Abstract

The gastrointestinal tract is abundantly colonized by microbes, yet the translocation of oral species to the intestine is considered a rare aberrant event, and a hallmark of disease. By studying salivary and fecal microbial strain populations of 310 species in 470 individuals from five countries, we found that transmission to, and subsequent colonization of, the large intestine by oral microbes is common and extensive among healthy individuals. We found evidence for a vast majority of oral species to be transferable, with increased levels of transmission in colorectal cancer and rheumatoid arthritis patients and, more generally, for species described as opportunistic pathogens. This establishes the oral cavity as an endogenous reservoir for gut microbial strains, and oral-fecal transmission as an important process that shapes the gastrointestinal microbiome in health and disease.

Data availability

Raw sequencing data have been deposited in the European Nucleotide Archive under project accessions PRJNA289586 and PRJEB28422.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Thomas Sebastian Benedikt Schmidt

    Structural and Computational Biology, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8587-4177
  2. Matthew Robert Hayward

    Structural and Computational Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Luis Pedro Coelho

    Structural and Computational Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9280-7885
  4. Simone S Li

    Structural and Computational Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0073-3656
  5. Paul Igor Costea

    Structural and Computational Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Anita Yvonne Voigt

    Structural and Computational Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Jakob Wirbel

    Structural and Computational Biology, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Oleksandr M Maistrenko

    Structural and Computational Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Renato JC Alves

    Structural and Computational Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7212-0234
  10. Emma Bergsten

    Department of Gastroenterology, Université Paris-Est, Créteil, France
    Competing interests
    The authors declare that no competing interests exist.
  11. Carine de Beaufort

    Luxembourg Centre for Systems Biomedicine, University of Luxembourg, Esch-sur-Alzette, Luxembourg
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4310-6799
  12. Iradj Sobhani

    Department of Gastroenterology, Université Paris-Est, Créteil, France
    Competing interests
    The authors declare that no competing interests exist.
  13. Anna Heintz-Buschart

    Luxembourg Centre for Systems Biomedicine, University of Luxembourg, Esch-sur-Alzette, Luxembourg
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9780-1933
  14. Shinichi Sunagawa

    Structural and Computational Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  15. Georg Zeller

    Structural and Computational Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  16. Paul Wilmes

    Luxembourg Centre for Systems Biomedicine, University of Luxembourg, Esch-sur-Alzette, Luxembourg
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6478-2924
  17. Peer Bork

    Structural and Computational Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    For correspondence
    bork@embl.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2627-833X

Funding

Fonds National de la Recherche Luxembourg (CORE/15/BM/10404093)

  • Thomas Sebastian Benedikt Schmidt
  • Matthew Robert Hayward
  • Anna Heintz-Buschart

H2020 European Research Council (ERC-AdG-669830)

  • Thomas Sebastian Benedikt Schmidt
  • Simone S Li
  • Oleksandr M Maistrenko
  • Renato JC Alves
  • Peer Bork

H2020 Marie Skłodowska-Curie Actions (661019)

  • Matthew Robert Hayward

German Network Bioinformatics (de.NBI #031A537B)

  • Georg Zeller
  • Peer Bork

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Max Nieuwdorp, AMC, Netherlands

Ethics

Human subjects: Informed consent was obtained from all study subjects for which novel data was generated; see respective previous publications for details (PMID: 27723761; PMID: 25432777; PMID: 25888008).

Version history

  1. Received: October 9, 2018
  2. Accepted: February 3, 2019
  3. Accepted Manuscript published: February 12, 2019 (version 1)
  4. Version of Record published: March 19, 2019 (version 2)

Copyright

© 2019, Schmidt et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Thomas Sebastian Benedikt Schmidt
  2. Matthew Robert Hayward
  3. Luis Pedro Coelho
  4. Simone S Li
  5. Paul Igor Costea
  6. Anita Yvonne Voigt
  7. Jakob Wirbel
  8. Oleksandr M Maistrenko
  9. Renato JC Alves
  10. Emma Bergsten
  11. Carine de Beaufort
  12. Iradj Sobhani
  13. Anna Heintz-Buschart
  14. Shinichi Sunagawa
  15. Georg Zeller
  16. Paul Wilmes
  17. Peer Bork
(2019)
Extensive transmission of microbes along the gastrointestinal tract
eLife 8:e42693.
https://doi.org/10.7554/eLife.42693

Share this article

https://doi.org/10.7554/eLife.42693

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