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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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Fungal volatiles mediate cheese rind microbiome assembly
Summary In vitrostudies in plant, soil, and human systems have shown that microbial volatiles can mediate microbe–microbe or microbe–host interactions. These previous studies have often used artificially high concentrations of volatiles compared toin situsystems and have not demonstrated the roles volatiles play in mediating community‐level dynamics. We used the notoriously volatile cheese rind microbiome to identify bacteria responsive to volatiles produced by five widespread cheese fungi.Vibrio caseihad the strongest growth stimulation when exposed to all fungi. In multispecies community experiments, fungal volatiles caused a shift to aVibrio‐dominated community, potentially explaining the widespread occurrence ofVibrioin surface‐ripened cheeses. RNA sequencing identified activation of the glyoxylate shunt as a possible mechanism underlying volatile‐mediated growth promotion and community assembly. Our study demonstrates how airborne chemicals could be used to control the composition of microbiomes and illustrates how volatiles may impact the development of cheese rinds.
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- Award ID(s):
- 1715553
- PAR ID:
- 10455254
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Environmental Microbiology
- Volume:
- 22
- Issue:
- 11
- ISSN:
- 1462-2912
- Format(s):
- Medium: X Size: p. 4745-4760
- Size(s):
- p. 4745-4760
- Sponsoring Org:
- National Science Foundation
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