The person-to-person transmission landscape of the gut and oral microbiomes
Creators
- Valles-Colomer, Mireia1
- Blanco-Míguez, Aitor1
- Manghi, Paolo1
- Asnicar, Francesco1
- Dubois, Leonard1
- Golzato, Davide1
- Armanini, Federica1
- Cumbo, Fabio1
- Huang, Kun D.1
- Manara, Serena1
- Masetti, Giulia1
- Pinto, Federica1
- Piperni, Elisa2
- Punčochář, Michal1
- Ricci, Liviana1
- Zolfo, Moreno1
- Farrant, Olivia3
- Goncalves, Adriana3
- Selma-Royo, Marta4
- Binetti, Ana G.5
- Becerra, Jimmy E.6
- Han, Bei7
- Lusingu, John8
- Amuasi, John9
- Amoroso, Loredana10
- Visconti, Alessia11
- Steves, Claire M.11
- Falchi, Mario11
- Filosi, Michele1
- Tett, Adrian12
- Last, Anna3
- Xu, Qian13
- Qin, Nan13
- Qin, Huanlong14
- May, Jürgen15
- Eibach, Daniel15
- Corrias, Maria Valeria16
- Ponzoni, Mirco16
- Pasolli, Edoardo17
- Spector, Tim D.11
- Domenici, Enrico18
- Collado, Maria Carmen19
- Segata, Nicola20
- 1. Department CIBIO, University of Trento, Trento, Italy
- 2. Department of Experimental Oncology, IEO European Institute of Oncology IRCCS, Milan, Italy
- 3. Clinical Research Department, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, UK
- 4. Department CIBIO, University of Trento, Trento, Italy; Institute of Agrochemistry and Food Technology-National Research Council (IATA-CSIC), Paterna, Valencia, Spain
- 5. Instituto de Lactología Industrial (CONICET-UNL), Facultad de Ingeniería Química, Universidad Nacional del Litoral, Santa Fe, Argentina
- 6. Grupo de Investigación Alimentación y Comportamiento Humano, Universidad Metropolitana, Barranquilla, Colombia
- 7. School of Public Health, Health Science Center, Xi'an Jiaotong University, Xi'an, China
- 8. National Institute for Medical Research, Tanga Medical Research Centre, Tanga, Tanzania
- 9. Kumasi Centre for Collaborative Research in Tropical Medicine, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana
- 10. Oncology Unit, IRCCS Istituto Giannina Gaslini, Genoa, Italy
- 11. Department of Twin Research and Genetic Epidemiology, King's College London, London, UK
- 12. Centre for Microbiology and Environmental Systems Science, University of Vienna, Vienna, Austria
- 13. Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, China; Realbio Genomics Institute, Shanghai, China
- 14. Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, China
- 15. Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany
- 16. Laboratory of Experimental Therapies in Oncology, IRCCS Istituto Giannina Gaslini, Genoa, Italy
- 17. Department of Agricultural Sciences, University of Naples 'Federico II', Portici, Italy
- 18. Department CIBIO, University of Trento, Trento, Italy; Centre for Computational and Systems Biology (COSBI), Microsoft Research Foundation, Rovereto, Italy
- 19. Institute of Agrochemistry and Food Technology-National Research Council (IATA-CSIC), Paterna, Valencia, Spain
- 20. Department CIBIO, University of Trento, Trento, Italy; Department of Experimental Oncology, IEO European Institute of Oncology IRCCS, Milan, Italy
Description
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.
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