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Microbial genomes from non-human primate gut metagenomes expand the primate-associated bacterial tree of life with over 1000 novel species

BACKGROUND: Humans have coevolved with microbial communities to establish a mutually advantageous relationship that is still poorly characterized and can provide a better understanding of the human microbiome. Comparative metagenomic analysis of human and non-human primate (NHP) microbiomes offers a...

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Autores principales: Manara, Serena, Asnicar, Francesco, Beghini, Francesco, Bazzani, Davide, Cumbo, Fabio, Zolfo, Moreno, Nigro, Eleonora, Karcher, Nicolai, Manghi, Paolo, Metzger, Marisa Isabell, Pasolli, Edoardo, Segata, Nicola
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6935492/
https://www.ncbi.nlm.nih.gov/pubmed/31883524
http://dx.doi.org/10.1186/s13059-019-1923-9
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author Manara, Serena
Asnicar, Francesco
Beghini, Francesco
Bazzani, Davide
Cumbo, Fabio
Zolfo, Moreno
Nigro, Eleonora
Karcher, Nicolai
Manghi, Paolo
Metzger, Marisa Isabell
Pasolli, Edoardo
Segata, Nicola
author_facet Manara, Serena
Asnicar, Francesco
Beghini, Francesco
Bazzani, Davide
Cumbo, Fabio
Zolfo, Moreno
Nigro, Eleonora
Karcher, Nicolai
Manghi, Paolo
Metzger, Marisa Isabell
Pasolli, Edoardo
Segata, Nicola
author_sort Manara, Serena
collection PubMed
description BACKGROUND: Humans have coevolved with microbial communities to establish a mutually advantageous relationship that is still poorly characterized and can provide a better understanding of the human microbiome. Comparative metagenomic analysis of human and non-human primate (NHP) microbiomes offers a promising approach to study this symbiosis. Very few microbial species have been characterized in NHP microbiomes due to their poor representation in the available cataloged microbial diversity, thus limiting the potential of such comparative approaches. RESULTS: We reconstruct over 1000 previously uncharacterized microbial species from 6 available NHP metagenomic cohorts, resulting in an increase of the mappable fraction of metagenomic reads by 600%. These novel species highlight that almost 90% of the microbial diversity associated with NHPs has been overlooked. Comparative analysis of this new catalog of taxa with the collection of over 150,000 genomes from human metagenomes points at a limited species-level overlap, with only 20% of microbial candidate species in NHPs also found in the human microbiome. This overlap occurs mainly between NHPs and non-Westernized human populations and NHPs living in captivity, suggesting that host lifestyle plays a role comparable to host speciation in shaping the primate intestinal microbiome. Several NHP-specific species are phylogenetically related to human-associated microbes, such as Elusimicrobia and Treponema, and could be the consequence of host-dependent evolutionary trajectories. CONCLUSIONS: The newly reconstructed species greatly expand the microbial diversity associated with NHPs, thus enabling better interrogation of the primate microbiome and empowering in-depth human and non-human comparative and co-diversification studies.
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spelling pubmed-69354922019-12-30 Microbial genomes from non-human primate gut metagenomes expand the primate-associated bacterial tree of life with over 1000 novel species Manara, Serena Asnicar, Francesco Beghini, Francesco Bazzani, Davide Cumbo, Fabio Zolfo, Moreno Nigro, Eleonora Karcher, Nicolai Manghi, Paolo Metzger, Marisa Isabell Pasolli, Edoardo Segata, Nicola Genome Biol Research BACKGROUND: Humans have coevolved with microbial communities to establish a mutually advantageous relationship that is still poorly characterized and can provide a better understanding of the human microbiome. Comparative metagenomic analysis of human and non-human primate (NHP) microbiomes offers a promising approach to study this symbiosis. Very few microbial species have been characterized in NHP microbiomes due to their poor representation in the available cataloged microbial diversity, thus limiting the potential of such comparative approaches. RESULTS: We reconstruct over 1000 previously uncharacterized microbial species from 6 available NHP metagenomic cohorts, resulting in an increase of the mappable fraction of metagenomic reads by 600%. These novel species highlight that almost 90% of the microbial diversity associated with NHPs has been overlooked. Comparative analysis of this new catalog of taxa with the collection of over 150,000 genomes from human metagenomes points at a limited species-level overlap, with only 20% of microbial candidate species in NHPs also found in the human microbiome. This overlap occurs mainly between NHPs and non-Westernized human populations and NHPs living in captivity, suggesting that host lifestyle plays a role comparable to host speciation in shaping the primate intestinal microbiome. Several NHP-specific species are phylogenetically related to human-associated microbes, such as Elusimicrobia and Treponema, and could be the consequence of host-dependent evolutionary trajectories. CONCLUSIONS: The newly reconstructed species greatly expand the microbial diversity associated with NHPs, thus enabling better interrogation of the primate microbiome and empowering in-depth human and non-human comparative and co-diversification studies. BioMed Central 2019-12-28 /pmc/articles/PMC6935492/ /pubmed/31883524 http://dx.doi.org/10.1186/s13059-019-1923-9 Text en © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Manara, Serena
Asnicar, Francesco
Beghini, Francesco
Bazzani, Davide
Cumbo, Fabio
Zolfo, Moreno
Nigro, Eleonora
Karcher, Nicolai
Manghi, Paolo
Metzger, Marisa Isabell
Pasolli, Edoardo
Segata, Nicola
Microbial genomes from non-human primate gut metagenomes expand the primate-associated bacterial tree of life with over 1000 novel species
title Microbial genomes from non-human primate gut metagenomes expand the primate-associated bacterial tree of life with over 1000 novel species
title_full Microbial genomes from non-human primate gut metagenomes expand the primate-associated bacterial tree of life with over 1000 novel species
title_fullStr Microbial genomes from non-human primate gut metagenomes expand the primate-associated bacterial tree of life with over 1000 novel species
title_full_unstemmed Microbial genomes from non-human primate gut metagenomes expand the primate-associated bacterial tree of life with over 1000 novel species
title_short Microbial genomes from non-human primate gut metagenomes expand the primate-associated bacterial tree of life with over 1000 novel species
title_sort microbial genomes from non-human primate gut metagenomes expand the primate-associated bacterial tree of life with over 1000 novel species
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6935492/
https://www.ncbi.nlm.nih.gov/pubmed/31883524
http://dx.doi.org/10.1186/s13059-019-1923-9
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