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Ecology drives a global network of gene exchange connecting the human microbiome

Author

Listed:
  • Chris S. Smillie

    (Computational and Systems Biology Initiative, Massachusetts Institute of Technology)

  • Mark B. Smith

    (Microbiology Graduate Program, Massachusetts Institute of Technology)

  • Jonathan Friedman

    (Computational and Systems Biology Initiative, Massachusetts Institute of Technology)

  • Otto X. Cordero

    (Massachusetts Institute of Technology)

  • Lawrence A. David

    (Society of Fellows, Harvard University)

  • Eric J. Alm

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Broad Institute)

Abstract

Gene swapping in the human microbiome Horizontal gene transfer — the exchange of genetic material between different species or lineages — is an important factor in bacterial evolution. A study of human microbiome data comprising more than 2,000 full bacterial genomes shows that this environment is a hotbed of horizontal gene transfer: pairs of bacteria isolated from the human body are 25-fold more likely to share transferred DNA than pairs from other environments. Thus microbial ecology — rather than phylogeny or geography — is the most important driver of the patterns of horizontal gene exchange. Further analysis revealed 42 unique antibiotic-resistance genes that had been transferred between human and agricultural isolates, and 43 transfers across national borders.

Suggested Citation

  • Chris S. Smillie & Mark B. Smith & Jonathan Friedman & Otto X. Cordero & Lawrence A. David & Eric J. Alm, 2011. "Ecology drives a global network of gene exchange connecting the human microbiome," Nature, Nature, vol. 480(7376), pages 241-244, December.
    • Handle: RePEc:nat:nature:v:480:y:2011:i:7376:d:10.1038_nature10571
    DOI: 10.1038/nature10571
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    Citations

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    Cited by:

    1. Charles K Fisher & Thierry Mora & Aleksandra M Walczak, 2017. "Variable habitat conditions drive species covariation in the human microbiota," PLOS Computational Biology, Public Library of Science, vol. 13(4), pages 1-18, April.
    2. Rohan Maddamsetti & Yi Yao & Teng Wang & Junheng Gao & Vincent T. Huang & Grayson S. Hamrick & Hye-In Son & Lingchong You, 2024. "Duplicated antibiotic resistance genes reveal ongoing selection and horizontal gene transfer in bacteria," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Patrick Munk & Christian Brinch & Frederik Duus Møller & Thomas N. Petersen & Rene S. Hendriksen & Anne Mette Seyfarth & Jette S. Kjeldgaard & Christina Aaby Svendsen & Bram Bunnik & Fanny Berglund & , 2022. "Genomic analysis of sewage from 101 countries reveals global landscape of antimicrobial resistance," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Samuel C. Forster & Junyan Liu & Nitin Kumar & Emily L. Gulliver & Jodee A. Gould & Alejandra Escobar-Zepeda & Tapoka Mkandawire & Lindsay J. Pike & Yan Shao & Mark D. Stares & Hilary P. Browne & B. A, 2022. "Strain-level characterization of broad host range mobile genetic elements transferring antibiotic resistance from the human microbiome," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    5. Nils Giordano & Marinna Gaudin & Camille Trottier & Erwan Delage & Charlotte Nef & Chris Bowler & Samuel Chaffron, 2024. "Genome-scale community modelling reveals conserved metabolic cross-feedings in epipelagic bacterioplankton communities," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    6. Paulo Martins Da Costa & Luís Loureiro & Augusto J. F. Matos, 2013. "Transfer of Multidrug-Resistant Bacteria Between Intermingled Ecological Niches: The Interface Between Humans, Animals and the Environment," IJERPH, MDPI, vol. 10(1), pages 1-17, January.
    7. Wenxiu Wang & Weizhi Song & Marwan E. Majzoub & Xiaoyuan Feng & Bu Xu & Jianchang Tao & Yuanqing Zhu & Zhiyong Li & Pei-Yuan Qian & Nicole S. Webster & Torsten Thomas & Lu Fan, 2024. "Decoupling of strain- and intrastrain-level interactions of microbiomes in a sponge holobiont," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    8. Eugen Pfeifer & Eduardo P. C. Rocha, 2024. "Phage-plasmids promote recombination and emergence of phages and plasmids," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    9. Izabela Wolak & Małgorzata Czatzkowska & Monika Harnisz & Jan Paweł Jastrzębski & Łukasz Paukszto & Paulina Rusanowska & Ewa Felis & Ewa Korzeniewska, 2022. "Metagenomic Analysis of the Long-Term Synergistic Effects of Antibiotics on the Anaerobic Digestion of Cattle Manure," Energies, MDPI, vol. 15(5), pages 1-19, March.
    10. Kihyun Lee & Sebastien Raguideau & Kimmo Sirén & Francesco Asnicar & Fabio Cumbo & Falk Hildebrand & Nicola Segata & Chang-Jun Cha & Christopher Quince, 2023. "Population-level impacts of antibiotic usage on the human gut microbiome," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    11. Peter J. Diebold & Matthew W. Rhee & Qiaojuan Shi & Nguyen Vinh Trung & Fayaz Umrani & Sheraz Ahmed & Vandana Kulkarni & Prasad Deshpande & Mallika Alexander & Ngo Hoa & Nicholas A. Christakis & Najee, 2023. "Clinically relevant antibiotic resistance genes are linked to a limited set of taxa within gut microbiome worldwide," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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