Extensive Unexplored Human Microbiome Diversity Revealed by Over 150,000 Genomes from Metagenomes Spanning Age, Geography, and Lifestyle

Pasolli, Edoardo, Asnicar, Francesco, Manara, Serena, Zolfo, Moreno, Karcher, Nicolai, Armanini, Federica, Beghini, Francesco, Manghi, Paolo, Tett, Adrian, Ghensi, Paolo, Collado, Maria Carmen, Rice, Benjamin L., DuLong, Casey, Morgan, Xochitl C., Golden, Christopher D., Quince, Christopher, Huttenhower, Curtis and Segata, Nicola (2019) Extensive Unexplored Human Microbiome Diversity Revealed by Over 150,000 Genomes from Metagenomes Spanning Age, Geography, and Lifestyle. Cell, 176 (3). 649-662.e20. ISSN 0092-8674

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Abstract

The body-wide human microbiome plays a role in health, but its full diversity remains uncharacterized, particularly outside of the gut and in international populations. We leveraged 9,428 metagenomes to reconstruct 154,723 microbial genomes (45% of high quality) spanning body sites, ages, countries, and lifestyles. We recapitulated 4,930 species-level genome bins (SGBs), 77% without genomes in public repositories (unknown SGBs [uSGBs]). uSGBs are prevalent (in 93% of well-assembled samples), expand underrepresented phyla, and are enriched in non-Westernized populations (40% of the total SGBs). We annotated 2.85 M genes in SGBs, many associated with conditions including infant development (94,000) or Westernization (106,000). SGBs and uSGBs permit deeper microbiome analyses and increase the average mappability of metagenomic reads from 67.76% to 87.51% in the gut (median 94.26%) and 65.14% to 82.34% in the mouth. We thus identify thousands of microbial genomes from yet-to-be-named species, expand the pangenomes of human-associated microbes, and allow better exploitation of metagenomic technologies.

Item Type: Article
Additional Information: Funding Information: We thank the MAHERY team, particularly Anjaranirina Evelyn Jean Gasta, Hervet Randriamady, and Miadana Vonona Arisoa, and the GeNaPi Project Team, particularly Mari Olcina, Lourdes Larruy, Carla Muñoz, and Cristina Alcántara. We thank Levi Waldron and all the members of the Segata and Huttenhower laboratories for fruitful discussions, the students of the Computational Microbial Genomics master course at University of Trento for help with the manual curation of assemblies, and the HPC and NGS facilities at University of Trento. This work was supported by EU-H2020 ( DiMeTrack-707345 ) to E.P.; by NIH NHGRI ( R01HG005220 ), NIDDK ( R24DK110499 ), NIDDK ( U54DE023798 ), CMIT ( 6935956 ) to C.H.; and by ERC ( MetaPG-716575 ), MIUR ( RBFR13EWWI ), EU-FP7 ( PCIG13-GA-2013-618833 ), CARITRO ( 2013.0239 ), and LEO Pharma Foundation to N.S. Madagascar data and sample collection was supported by the Rockefeller Foundation to C.D.G. Funding Information: We thank the MAHERY team, particularly Anjaranirina Evelyn Jean Gasta, Hervet Randriamady, and Miadana Vonona Arisoa, and the GeNaPi Project Team, particularly Mari Olcina, Lourdes Larruy, Carla Muñoz, and Cristina Alcántara. We thank Levi Waldron and all the members of the Segata and Huttenhower laboratories for fruitful discussions, the students of the Computational Microbial Genomics master course at University of Trento for help with the manual curation of assemblies, and the HPC and NGS facilities at University of Trento. This work was supported by EU-H2020 (DiMeTrack-707345) to E.P.; by NIH NHGRI (R01HG005220), NIDDK (R24DK110499), NIDDK (U54DE023798), CMIT (6935956) to C.H.; and by ERC (MetaPG-716575), MIUR (RBFR13EWWI), EU-FP7 (PCIG13-GA-2013-618833), CARITRO (2013.0239), and LEO Pharma Foundation to N.S. Madagascar data and sample collection was supported by the Rockefeller Foundation to C.D.G. Publisher Copyright: © 2019 The Author(s)
Uncontrolled Keywords: human microbiome,metagenomic assembly,metagenomic mappability,metagenomic meta-analysis,metagenomics,non-westernized microbiomes,unexplored microbial diversity,biochemistry, genetics and molecular biology(all),sdg 3 - good health and well-being ,/dk/atira/pure/subjectarea/asjc/1300
Faculty \ School: Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 08 Sep 2022 14:30
Last Modified: 22 Sep 2022 18:34
URI: https://ueaeprints.uea.ac.uk/id/eprint/87976
DOI: 10.1016/j.cell.2019.01.001

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