptation beyond Penicillium: contrasting genomic trajectories in the distantly related Nectriaceae molds

Fungal domestication provides a powerful framework for understanding adaptation to human-made environments, yet genomic studies of cheese-associated fungi have largely focused on Penicillium molds. Here, we investigated cheese-associated Nectriaceae, a phylogenetically distant fungal lineage of ascomycetes, by comparing genomes of nine cheese isolates, belonging to five species, with 22 relatives from other environments. Comparative genomic analyses revealed strikingly contrasting evolutionary trajectories in the two cheese-associated genera. Longinectria showed extensive gene family expansions and duplications, particularly affecting nutrient transport, specialised metabolism and fungal recognition, whereas cheese-associated Bisifusarium exhibited genome reduction and contraction of many of the same functional systems. In Bisifusarium domesticum, these reductions extended to biosynthetic gene clusters, carbohydrate-active enzymes and peptidases, consistent with ecological specialisation. We further identified a 75-kb region with >98% nucleotide identity between two cheese-associated Bisifusarium species, strongly supporting recent horizontal transfer. This region contains several genes involved in ion transport and salt tolerance, including functions previously identified in horizontally transferred regions of cheese-associated Penicillium populations. Together, our results reveal multiple genomic routes to cheese association and highlight gene-family turnover, adaptive protein evolution and horizontal gene transfer as complementary mechanisms shaping fungal evolution in anthropogenic environments.

evolutionary biology↗

bioRxiv2026

A recent domestication event in Penicillium biforme, independent of the emblematic cheese mold P. camemberti

Domestication of molds for cheese production has repeatedly shaped Penicillium fungi, most notably giving rise to the emblematic P. camemberti lineage, derived from P. biforme. Here, we identified a new P. biforme lineage, named cheesy, likely selected from P. biforme for food fermentation, including cheese and sausage production. This lineage exhibits evidence of a severe bottleneck, with little nucleotide polymorphism and a single mating type. The cheesy lineage has evolved advantageous traits for cheesemaking: compared to other P. biforme strains and its wild relative P. fuscoglaucum, it displays faster growth on cheese, galactose and lactose media, higher sporulation and germination rates on cheese, elevated lipolytic activity, enhanced inhibition capacities, and produced specific volatile organic compounds. Additionally, P. camemberti and P. biforme cheesy differ in their content of Starship mobile elements, acquired through horizontal transfers. These elements carry cargo genes potentially relevant for adaptation to cheese. Notably, the cheesy lineage has acquired a 20 kb Starship element (Rattus), nested within a much larger 160 kb Starship (Bilge), and carrying cargo genes with predicted functions involved in antagonistic interactions among micro-organisms. SignificanceO_LIWe identified a new Penicillium biforme lineage, named cheesy, which was likely selected from P. biforme for food fermentation (cheese and sausage), genetically and phenotypically different from the emblematic P. camemberti lineage. This lineage suffered from a severe bottleneck, displaying very little nucleotide polymorphism and a single mating type. C_LIO_LIThis newly identified lineage has evolved advantageous traits for cheesemaking; compared to other P. biforme strains and its wild relative P. fuscoglaucum, it displayed faster growth on cheese, galactose and lactose media, higher sporulation and germination rates on cheese, higher lipolytic activity, better inhibition capacities and specific volatile organic compounds. C_LIO_LIPenicillium camemberti and P. biforme cheesy also differed by their content in Starship mobile elements, acquired through horizontal transfers, and carrying cargo genes potentially relevant for adaptation to cheese. C_LIO_LINotably, the cheesy lineage has acquired a specific 20 kb Starship nested within a much larger 160 kb Starship, and likely involved in antagonistic interactions. C_LI

evolutionary biology↗

bioRxiv2024

Generation of diversity in the blue cheese mold Penicillium roqueforti and identification of pleiotropic QTL for key cheese-making phenotypes

Elucidating the genomic architecture of quantitative traits is essential for our understanding of adaptation and for breeding in domesticated organisms. Penicillium roqueforti is the mold used worldwide for the blue cheese maturation, contributing to flavors through proteolytic and lipolytic activities. The two domesticated cheese populations display very little genetic diversity, but are differentiated and carry opposite mating types. We produced haploid F1 progenies from five crosses, using parents belonging to cheese and non-cheese populations. Analyses of high-quality genome assemblies of the parental strains revealed five large translocations, two having occurred via a circular intermediate. Offspring genotyping with genotype-by-sequencing (GBS) revealed several genomic regions with segregation distortion, possibly linked to degeneration in cheese lineages. We found transgressions for several traits relevant for cheese making, with offspring having more extreme trait values than parental strains. We identified quantitative trait loci (QTLs) for colony color, lipolysis, proteolysis, extrolite production, including mycotoxins, but not for growth rates. Some genomic regions appeared rich in QTLs for both lipid and protein metabolism, and other regions for the production of multiple extrolites, indicating that QTLs have pleiotropic impacts. Some QTLs corresponded to known biosynthetic gene clusters, e.g., for the production of melanin or extrolites. F1 hybrids constitute valuable strains for cheese producers, with new traits and genetic diversity, and allowed identifying target genomic regions for traits important in cheese making, paving the way for strain improvement. The findings further contribute to our understanding of the genetic mechanisms underlying rapid adaptation, revealing convergent adaptation targeting major regulators.

evolutionary biology↗

bioRxiv2024

Different metabolite profiles across Penicillium roqueforti populations associated with ecological niche specialisation and domestication

Fungi are known to produce many chemically diversified metabolites, yet their ecological roles are not always fully understood. The blue cheese making fungus Penicillium roqueforti thrives in different ecological niches and is known to produce a wide range of metabolites, including mycotoxins. Three P. roqueforti populations have been domesticated for cheese production and two populations thrive in other anthropized environments, i.e., spoiled food, lumber and silage. Here, we looked for differences in targeted and untargeted metabolite production profiles between populations using HPLC-HR-Q-TOF and UHPLC-Q-TOF-HR-MS/MS. The non-cheese populations produced several fatty acids and different terpenoids, lacking in cheese strains. The Termignon cheese population displayed intermediate metabolite profiles between cheese and non-cheese populations, as previously shown for other traits. The non-Roquefort population, the cheese population with the strongest domestication syndrome, produced the lowest quantities of measured metabolites, including known mycotoxins such as mycophenolic acid (MPA), andrastin A and PR toxin. Its inability to produce MPA was due to a deletion in the mpaC gene, while a premature stop codon in ORF 11 of the PR toxin gene cluster explained its absence and the accumulation of its eremofortin A & B intermediates. In the Roquefort population, we detected no PR toxin nor eremofortins A or B, but found no indel or frameshift mutation, suggesting downregulation. Our results suggest that domesticated cheese populations were selected for lower toxin production while populations from other anthropized environments maintained high metabolite diversity, the bioactivities of these compounds being likely important in these ecological niches.

microbiology↗

bioRxiv2023

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. 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 Termignon population 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. 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.

microbiology↗

bioRxiv2022

Footprints of domestication in dry-cured meat Penicillium fungi: convergent specific phenotypes and horizontal gene transfers

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 are 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.

evolutionary biology↗

bioRxiv2020

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 levels 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 impacts on cheese-making.

evolutionary biology↗

bioRxiv2018

Independent domestication events in the blue-cheese fungus Penicillium roqueforti

Domestication provides an excellent framework for studying adaptive divergence. Using population genomics and phenotypic assays, we reconstructed the domestication history of the blue cheese mold Penicillium roqueforti. We showed that this fungus was domesticated twice independently. The population used in Roquefort originated from an old domestication event associated with weak bottlenecks and exhibited traits beneficial for pre-industrial cheese production (slower growth in cheese and greater spore production on bread, the traditional multiplication medium). The other cheese population originated more recently from the selection of a single clonal lineage, was associated to all types of blue cheese worldwide but Roquefort, and displayed phenotypes more suited for industrial cheese production (high lipolytic activity, efficient cheese cavity colonization ability and salt tolerance). We detected genomic regions affected by recent positive selection and putative horizontal gene transfers. This study sheds light on the processes of rapid adaptation and raises questions about genetic resource conservation.

evolutionary biology↗