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Comparative genomics of the genus Roseburia reveals divergent biosynthetic pathways that may influence colonic competition among species

Roseburia species are important denizens of the human gut microbiome that ferment complex polysaccharides to butyrate as a terminal fermentation product, which influences human physiology and serves as an energy source for colonocytes. Previous comparative genomics analyses of the genus Roseburia ha...

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Autores principales: Hillman, Ethan T., Kozik, Ariangela J., Hooker, Casey A., Burnett, John L., Heo, Yoojung, Kiesel, Violet A., Nevins, Clayton J., Oshiro, Jordan M.K.I., Robins, Melissa M., Thakkar, Riya D., Wu, Sophie Tongyu, Lindemann, Stephen R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Microbiology Society 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7478625/
https://www.ncbi.nlm.nih.gov/pubmed/32589566
http://dx.doi.org/10.1099/mgen.0.000399
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author Hillman, Ethan T.
Kozik, Ariangela J.
Hooker, Casey A.
Burnett, John L.
Heo, Yoojung
Kiesel, Violet A.
Nevins, Clayton J.
Oshiro, Jordan M.K.I.
Robins, Melissa M.
Thakkar, Riya D.
Wu, Sophie Tongyu
Lindemann, Stephen R.
author_facet Hillman, Ethan T.
Kozik, Ariangela J.
Hooker, Casey A.
Burnett, John L.
Heo, Yoojung
Kiesel, Violet A.
Nevins, Clayton J.
Oshiro, Jordan M.K.I.
Robins, Melissa M.
Thakkar, Riya D.
Wu, Sophie Tongyu
Lindemann, Stephen R.
author_sort Hillman, Ethan T.
collection PubMed
description Roseburia species are important denizens of the human gut microbiome that ferment complex polysaccharides to butyrate as a terminal fermentation product, which influences human physiology and serves as an energy source for colonocytes. Previous comparative genomics analyses of the genus Roseburia have examined polysaccharide degradation genes. Here, we characterize the core and pangenomes of the genus Roseburia with respect to central carbon and energy metabolism, as well as biosynthesis of amino acids and B vitamins using orthology-based methods, uncovering significant differences among species in their biosynthetic capacities. Variation in gene content among Roseburia species and strains was most significant for cofactor biosynthesis. Unlike all other species of Roseburia that we analysed, Roseburia inulinivorans strains lacked biosynthetic genes for riboflavin or pantothenate but possessed folate biosynthesis genes. Differences in gene content for B vitamin synthesis were matched with differences in putative salvage and synthesis strategies among species. For example, we observed extended biotin salvage capabilities in R. intestinalis strains, which further suggest that B vitamin acquisition strategies may impact fitness in the gut ecosystem. As differences in the functional potential to synthesize components of biomass (e.g. amino acids, vitamins) can drive interspecies interactions, variation in auxotrophies of the Roseburia spp. genomes may influence in vivo gut ecology. This study serves to advance our understanding of the potential metabolic interactions that influence the ecology of Roseburia spp. and, ultimately, may provide a basis for rational strategies to manipulate the abundances of these species.
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spelling pubmed-74786252020-09-09 Comparative genomics of the genus Roseburia reveals divergent biosynthetic pathways that may influence colonic competition among species Hillman, Ethan T. Kozik, Ariangela J. Hooker, Casey A. Burnett, John L. Heo, Yoojung Kiesel, Violet A. Nevins, Clayton J. Oshiro, Jordan M.K.I. Robins, Melissa M. Thakkar, Riya D. Wu, Sophie Tongyu Lindemann, Stephen R. Microb Genom Research Article Roseburia species are important denizens of the human gut microbiome that ferment complex polysaccharides to butyrate as a terminal fermentation product, which influences human physiology and serves as an energy source for colonocytes. Previous comparative genomics analyses of the genus Roseburia have examined polysaccharide degradation genes. Here, we characterize the core and pangenomes of the genus Roseburia with respect to central carbon and energy metabolism, as well as biosynthesis of amino acids and B vitamins using orthology-based methods, uncovering significant differences among species in their biosynthetic capacities. Variation in gene content among Roseburia species and strains was most significant for cofactor biosynthesis. Unlike all other species of Roseburia that we analysed, Roseburia inulinivorans strains lacked biosynthetic genes for riboflavin or pantothenate but possessed folate biosynthesis genes. Differences in gene content for B vitamin synthesis were matched with differences in putative salvage and synthesis strategies among species. For example, we observed extended biotin salvage capabilities in R. intestinalis strains, which further suggest that B vitamin acquisition strategies may impact fitness in the gut ecosystem. As differences in the functional potential to synthesize components of biomass (e.g. amino acids, vitamins) can drive interspecies interactions, variation in auxotrophies of the Roseburia spp. genomes may influence in vivo gut ecology. This study serves to advance our understanding of the potential metabolic interactions that influence the ecology of Roseburia spp. and, ultimately, may provide a basis for rational strategies to manipulate the abundances of these species. Microbiology Society 2020-06-26 /pmc/articles/PMC7478625/ /pubmed/32589566 http://dx.doi.org/10.1099/mgen.0.000399 Text en © 2020 The Authors http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License.
spellingShingle Research Article
Hillman, Ethan T.
Kozik, Ariangela J.
Hooker, Casey A.
Burnett, John L.
Heo, Yoojung
Kiesel, Violet A.
Nevins, Clayton J.
Oshiro, Jordan M.K.I.
Robins, Melissa M.
Thakkar, Riya D.
Wu, Sophie Tongyu
Lindemann, Stephen R.
Comparative genomics of the genus Roseburia reveals divergent biosynthetic pathways that may influence colonic competition among species
title Comparative genomics of the genus Roseburia reveals divergent biosynthetic pathways that may influence colonic competition among species
title_full Comparative genomics of the genus Roseburia reveals divergent biosynthetic pathways that may influence colonic competition among species
title_fullStr Comparative genomics of the genus Roseburia reveals divergent biosynthetic pathways that may influence colonic competition among species
title_full_unstemmed Comparative genomics of the genus Roseburia reveals divergent biosynthetic pathways that may influence colonic competition among species
title_short Comparative genomics of the genus Roseburia reveals divergent biosynthetic pathways that may influence colonic competition among species
title_sort comparative genomics of the genus roseburia reveals divergent biosynthetic pathways that may influence colonic competition among species
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7478625/
https://www.ncbi.nlm.nih.gov/pubmed/32589566
http://dx.doi.org/10.1099/mgen.0.000399
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