Elevated rates of horizontal gene transfer in the industrialized human microbiome.


Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
15 04 2021
Historique:
received: 29 07 2020
revised: 27 10 2020
accepted: 24 02 2021
pubmed: 2 4 2021
medline: 21 10 2021
entrez: 1 4 2021
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 33794144
pii: S0092-8674(21)00241-5
doi: 10.1016/j.cell.2021.02.052
pii:
doi:

Substances chimiques

DNA, Bacterial 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2053-2067.e18

Subventions

Organisme : NCATS NIH HHS
ID : TL1 TR002380
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR002377
Pays : United States

Informations de copyright

Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

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.

Auteurs

Mathieu Groussin (M)

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.

Mathilde Poyet (M)

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.

Ainara Sistiaga (A)

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.

Sean M Kearney (SM)

Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA.

Katya Moniz (K)

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.

Mary Noel (M)

The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Chief Dull Knife College, Lame Deer, MT, USA.

Jeff Hooker (J)

The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Chief Dull Knife College, Lame Deer, MT, USA.

Sean M Gibbons (SM)

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.

Laure Segurel (L)

The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; UMR7206 Eco-anthropologie, CNRS-MNHN-Univ Paris Diderot-Sorbonne, Paris, France.

Alain Froment (A)

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.

Rihlat Said Mohamed (RS)

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.

Alain Fezeu (A)

The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Institut de Recherche pour le Développement, Yaounde, Cameroon.

Vanessa A Juimo (VA)

The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Institut de Recherche pour le Développement, Yaounde, Cameroon.

Sophie Lafosse (S)

UMR7206 Eco-anthropologie, CNRS-MNHN-Univ Paris Diderot-Sorbonne, Paris, France.

Francis E Tabe (FE)

Faculté de Médecine et des Sciences Biomédicales, Université Yaoundé 1, Yaoundé, Cameroun.

Catherine Girard (C)

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.

Deborah Iqaluk (D)

The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Resolute Bay, Nunavut, Canada.

Le Thanh Tu Nguyen (LTT)

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.

B Jesse Shapiro (BJ)

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.

Jenni Lehtimäki (J)

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.

Lasse Ruokolainen (L)

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.

Pinja P Kettunen (PP)

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.

Tommi Vatanen (T)

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.

Shani Sigwazi (S)

The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Tumaini University Makumira, Arusha, Tanzania.

Audax Mabulla (A)

The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Archaeology and Heritage Studies, University of Dar es Salaam, Tanzania.

Manuel Domínguez-Rodrigo (M)

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.

Yvonne A Nartey (YA)

The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.

Adwoa Agyei-Nkansah (A)

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.

Amoako Duah (A)

The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Medicine, St. Dominic Hospital, Akwatia, Ghana.

Yaw A Awuku (YA)

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.

Kenneth A Valles (KA)

The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Medical Scientist Training Program, Mayo Clinic, Rochester, 55905, USA.

Shadrack O Asibey (SO)

The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Catholic University College, Sunyani, Ghana.

Mary Y Afihene (MY)

The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Medicine, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana.

Lewis R Roberts (LR)

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.

Amelie Plymoth (A)

The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.

Charles A Onyekwere (CA)

The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Medicine, Lagos State University College of Medicine, Lagos, Nigeria.

Roger E Summons (RE)

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.

Ramnik J Xavier (RJ)

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.

Eric J Alm (EJ)

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.

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