Dataset Information

Rapid Phenotypic and Metabolomic Domestication of Wild Penicillium Molds on Cheese.

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.

SUBMITTER: Bodinaku I

PROVIDER: S-EPMC6794487 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Publications

Rapid Phenotypic and Metabolomic Domestication of Wild <i>Penicillium</i> Molds on Cheese.

Bodinaku Ina I Shaffer Jason J Connors Allison B AB Steenwyk Jacob L JL Biango-Daniels Megan N MN Kastman Erik K EK Rokas Antonis A Robbat Albert A Wolfe Benjamin E BE

mBio 20191015 5

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 <i>Penicil ...[more]

PMID: 31615965

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Project description:The observation that Penicillium molds can inhibit the growth of Staphylococcus was a catalyst for the antibiotic revolution. Considerable attention has been paid to purified Penicillium metabolites that inhibit bacteria, but little is known about how Penicillium species impact the ecology and evolution of bacteria in multispecies microbial communities. Here, we investigated how four different species of Penicillium can impact global transcription and evolution of a widespread Staphylococcus species (S. equorum) using the cheese rind model microbiome. Through RNA sequencing, we identified a core transcriptional response of S. equorum against all five tested Penicillium strains, including upregulation of thiamine biosynthesis, fatty acid degradation, and amino acid metabolism as well as downregulation of genes involved in the transport of siderophores. In a 12-week evolution experiment where we co-cultured S. equorum with the same Penicillium strains, we observed surprisingly few non-synonymous mutations across S. equorum populations evolved with the Penicillium species. A mutation in a putative DHH family phosphoesterase gene only occurred in populations evolved without Penicillium and decreased the fitness of S. equorum when co-cultured with an antagonistic Penicillium strain. Our results highlight the potential for conserved mechanisms of Staphylococcus-Penicillium interactions and demonstrate how fungal biotic environments may constrain the evolution of bacterial species.IMPORTANCEFungi and bacteria are commonly found co-occurring both in natural and synthetic microbiomes, but our understanding of fungal-bacterial interactions is limited to a handful of species. Conserved mechanisms of interactions and evolutionary consequences of fungal-bacterial interactions are largely unknown. Our RNA sequencing and experimental evolution data with Penicillium species and the bacterium S. equorum demonstrate that divergent fungal species can elicit conserved transcriptional and genomic responses in co-occurring bacteria. Penicillium molds are integral to the discovery of novel antibiotics and production of certain foods. By understanding how Penicillium species affect bacteria, our work can further efforts to design and manage Penicillium-dominated microbial communities in industry and food production.

Dataset Information

Rapid Phenotypic and Metabolomic Domestication of Wild Penicillium Molds on Cheese.

Publications

Rapid Phenotypic and Metabolomic Domestication of Wild <i>Penicillium</i> Molds on Cheese.

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