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Deciphering functional redundancy in the human microbiome

Although the taxonomic composition of the human microbiome varies tremendously across individuals, its gene composition or functional capacity is highly conserved — implying an ecological property known as functional redundancy. Such functional redundancy has been hypothesized to underlie the stabil...

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Autores principales: Tian, Liang, Wang, Xu-Wen, Wu, Ang-Kun, Fan, Yuhang, Friedman, Jonathan, Dahlin, Amber, Waldor, Matthew K., Weinstock, George M., Weiss, Scott T., Liu, Yang-Yu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7719190/
https://www.ncbi.nlm.nih.gov/pubmed/33277504
http://dx.doi.org/10.1038/s41467-020-19940-1
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author Tian, Liang
Wang, Xu-Wen
Wu, Ang-Kun
Fan, Yuhang
Friedman, Jonathan
Dahlin, Amber
Waldor, Matthew K.
Weinstock, George M.
Weiss, Scott T.
Liu, Yang-Yu
author_facet Tian, Liang
Wang, Xu-Wen
Wu, Ang-Kun
Fan, Yuhang
Friedman, Jonathan
Dahlin, Amber
Waldor, Matthew K.
Weinstock, George M.
Weiss, Scott T.
Liu, Yang-Yu
author_sort Tian, Liang
collection PubMed
description Although the taxonomic composition of the human microbiome varies tremendously across individuals, its gene composition or functional capacity is highly conserved — implying an ecological property known as functional redundancy. Such functional redundancy has been hypothesized to underlie the stability and resilience of the human microbiome, but this hypothesis has never been quantitatively tested. The origin of functional redundancy is still elusive. Here, we investigate the basis for functional redundancy in the human microbiome by analyzing its genomic content network — a bipartite graph that links microbes to the genes in their genomes. We find that this network exhibits several topological features that favor high functional redundancy. Furthermore, we develop a simple genome evolution model to generate genomic content network, finding that moderate selection pressure and high horizontal gene transfer rate are necessary to generate genomic content networks with key topological features that favor high functional redundancy. Finally, we analyze data from two published studies of fecal microbiota transplantation (FMT), finding that high functional redundancy of the recipient’s pre-FMT microbiota raises barriers to donor microbiota engraftment. This work elucidates the potential ecological and evolutionary processes that create and maintain functional redundancy in the human microbiome and contribute to its resilience.
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spelling pubmed-77191902020-12-11 Deciphering functional redundancy in the human microbiome Tian, Liang Wang, Xu-Wen Wu, Ang-Kun Fan, Yuhang Friedman, Jonathan Dahlin, Amber Waldor, Matthew K. Weinstock, George M. Weiss, Scott T. Liu, Yang-Yu Nat Commun Article Although the taxonomic composition of the human microbiome varies tremendously across individuals, its gene composition or functional capacity is highly conserved — implying an ecological property known as functional redundancy. Such functional redundancy has been hypothesized to underlie the stability and resilience of the human microbiome, but this hypothesis has never been quantitatively tested. The origin of functional redundancy is still elusive. Here, we investigate the basis for functional redundancy in the human microbiome by analyzing its genomic content network — a bipartite graph that links microbes to the genes in their genomes. We find that this network exhibits several topological features that favor high functional redundancy. Furthermore, we develop a simple genome evolution model to generate genomic content network, finding that moderate selection pressure and high horizontal gene transfer rate are necessary to generate genomic content networks with key topological features that favor high functional redundancy. Finally, we analyze data from two published studies of fecal microbiota transplantation (FMT), finding that high functional redundancy of the recipient’s pre-FMT microbiota raises barriers to donor microbiota engraftment. This work elucidates the potential ecological and evolutionary processes that create and maintain functional redundancy in the human microbiome and contribute to its resilience. Nature Publishing Group UK 2020-12-04 /pmc/articles/PMC7719190/ /pubmed/33277504 http://dx.doi.org/10.1038/s41467-020-19940-1 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Tian, Liang
Wang, Xu-Wen
Wu, Ang-Kun
Fan, Yuhang
Friedman, Jonathan
Dahlin, Amber
Waldor, Matthew K.
Weinstock, George M.
Weiss, Scott T.
Liu, Yang-Yu
Deciphering functional redundancy in the human microbiome
title Deciphering functional redundancy in the human microbiome
title_full Deciphering functional redundancy in the human microbiome
title_fullStr Deciphering functional redundancy in the human microbiome
title_full_unstemmed Deciphering functional redundancy in the human microbiome
title_short Deciphering functional redundancy in the human microbiome
title_sort deciphering functional redundancy in the human microbiome
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7719190/
https://www.ncbi.nlm.nih.gov/pubmed/33277504
http://dx.doi.org/10.1038/s41467-020-19940-1
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