Rapid Phenotypic and Metabolomic Domestication of Wild <italic toggle="yes">Penicillium</italic> 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 experiment...

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Autores principales:	Ina Bodinaku, Jason Shaffer, Allison B. Connors, Jacob L. Steenwyk, Megan N. Biango-Daniels, Erik K. Kastman, Antonis Rokas, Albert Robbat, Benjamin E. Wolfe
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Penicillium cheese evolution mycotoxins secondary metabolism transcriptome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/bab4d765bffe4fff973fe33cf46619c8
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spelling	oai:doaj.org-article:bab4d765bffe4fff973fe33cf46619c82021-11-15T15:59:41ZRapid Phenotypic and Metabolomic Domestication of Wild <italic toggle="yes">Penicillium</italic> Molds on Cheese10.1128/mBio.02445-192150-7511https://doaj.org/article/bab4d765bffe4fff973fe33cf46619c82019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02445-19https://doaj.org/toc/2150-7511ABSTRACT 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.Ina BodinakuJason ShafferAllison B. ConnorsJacob L. SteenwykMegan N. Biango-DanielsErik K. KastmanAntonis RokasAlbert RobbatBenjamin E. WolfeAmerican Society for MicrobiologyarticlePenicilliumcheeseevolutionmycotoxinssecondary metabolismtranscriptomeMicrobiologyQR1-502ENmBio, Vol 10, Iss 5 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Penicillium cheese evolution mycotoxins secondary metabolism transcriptome Microbiology QR1-502
spellingShingle	Penicillium cheese evolution mycotoxins secondary metabolism transcriptome Microbiology QR1-502 Ina Bodinaku Jason Shaffer Allison B. Connors Jacob L. Steenwyk Megan N. Biango-Daniels Erik K. Kastman Antonis Rokas Albert Robbat Benjamin E. Wolfe Rapid Phenotypic and Metabolomic Domestication of Wild <italic toggle="yes">Penicillium</italic> Molds on Cheese
description	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.
format	article
author	Ina Bodinaku Jason Shaffer Allison B. Connors Jacob L. Steenwyk Megan N. Biango-Daniels Erik K. Kastman Antonis Rokas Albert Robbat Benjamin E. Wolfe
author_facet	Ina Bodinaku Jason Shaffer Allison B. Connors Jacob L. Steenwyk Megan N. Biango-Daniels Erik K. Kastman Antonis Rokas Albert Robbat Benjamin E. Wolfe
author_sort	Ina Bodinaku
title	Rapid Phenotypic and Metabolomic Domestication of Wild <italic toggle="yes">Penicillium</italic> Molds on Cheese
title_short	Rapid Phenotypic and Metabolomic Domestication of Wild <italic toggle="yes">Penicillium</italic> Molds on Cheese
title_full	Rapid Phenotypic and Metabolomic Domestication of Wild <italic toggle="yes">Penicillium</italic> Molds on Cheese
title_fullStr	Rapid Phenotypic and Metabolomic Domestication of Wild <italic toggle="yes">Penicillium</italic> Molds on Cheese
title_full_unstemmed	Rapid Phenotypic and Metabolomic Domestication of Wild <italic toggle="yes">Penicillium</italic> Molds on Cheese
title_sort	rapid phenotypic and metabolomic domestication of wild <italic toggle="yes">penicillium</italic> molds on cheese
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/bab4d765bffe4fff973fe33cf46619c8
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Rapid Phenotypic and Metabolomic Domestication of Wild <italic toggle="yes">Penicillium</italic> Molds on Cheese

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