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Industrialization is associated with elevated rates of horizontal gene transfer in the human microbiome

Mathieu Groussin, Mathilde Poyet, Ainara Sistiaga, Sean M. Kearney, Katya Moniz, Mary Noel, Jeff Hooker, Sean M. Gibbons, Laure Segurel, Alain Froment, Rihlat Said Mohamed, Alain Fezeu, Vanessa A. Juimo, Catherine Girard, Le Thanh Tu Nguyen, B. Jesse Shapiro, Jenni M. S. Lehtimäki, Lasse Ruokolainen, Pinja P. Kettunen, Tommi Vatanen, Shani Sigwazi, Audax Mabulla, Manuel Domínguez-Rodrigo, Roger E. Summons, Ramnik J. Xavier, Eric J. Alm
doi: https://doi.org/10.1101/2020.01.28.922104
Mathieu Groussin
1Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
2Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
3The Broad Institute of MIT and Harvard, Cambridge, MA, 02142, USA
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Mathilde Poyet
1Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
2Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
3The Broad Institute of MIT and Harvard, Cambridge, MA, 02142, USA
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Ainara Sistiaga
4Department of Earth, Atmospheric and Planetary Science, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
5Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark
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Sean M. Kearney
1Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
2Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
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Katya Moniz
1Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
2Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
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Mary Noel
6Chief Dull Knife College, Lame Deer, MT, 59043, USA
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Jeff Hooker
6Chief Dull Knife College, Lame Deer, MT, 59043, USA
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Sean M. Gibbons
7Institute for Systems Biology, Seattle, WA 98109, USA
8eScience Institute, University of Washington, Seattle, WA 98195, USA
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Laure Segurel
9UMR7206 Eco-anthropologie, CNRS-MNHN-Univ Paris Diderot-Sorbonne, France
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Alain Froment
10Institut de Recherche pour le Développement UMR 208, Muséum National d’Histoire Naturelle, Paris, France
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Rihlat Said Mohamed
11SA MRC / Wits Developmental Pathways for Health Research Unit, Department of Paediatrics, School of Clinical Medicine, Faculty of Health Sciences, University of Witwatersrand, Johannesburg, South Africa
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Alain Fezeu
12Institut de Recherche pour le Développement, Yaounde, Cameroon
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Vanessa A. Juimo
12Institut de Recherche pour le Développement, Yaounde, Cameroon
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Catherine Girard
13Université de Montréal, Département de sciences biologiques, C.P. 6128, succursale Centre-ville, Montreal, Quebec H3C 3J7, Canada
14Centre d’études nordiques & Sentinelle Nord, Département de biochimie, de microbiologie et de bio-informatique, Université Laval, 1030 rue de la Médecine, Québec (QC) Canada G1V0A6
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Le Thanh Tu Nguyen
1Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
2Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
3The Broad Institute of MIT and Harvard, Cambridge, MA, 02142, USA
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B. Jesse Shapiro
13Université de Montréal, Département de sciences biologiques, C.P. 6128, succursale Centre-ville, Montreal, Quebec H3C 3J7, Canada
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Jenni M. S. Lehtimäki
15Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental sciences, University of Helsinki, Finland
16COPSAC, Copenhagen Prospective Studies on Asthma in Childhood, Herlev and Gentofte Hospital, University of Copenhagen, Ledreborg Alle 34, 2820, Gentofte, Denmark
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Lasse Ruokolainen
15Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental sciences, University of Helsinki, Finland
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Pinja P. Kettunen
15Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental sciences, University of Helsinki, Finland
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Tommi Vatanen
3The Broad Institute of MIT and Harvard, Cambridge, MA, 02142, USA
17The Liggins Institute, University of Auckland, Auckland, 1023, New Zealand
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Shani Sigwazi
18Tumaini University Makumira, Arusha, Tanzania
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Audax Mabulla
19Archaeology Unit, University of Dar es Salaam, Dar es Salaam, Tanzania
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Manuel Domínguez-Rodrigo
20Department of Prehistory, Complutense University, Madrid, Spain
21Institute of Evolution in Africa, University of Alcalá de Henares, Madrid, Spain
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Roger E. Summons
4Department of Earth, Atmospheric and Planetary Science, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
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Ramnik J. Xavier
3The Broad Institute of MIT and Harvard, Cambridge, MA, 02142, USA
22Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA
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Eric J. Alm
1Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
2Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
3The Broad Institute of MIT and Harvard, Cambridge, MA, 02142, USA
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  • For correspondence: ejalm@mit.edu
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Abstract

Horizontal Gene Transfer, the process by which bacteria acquire new genes and functions from non-parental sources, is common in the human microbiome 1,2. If the timescale of HGT is rapid compared to the timescale of human colonization, then it could have the effect of ‘personalizing’ bacterial genomes by providing incoming strains with the genes necessary to adapt to the diet or lifestyle of a new host. The extent to which HGT occurs on the timescale of human colonization, however, remains unclear. Here, we analyzed 6,188 newly isolated and sequenced gut bacteria from 34 individuals in 9 human populations, and show that HGT is more common among bacteria isolated from the same human host, indicating that the timescale of transfer is short compared to the timescale of human colonization. Comparing across 9 human populations reveals that high rates of transfer may be a recent development in human history linked to industrialization and urbanization. In addition, we find that the genes involved in transfer reflect the lifestyle of the human hosts, with elevated transfer of carbohydrate metabolism genes in hunter gatherer populations, and transfer of antibiotic resistance genes among pastoralists who live in close contact with livestock. These results suggest that host-associated bacterial genomes are not static within individuals, but continuously acquire new functionality based on host diet and lifestyle.

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Posted January 29, 2020.
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Industrialization is associated with elevated rates of horizontal gene transfer in the human microbiome
Mathieu Groussin, Mathilde Poyet, Ainara Sistiaga, Sean M. Kearney, Katya Moniz, Mary Noel, Jeff Hooker, Sean M. Gibbons, Laure Segurel, Alain Froment, Rihlat Said Mohamed, Alain Fezeu, Vanessa A. Juimo, Catherine Girard, Le Thanh Tu Nguyen, B. Jesse Shapiro, Jenni M. S. Lehtimäki, Lasse Ruokolainen, Pinja P. Kettunen, Tommi Vatanen, Shani Sigwazi, Audax Mabulla, Manuel Domínguez-Rodrigo, Roger E. Summons, Ramnik J. Xavier, Eric J. Alm
bioRxiv 2020.01.28.922104; doi: https://doi.org/10.1101/2020.01.28.922104
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Industrialization is associated with elevated rates of horizontal gene transfer in the human microbiome
Mathieu Groussin, Mathilde Poyet, Ainara Sistiaga, Sean M. Kearney, Katya Moniz, Mary Noel, Jeff Hooker, Sean M. Gibbons, Laure Segurel, Alain Froment, Rihlat Said Mohamed, Alain Fezeu, Vanessa A. Juimo, Catherine Girard, Le Thanh Tu Nguyen, B. Jesse Shapiro, Jenni M. S. Lehtimäki, Lasse Ruokolainen, Pinja P. Kettunen, Tommi Vatanen, Shani Sigwazi, Audax Mabulla, Manuel Domínguez-Rodrigo, Roger E. Summons, Ramnik J. Xavier, Eric J. Alm
bioRxiv 2020.01.28.922104; doi: https://doi.org/10.1101/2020.01.28.922104

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