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The person-to-person transmission landscape of the gut and oral microbiomes

Author

Listed:
  • Mireia Valles-Colomer

    (University of Trento)

  • Aitor Blanco-Míguez

    (University of Trento)

  • Paolo Manghi

    (University of Trento)

  • Francesco Asnicar

    (University of Trento)

  • Leonard Dubois

    (University of Trento)

  • Davide Golzato

    (University of Trento)

  • Federica Armanini

    (University of Trento)

  • Fabio Cumbo

    (University of Trento)

  • Kun D. Huang

    (University of Trento)

  • Serena Manara

    (University of Trento)

  • Giulia Masetti

    (University of Trento)

  • Federica Pinto

    (University of Trento)

  • Elisa Piperni

    (IEO European Institute of Oncology IRCCS)

  • Michal Punčochář

    (University of Trento)

  • Liviana Ricci

    (University of Trento)

  • Moreno Zolfo

    (University of Trento)

  • Olivia Farrant

    (London School of Hygiene and Tropical Medicine)

  • Adriana Goncalves

    (London School of Hygiene and Tropical Medicine)

  • Marta Selma-Royo

    (University of Trento
    Paterna)

  • Ana G. Binetti

    (Universidad Nacional del Litoral)

  • Jimmy E. Becerra

    (Universidad Metropolitana)

  • Bei Han

    (Xi’an Jiaotong University)

  • John Lusingu

    (National Institute for Medical Research, Tanga Medical Research Centre)

  • John Amuasi

    (Kwame Nkrumah University of Science and Technology)

  • Loredana Amoroso

    (Oncology Unit, IRCCS Istituto Giannina Gaslini)

  • Alessia Visconti

    (King’s College London)

  • Claire M. Steves

    (King’s College London)

  • Mario Falchi

    (King’s College London)

  • Michele Filosi

    (University of Trento)

  • Adrian Tett

    (University of Trento
    University of Vienna)

  • Anna Last

    (London School of Hygiene and Tropical Medicine)

  • Qian Xu

    (Tongji University School of Medicine
    Realbio Genomics Institute)

  • Nan Qin

    (Tongji University School of Medicine
    Realbio Genomics Institute)

  • Huanlong Qin

    (Tongji University School of Medicine)

  • Jürgen May

    (Bernhard Nocht Institute for Tropical Medicine)

  • Daniel Eibach

    (Bernhard Nocht Institute for Tropical Medicine)

  • Maria Valeria Corrias

    (IRCCS Istituto Giannina Gaslini)

  • Mirco Ponzoni

    (IRCCS Istituto Giannina Gaslini)

  • Edoardo Pasolli

    (University of Naples ‘Federico II’)

  • Tim D. Spector

    (King’s College London)

  • Enrico Domenici

    (University of Trento
    Microsoft Research Foundation)

  • Maria Carmen Collado

    (Paterna)

  • Nicola Segata

    (University of Trento
    IEO European Institute of Oncology IRCCS)

Abstract

The human microbiome is an integral component of the human body and a co-determinant of several health conditions1,2. However, the extent to which interpersonal relations shape the individual genetic makeup of the microbiome and its transmission within and across populations remains largely unknown3,4. Here, capitalizing on more than 9,700 human metagenomes and computational strain-level profiling, we detected extensive bacterial strain sharing across individuals (more than 10 million instances) with distinct mother-to-infant, intra-household and intra-population transmission patterns. Mother-to-infant gut microbiome transmission was considerable and stable during infancy (around 50% of the same strains among shared species (strain-sharing rate)) and remained detectable at older ages. By contrast, the transmission of the oral microbiome occurred largely horizontally and was enhanced by the duration of cohabitation. There was substantial strain sharing among cohabiting individuals, with 12% and 32% median strain-sharing rates for the gut and oral microbiomes, and time since cohabitation affected strain sharing more than age or genetics did. Bacterial strain sharing additionally recapitulated host population structures better than species-level profiles did. Finally, distinct taxa appeared as efficient spreaders across transmission modes and were associated with different predicted bacterial phenotypes linked with out-of-host survival capabilities. The extent of microorganism transmission that we describe underscores its relevance in human microbiome studies5, especially those on non-infectious, microbiome-associated diseases.

Suggested Citation

  • Mireia Valles-Colomer & Aitor Blanco-Míguez & Paolo Manghi & Francesco Asnicar & Leonard Dubois & Davide Golzato & Federica Armanini & Fabio Cumbo & Kun D. Huang & Serena Manara & Giulia Masetti & Fed, 2023. "The person-to-person transmission landscape of the gut and oral microbiomes," Nature, Nature, vol. 614(7946), pages 125-135, February.
  • Handle: RePEc:nat:nature:v:614:y:2023:i:7946:d:10.1038_s41586-022-05620-1
    DOI: 10.1038/s41586-022-05620-1
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    Citations

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    Cited by:

    1. Qiwen Cheng & Rosa Krajmalnik-Brown & John K. DiBaise & Juan Maldonado & M. Aaron Guest & Michael Todd & Shelby L. Langer, 2023. "Relationship Functioning and Gut Microbiota Composition among Older Adult Couples," IJERPH, MDPI, vol. 20(8), pages 1-17, April.
    2. Tomás Clive Barker-Tejeda & Elisa Zubeldia-Varela & Andrea Macías-Camero & Lola Alonso & Isabel Adoración Martín-Antoniano & María Fernanda Rey-Stolle & Leticia Mera-Berriatua & Raphaëlle Bazire & Pau, 2024. "Comparative characterization of the infant gut microbiome and their maternal lineage by a multi-omics approach," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    3. M. C. Rühlemann & C. Bang & J. F. Gogarten & B. M. Hermes & M. Groussin & S. Waschina & M. Poyet & M. Ulrich & C. Akoua-Koffi & T. Deschner & J. J. Muyembe-Tamfum & M. M. Robbins & M. Surbeck & R. M. , 2024. "Functional host-specific adaptation of the intestinal microbiome in hominids," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Sanzhima Garmaeva & Trishla Sinha & Anastasia Gulyaeva & Nataliia Kuzub & Johanne E. Spreckels & Sergio Andreu-Sánchez & Ranko Gacesa & Arnau Vich Vila & Siobhan Brushett & Marloes Kruk & Jackie Deken, 2024. "Transmission and dynamics of mother-infant gut viruses during pregnancy and early life," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    5. Yadid M. Algavi & Elhanan Borenstein, 2024. "Relative dispersion ratios following fecal microbiota transplant elucidate principles governing microbial migration dynamics," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

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