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

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, Federica Pinto, Elisa Piperni, Michal Punčochář, Liviana Ricci, Moreno Zolfo, Olivia Farrant, Adriana Goncalves, Marta Selma-Royo, Ana G. Binetti, Jimmy E. Becerra, Bei Han, John Lusingu, John Amuasi, Loredana Amoroso, Alessia Visconti, Claire M. Steves, Mario Falchi, Michele Filosi, Adrian Tett, Anna Last, Qian Xu, Nan Qin, Huanlong Qin, Jürgen May, Daniel Eibach, Maria Valeria Corrias, Mirco Ponzoni, Edoardo Pasolli, Tim D. Spector, Enrico Domenici, Maria Carmen Collado and Nicola Segata ()
Additional contact information
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
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
Anna Last: London School of Hygiene and Tropical Medicine
Qian Xu: Tongji University School of Medicine
Nan Qin: Tongji University School of Medicine
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
Maria Carmen Collado: Paterna
Nicola Segata: University of Trento

Nature, 2023, vol. 614, issue 7946, 125-135

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41586-022-05620-1

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