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ABSTRACT Fermented foods provide novel ecological opportunities for natural populations of microbes to evolve through successive recolonization of resource-rich substrates. Comparative genomic data have reconstructed the evolutionary histories of microbes adapted to food environments, but experimental studies directly demonstrating the process of domestication are lacking for most fermented food microbes. Here, we show that during adaptation to cheese, phenotypic and metabolomic traits of wild Penicillium molds rapidly change to produce domesticated phenotypes with properties similar to those of the industrial cultures used to make Camembert and other bloomy rind cheeses. Over a period of just a few weeks, populations of wild Penicillium strains serially passaged on cheese had reduced pigment, spore, and mycotoxin production. Domesticated strains also had a striking change in volatile metabolite production, shifting from production of earthy or musty volatile compounds (e.g., geosmin) to fatty and cheesy volatiles (e.g., 2-nonanone, 2-undecanone). RNA sequencing demonstrated a significant decrease in expression of 356 genes in domesticated strains, with an enrichment of many secondary metabolite production pathways in these downregulated genes. By manipulating the presence of neighboring microbial species and overall resource availability, we demonstrate that the limited competition and high nutrient availability of the cheese environment promote rapid trait evolution of Penicillium molds. IMPORTANCE Industrial cultures of filamentous fungi are used to add unique aesthetics and flavors to cheeses and other microbial foods. How these microbes adapted to live in food environments is generally unknown as most microbial domestication is unintentional. Our work demonstrates that wild molds closely related to the starter culture Penicillium camemberti can readily lose traits and quickly shift toward producing desirable aroma compounds. In addition to experimentally demonstrating a putative domestication pathway for P. camemberti , our work suggests that wild Penicillium isolates could be rapidly domesticated to produce new flavors and aesthetics in fermented foods.
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This content will become publicly available on April 10, 2026
Transposable elements facilitate the unintentional domestication of a cheese-associated Penicillium mold
SUMMARY Previous comparative and experimental evolution studies have suggested how fungi may rapidly adapt to new environments, but direct observation ofin situselection in fungal populations is rare due to challenges with tracking populations over human time scales. We monitored a population ofPenicillium solitumover eight years in a cheese cave and documented a phenotypic shift from predominantly green to white strains. Diverse mutations in thealb1gene, which encodes the first protein in the DHN-melanin biosynthesis pathway, explained the green to white shift. A similar phenotypic shift was recapitulated with analb1knockout and experimental evolution in laboratory populations. The most common genetic disruption of thealb1genomic region was caused by putative transposable element insertions upstream of the gene. White strains had substantial downregulation in global transcription, with genetically distinct white strains possessing divergent shifts in expression of different biological processes. White strains outcompeted green strains in co-culture, but this competitive advantage was only observed in the absence of light, suggesting that loss of melanin is only adaptive in dark conditions. Our results illustrate how fermented food production by humans provides opportunities for relaxed selection of key fungal traits over short time scales. Unintentional domestication of microbes by cheesemakers may provide opportunities to generate new strains for innovation in traditional cheese production.
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- Award ID(s):
- 1942063
- PAR ID:
- 10617419
- Publisher / Repository:
- bioRxiv
- Date Published:
- Format(s):
- Medium: X
- Institution:
- bioRxiv
- Sponsoring Org:
- National Science Foundation
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