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author Valles-Colomer, Mireia
Blanco-Míguez, Aitor
Manghi, Paolo
Asnicar, Francesco
Dubois, Leonard
Golzato, Davide
Armanini, Federica
Cumbo, Fabio
Huang, Kun D.
Manara, Serena
Masetti, Giulia
Pinto, Federica
Piperni, Elisa
Punčochář, Michal
Ricci, Liviana
Zolfo, Moreno
Farrant, Olivia
Goncalves, Adriana
Selma-Royo, Marta
Binetti, Ana G.
Becerra, Jimmy E.
Han, Bei
Lusingu, John
Amuasi, John
Amoroso, Loredana
Visconti, Alessia
Steves, Claire M.
Falchi, Mario
Filosi, Michele
Tett, Adrian
Last, Anna
Xu, Qian
Qin, Nan
Qin, Huanlong
May, Jürgen
Eibach, Daniel
Corrias, Maria Valeria
Ponzoni, Mirco
Pasolli, Edoardo
Spector, Tim D.
Domenici, Enrico
Collado, Maria Carmen
Segata, Nicola
author_facet Valles-Colomer, Mireia
Blanco-Míguez, Aitor
Manghi, Paolo
Asnicar, Francesco
Dubois, Leonard
Golzato, Davide
Armanini, Federica
Cumbo, Fabio
Huang, Kun D.
Manara, Serena
Masetti, Giulia
Pinto, Federica
Piperni, Elisa
Punčochář, Michal
Ricci, Liviana
Zolfo, Moreno
Farrant, Olivia
Goncalves, Adriana
Selma-Royo, Marta
Binetti, Ana G.
Becerra, Jimmy E.
Han, Bei
Lusingu, John
Amuasi, John
Amoroso, Loredana
Visconti, Alessia
Steves, Claire M.
Falchi, Mario
Filosi, Michele
Tett, Adrian
Last, Anna
Xu, Qian
Qin, Nan
Qin, Huanlong
May, Jürgen
Eibach, Daniel
Corrias, Maria Valeria
Ponzoni, Mirco
Pasolli, Edoardo
Spector, Tim D.
Domenici, Enrico
Collado, Maria Carmen
Segata, Nicola
author_sort Valles-Colomer, Mireia
collection PubMed
description The human microbiome is an integral component of the human body and a co-determinant of several health conditions(1,2). However, the extent to which interpersonal relations shape the individual genetic makeup of the microbiome and its transmission within and across populations remains largely unknown(3,4). 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 studies(5), especially those on non-infectious, microbiome-associated diseases.
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spelling pubmed-98920082023-02-03 The person-to-person transmission landscape of the gut and oral microbiomes Valles-Colomer, Mireia Blanco-Míguez, Aitor Manghi, Paolo Asnicar, Francesco Dubois, Leonard Golzato, Davide Armanini, Federica Cumbo, Fabio Huang, Kun D. Manara, Serena Masetti, Giulia Pinto, Federica Piperni, Elisa Punčochář, Michal Ricci, Liviana Zolfo, Moreno Farrant, Olivia Goncalves, Adriana Selma-Royo, Marta Binetti, Ana G. Becerra, Jimmy E. Han, Bei Lusingu, John Amuasi, John Amoroso, Loredana Visconti, Alessia Steves, Claire M. Falchi, Mario Filosi, Michele Tett, Adrian Last, Anna Xu, Qian Qin, Nan Qin, Huanlong May, Jürgen Eibach, Daniel Corrias, Maria Valeria Ponzoni, Mirco Pasolli, Edoardo Spector, Tim D. Domenici, Enrico Collado, Maria Carmen Segata, Nicola Nature Article The human microbiome is an integral component of the human body and a co-determinant of several health conditions(1,2). However, the extent to which interpersonal relations shape the individual genetic makeup of the microbiome and its transmission within and across populations remains largely unknown(3,4). 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 studies(5), especially those on non-infectious, microbiome-associated diseases. Nature Publishing Group UK 2023-01-18 2023 /pmc/articles/PMC9892008/ /pubmed/36653448 http://dx.doi.org/10.1038/s41586-022-05620-1 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Valles-Colomer, Mireia
Blanco-Míguez, Aitor
Manghi, Paolo
Asnicar, Francesco
Dubois, Leonard
Golzato, Davide
Armanini, Federica
Cumbo, Fabio
Huang, Kun D.
Manara, Serena
Masetti, Giulia
Pinto, Federica
Piperni, Elisa
Punčochář, Michal
Ricci, Liviana
Zolfo, Moreno
Farrant, Olivia
Goncalves, Adriana
Selma-Royo, Marta
Binetti, Ana G.
Becerra, Jimmy E.
Han, Bei
Lusingu, John
Amuasi, John
Amoroso, Loredana
Visconti, Alessia
Steves, Claire M.
Falchi, Mario
Filosi, Michele
Tett, Adrian
Last, Anna
Xu, Qian
Qin, Nan
Qin, Huanlong
May, Jürgen
Eibach, Daniel
Corrias, Maria Valeria
Ponzoni, Mirco
Pasolli, Edoardo
Spector, Tim D.
Domenici, Enrico
Collado, Maria Carmen
Segata, Nicola
The person-to-person transmission landscape of the gut and oral microbiomes
title The person-to-person transmission landscape of the gut and oral microbiomes
title_full The person-to-person transmission landscape of the gut and oral microbiomes
title_fullStr The person-to-person transmission landscape of the gut and oral microbiomes
title_full_unstemmed The person-to-person transmission landscape of the gut and oral microbiomes
title_short The person-to-person transmission landscape of the gut and oral microbiomes
title_sort person-to-person transmission landscape of the gut and oral microbiomes
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9892008/
https://www.ncbi.nlm.nih.gov/pubmed/36653448
http://dx.doi.org/10.1038/s41586-022-05620-1
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