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Strain-Level Diversity Impacts Cheese Rind Microbiome Assembly and Function

Diversification can generate genomic and phenotypic strain-level diversity within microbial species. This microdiversity is widely recognized in populations, but the community-level consequences of microbial strain-level diversity are poorly characterized. Using the cheese rind model system, we test...

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Autores principales: Niccum, Brittany A., Kastman, Erik K., Kfoury, Nicole, Robbat, Albert, Wolfe, Benjamin E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7300356/
https://www.ncbi.nlm.nih.gov/pubmed/32546667
http://dx.doi.org/10.1128/mSystems.00149-20
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author Niccum, Brittany A.
Kastman, Erik K.
Kfoury, Nicole
Robbat, Albert
Wolfe, Benjamin E.
author_facet Niccum, Brittany A.
Kastman, Erik K.
Kfoury, Nicole
Robbat, Albert
Wolfe, Benjamin E.
author_sort Niccum, Brittany A.
collection PubMed
description Diversification can generate genomic and phenotypic strain-level diversity within microbial species. This microdiversity is widely recognized in populations, but the community-level consequences of microbial strain-level diversity are poorly characterized. Using the cheese rind model system, we tested whether strain diversity across microbiomes from distinct geographic regions impacts assembly dynamics and functional outputs. We first isolated the same three bacterial species (Staphylococcus equorum, Brevibacterium auranticum, and Brachybacterium alimentarium) from nine cheeses produced in different regions of the United States and Europe to construct nine synthetic microbial communities consisting of distinct strains of the same three bacterial species. Comparative genomics identified distinct phylogenetic clusters and significant variation in genome content across the nine synthetic communities. When we assembled each synthetic community with initially identical compositions, community structure diverged over time, resulting in communities with different dominant taxa. The taxonomically identical communities showed differing responses to abiotic (high salt) and biotic (the fungus Penicillium) perturbations, with some communities showing no response and others substantially shifting in composition. Functional differences were also observed across the nine communities, with significant variation in pigment production (light yellow to orange) and in composition of volatile organic compound profiles emitted from the rinds (nutty to sulfury). IMPORTANCE Our work demonstrated that the specific microbial strains used to construct a microbiome could impact the species composition, perturbation responses, and functional outputs of that system. These findings suggest that 16S rRNA gene taxonomic profiles alone may have limited potential to predict the dynamics of microbial communities because they usually do not capture strain-level diversity. Observations from our synthetic communities also suggest that strain-level diversity has the potential to drive variability in the aesthetics and quality of surface-ripened cheeses.
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spelling pubmed-73003562020-06-25 Strain-Level Diversity Impacts Cheese Rind Microbiome Assembly and Function Niccum, Brittany A. Kastman, Erik K. Kfoury, Nicole Robbat, Albert Wolfe, Benjamin E. mSystems Research Article Diversification can generate genomic and phenotypic strain-level diversity within microbial species. This microdiversity is widely recognized in populations, but the community-level consequences of microbial strain-level diversity are poorly characterized. Using the cheese rind model system, we tested whether strain diversity across microbiomes from distinct geographic regions impacts assembly dynamics and functional outputs. We first isolated the same three bacterial species (Staphylococcus equorum, Brevibacterium auranticum, and Brachybacterium alimentarium) from nine cheeses produced in different regions of the United States and Europe to construct nine synthetic microbial communities consisting of distinct strains of the same three bacterial species. Comparative genomics identified distinct phylogenetic clusters and significant variation in genome content across the nine synthetic communities. When we assembled each synthetic community with initially identical compositions, community structure diverged over time, resulting in communities with different dominant taxa. The taxonomically identical communities showed differing responses to abiotic (high salt) and biotic (the fungus Penicillium) perturbations, with some communities showing no response and others substantially shifting in composition. Functional differences were also observed across the nine communities, with significant variation in pigment production (light yellow to orange) and in composition of volatile organic compound profiles emitted from the rinds (nutty to sulfury). IMPORTANCE Our work demonstrated that the specific microbial strains used to construct a microbiome could impact the species composition, perturbation responses, and functional outputs of that system. These findings suggest that 16S rRNA gene taxonomic profiles alone may have limited potential to predict the dynamics of microbial communities because they usually do not capture strain-level diversity. Observations from our synthetic communities also suggest that strain-level diversity has the potential to drive variability in the aesthetics and quality of surface-ripened cheeses. American Society for Microbiology 2020-06-16 /pmc/articles/PMC7300356/ /pubmed/32546667 http://dx.doi.org/10.1128/mSystems.00149-20 Text en Copyright © 2020 Niccum et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Niccum, Brittany A.
Kastman, Erik K.
Kfoury, Nicole
Robbat, Albert
Wolfe, Benjamin E.
Strain-Level Diversity Impacts Cheese Rind Microbiome Assembly and Function
title Strain-Level Diversity Impacts Cheese Rind Microbiome Assembly and Function
title_full Strain-Level Diversity Impacts Cheese Rind Microbiome Assembly and Function
title_fullStr Strain-Level Diversity Impacts Cheese Rind Microbiome Assembly and Function
title_full_unstemmed Strain-Level Diversity Impacts Cheese Rind Microbiome Assembly and Function
title_short Strain-Level Diversity Impacts Cheese Rind Microbiome Assembly and Function
title_sort strain-level diversity impacts cheese rind microbiome assembly and function
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7300356/
https://www.ncbi.nlm.nih.gov/pubmed/32546667
http://dx.doi.org/10.1128/mSystems.00149-20
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