Elevated rates of horizontal gene transfer in the industrialized human microbiome

Mathieu Groussin¹, Mathilde Poyet², Ainara Sistiaga³, Sean M Kearney⁴, Katya Moniz⁵, Mary Noel⁶, Jeff Hooker⁶, Sean M Gibbons⁷, Laure Segurel⁸, Alain Froment⁹, Rihlat Said Mohamed¹⁰, Alain Fezeu¹¹, Vanessa A Juimo¹¹, Sophie Lafosse¹², Francis E Tabe¹³, Catherine Girard¹⁴, Deborah Iqaluk¹⁵, Le Thanh Tu Nguyen¹⁶, B Jesse Shapiro¹⁷, Jenni Lehtimäki¹⁸, Lasse Ruokolainen¹⁹, Pinja P Kettunen¹⁹, Tommi Vatanen²⁰, Shani Sigwazi²¹, Audax Mabulla²², Manuel Domínguez-Rodrigo²³, Yvonne A Nartey²⁴, Adwoa Agyei-Nkansah²⁵, Amoako Duah²⁶, Yaw A Awuku²⁷, Kenneth A Valles²⁸, Shadrack O Asibey²⁹, Mary Y Afihene³⁰, Lewis R Roberts³¹, Amelie Plymoth²⁴, Charles A Onyekwere³², Roger E Summons³³, Ramnik J Xavier³⁴, Eric J Alm³⁵

Affiliations

¹ Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA; The Broad Institute of MIT and Harvard, Cambridge, MA, USA; The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA. Electronic address: mgroussi@mit.edu.
² Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA; The Broad Institute of MIT and Harvard, Cambridge, MA, USA; The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA. Electronic address: mpoyet@mit.edu.
³ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Earth, Atmospheric and Planetary Science, Massachusetts Institute of Technology, Cambridge, MA, USA; GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.
⁴ Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA.
⁵ Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA; The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA.
⁶ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Chief Dull Knife College, Lame Deer, MT, USA.
⁷ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Institute for Systems Biology, Seattle, WA, USA; Department of Bioengineering, University of Washington, Seattle, WA, USA.
⁸ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; UMR7206 Eco-anthropologie, CNRS-MNHN-Univ Paris Diderot-Sorbonne, Paris, France.
⁹ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Institut de Recherche pour le Développement UMR 208, Muséum National d'Histoire Naturelle, Paris, France.
¹⁰ SA 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.
¹¹ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Institut de Recherche pour le Développement, Yaounde, Cameroon.
¹² UMR7206 Eco-anthropologie, CNRS-MNHN-Univ Paris Diderot-Sorbonne, Paris, France.
¹³ Faculté de Médecine et des Sciences Biomédicales, Université Yaoundé 1, Yaoundé, Cameroun.
¹⁴ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Université de Montréal, Département de sciences biologiques, C.P. 6128, succursale Centre-ville, Montréal, QC, Canada; Centre d'études nordiques, Département de biochimie, de microbiologie et de bio-informatique, Université Laval, 1030 rue de la Médecine, Québec, QC, Canada.
¹⁵ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Resolute Bay, Nunavut, Canada.
¹⁶ Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA; The Broad Institute of MIT and Harvard, Cambridge, MA, USA; The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA.
¹⁷ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Université de Montréal, Département de sciences biologiques, C.P. 6128, succursale Centre-ville, Montréal, QC, Canada; Department of Microbiology and Immunology, McGill University, Montreal, QC, Canada; McGill Genome Centre, McGill University, Montreal, QC, Canada.
¹⁸ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental sciences, University of Helsinki, Helsinki, Finland; Environmental Policy Centre, Finnish Environment Institute SYKE, Helsinki, Finland.
¹⁹ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental sciences, University of Helsinki, Helsinki, Finland.
²⁰ The Broad Institute of MIT and Harvard, Cambridge, MA, USA; The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; The Liggins Institute, University of Auckland, Auckland 1023, New Zealand.
²¹ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Tumaini University Makumira, Arusha, Tanzania.
²² The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Archaeology and Heritage Studies, University of Dar es Salaam, Tanzania.
²³ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Prehistory Unit, Department of History and Philosophy, University of Alcalá, Alcalá de Henares, Madrid, Spain; Institute of Evolution in Africa, University of Alcalá de Henares, Madrid, Spain.
²⁴ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
²⁵ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Medicine and Therapeutics, University of Ghana Medical School and Korle Bu Teaching Hospital, Accra, Ghana.
²⁶ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Medicine, St. Dominic Hospital, Akwatia, Ghana.
²⁷ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Internal Medicine and Therapeutics, School of Medical Sciences University of Cape Coast, Cape Coast, Ghana.
²⁸ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Medical Scientist Training Program, Mayo Clinic, Rochester, 55905, USA.
²⁹ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Catholic University College, Sunyani, Ghana.
³⁰ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Medicine, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana.
³¹ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Division of Gastroenterology and Hepatology, Mayo Clinic, 200 First Street SW, Rochester, MN, USA.
³² The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Medicine, Lagos State University College of Medicine, Lagos, Nigeria.
³³ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Earth, Atmospheric and Planetary Science, Massachusetts Institute of Technology, Cambridge, MA, USA.
³⁴ The Broad Institute of MIT and Harvard, Cambridge, MA, USA; The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA; Department of Molecular Biology, Massachusetts General Hospital, Boston, MA, USA.
³⁵ Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA; The Broad Institute of MIT and Harvard, Cambridge, MA, USA; The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA. Electronic address: ejalm@mit.edu.

PMID: 33794144
DOI: 10.1016/j.cell.2021.02.052

Free article

Elevated rates of horizontal gene transfer in the industrialized human microbiome

Mathieu Groussin et al. Cell. 2021.

Free article

. 2021 Apr 15;184(8):2053-2067.e18.

doi: 10.1016/j.cell.2021.02.052. Epub 2021 Mar 31.

Authors

Affiliations

¹ Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA; The Broad Institute of MIT and Harvard, Cambridge, MA, USA; The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA. Electronic address: mgroussi@mit.edu.
² Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA; The Broad Institute of MIT and Harvard, Cambridge, MA, USA; The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA. Electronic address: mpoyet@mit.edu.
³ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Earth, Atmospheric and Planetary Science, Massachusetts Institute of Technology, Cambridge, MA, USA; GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.
⁴ Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA.
⁵ Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA; The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA.
⁶ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Chief Dull Knife College, Lame Deer, MT, USA.
⁷ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Institute for Systems Biology, Seattle, WA, USA; Department of Bioengineering, University of Washington, Seattle, WA, USA.
⁸ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; UMR7206 Eco-anthropologie, CNRS-MNHN-Univ Paris Diderot-Sorbonne, Paris, France.
⁹ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Institut de Recherche pour le Développement UMR 208, Muséum National d'Histoire Naturelle, Paris, France.
¹⁰ SA 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.
¹¹ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Institut de Recherche pour le Développement, Yaounde, Cameroon.
¹² UMR7206 Eco-anthropologie, CNRS-MNHN-Univ Paris Diderot-Sorbonne, Paris, France.
¹³ Faculté de Médecine et des Sciences Biomédicales, Université Yaoundé 1, Yaoundé, Cameroun.
¹⁴ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Université de Montréal, Département de sciences biologiques, C.P. 6128, succursale Centre-ville, Montréal, QC, Canada; Centre d'études nordiques, Département de biochimie, de microbiologie et de bio-informatique, Université Laval, 1030 rue de la Médecine, Québec, QC, Canada.
¹⁵ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Resolute Bay, Nunavut, Canada.
¹⁶ Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA; The Broad Institute of MIT and Harvard, Cambridge, MA, USA; The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA.
¹⁷ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Université de Montréal, Département de sciences biologiques, C.P. 6128, succursale Centre-ville, Montréal, QC, Canada; Department of Microbiology and Immunology, McGill University, Montreal, QC, Canada; McGill Genome Centre, McGill University, Montreal, QC, Canada.
¹⁸ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental sciences, University of Helsinki, Helsinki, Finland; Environmental Policy Centre, Finnish Environment Institute SYKE, Helsinki, Finland.
¹⁹ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental sciences, University of Helsinki, Helsinki, Finland.
²⁰ The Broad Institute of MIT and Harvard, Cambridge, MA, USA; The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; The Liggins Institute, University of Auckland, Auckland 1023, New Zealand.
²¹ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Tumaini University Makumira, Arusha, Tanzania.
²² The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Archaeology and Heritage Studies, University of Dar es Salaam, Tanzania.
²³ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Prehistory Unit, Department of History and Philosophy, University of Alcalá, Alcalá de Henares, Madrid, Spain; Institute of Evolution in Africa, University of Alcalá de Henares, Madrid, Spain.
²⁴ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
²⁵ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Medicine and Therapeutics, University of Ghana Medical School and Korle Bu Teaching Hospital, Accra, Ghana.
²⁶ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Medicine, St. Dominic Hospital, Akwatia, Ghana.
²⁷ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Internal Medicine and Therapeutics, School of Medical Sciences University of Cape Coast, Cape Coast, Ghana.
²⁸ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Medical Scientist Training Program, Mayo Clinic, Rochester, 55905, USA.
²⁹ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Catholic University College, Sunyani, Ghana.
³⁰ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Medicine, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana.
³¹ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Division of Gastroenterology and Hepatology, Mayo Clinic, 200 First Street SW, Rochester, MN, USA.
³² The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Medicine, Lagos State University College of Medicine, Lagos, Nigeria.
³³ The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Earth, Atmospheric and Planetary Science, Massachusetts Institute of Technology, Cambridge, MA, USA.
³⁴ The Broad Institute of MIT and Harvard, Cambridge, MA, USA; The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA; Department of Molecular Biology, Massachusetts General Hospital, Boston, MA, USA.
³⁵ Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA; The Broad Institute of MIT and Harvard, Cambridge, MA, USA; The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA. Electronic address: ejalm@mit.edu.

PMID: 33794144
DOI: 10.1016/j.cell.2021.02.052

Abstract

Industrialization has impacted the human gut ecosystem, resulting in altered microbiome composition and diversity. Whether bacterial genomes may also adapt to the industrialization of their host populations remains largely unexplored. Here, we investigate the extent to which the rates and targets of horizontal gene transfer (HGT) vary across thousands of bacterial strains from 15 human populations spanning a range of industrialization. We show that HGTs have accumulated in the microbiome over recent host generations and that HGT occurs at high frequency within individuals. Comparison across human populations reveals that industrialized lifestyles are associated with higher HGT rates and that the functions of HGTs are related to the level of host industrialization. Our results suggest that gut bacteria continuously acquire new functionality based on host lifestyle and that high rates of HGT may be a recent development in human history linked to industrialization.

Keywords: antimicrobial resistance; bacterial genomics; culturomics; horizontal gene transfer; host-microbe interactions; human gut microbiome; industrialization; lifestyle; urbanization; virulence.

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Conflict of interest statement

Declaration of interests R.J.X. is a consultant to Novartis and Nestle. E.J.A. is a co-founder and shareholder of Finch Therapeutics, a company that specializes in microbiome-targeted therapeutics.

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Elevated rates of horizontal gene transfer in the industrialized human microbiome

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Elevated rates of horizontal gene transfer in the industrialized human microbiome

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