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

Summary

This study examined how different populations of the blue cheese fungus Penicillium roqueforti produce varying amounts of toxic and beneficial compounds depending on their environment. Cheese-making strains were found to produce fewer toxins than strains from spoiled food and lumber, likely due to selective breeding for safer products. The research identified specific genetic mutations that prevent cheese strains from producing certain toxins, helping explain why some cheese strains are safer than others.

Background

Penicillium roqueforti is a filamentous fungus that colonizes multiple ecological niches, including cheese production and spoiled food environments. Different populations of this species have undergone varying degrees of domestication and show adaptive differentiation. Understanding metabolite production patterns across populations may elucidate the ecological roles of specialized metabolites.

Objective

To compare metabolite production profiles between five known P. roqueforti populations representing cheese and non-cheese ecological niches using targeted and untargeted metabolomics approaches. To identify genetic mechanisms underlying differences in mycotoxin production between domesticated cheese populations and non-cheese populations.

Results

Metabolite profiles differed significantly between cheese and non-cheese populations, with non-cheese populations producing higher levels of PR toxin, fatty acids, and terpenoids. The non-Roquefort cheese population produced no detectable mycophenolic acid due to a 174 bp deletion in the mpaC gene and lacked PR toxin production due to a premature stop codon in ORF 11. The Termignon population displayed intermediate metabolite profiles consistent with protracted domestication.

Conclusion

Domesticated cheese populations show reduced mycotoxin production potentially due to trait degeneration and relaxed selection in the cheese environment. The maintenance of high metabolite diversity in non-cheese populations suggests these compounds provide bioactive properties important for fitness in diverse ecological niches. Genetic mutations in biosynthetic gene clusters explain some phenotypic differences between populations.
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