The person-to-person transmission landscape of the gut and oral microbiomes
Author:
Valles-Colomer MireiaORCID, Blanco-Míguez AitorORCID, Manghi PaoloORCID, Asnicar FrancescoORCID, Dubois Leonard, Golzato Davide, Armanini Federica, Cumbo Fabio, Huang Kun D., Manara SerenaORCID, Masetti Giulia, Pinto FedericaORCID, Piperni Elisa, Punčochář Michal, Ricci LivianaORCID, Zolfo MorenoORCID, Farrant Olivia, Goncalves Adriana, Selma-Royo Marta, Binetti Ana G.ORCID, Becerra Jimmy E., Han Bei, Lusingu John, Amuasi JohnORCID, Amoroso Loredana, Visconti AlessiaORCID, Steves Claire M., Falchi MarioORCID, Filosi MicheleORCID, Tett Adrian, Last Anna, Xu QianORCID, Qin NanORCID, Qin HuanlongORCID, May JürgenORCID, Eibach Daniel, Corrias Maria ValeriaORCID, Ponzoni Mirco, Pasolli Edoardo, Spector Tim D.ORCID, Domenici EnricoORCID, Collado Maria Carmen, Segata NicolaORCID
Abstract
AbstractThe 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.
Publisher
Springer Science and Business Media LLC
Subject
Multidisciplinary
Reference128 articles.
1. Falony, G. et al. Population-level analysis of gut microbiome variation. Science 352, 560–564 (2016). 2. Asnicar, F. et al. Microbiome connections with host metabolism and habitual diet from 1,098 deeply phenotyped individuals. Nat. Med. 27, 321–332 (2021). 3. Browne, H. P., Neville, B. A., Forster, S. C. & Lawley, T. D. Transmission of the gut microbiota: spreading of health. Nat. Rev. Microbiol. 15, 531–543 (2017). 4. Robinson, C. D., Bohannan, B. J. & Britton, R. A. Scales of persistence: transmission and the microbiome. Curr. Opin. Microbiol. 50, 42–49 (2019). 5. Finlay, B. B. & CIFAR Humans and the Microbiome. Are noncommunicable diseases communicable? Science 367, 250–251 (2020).
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