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; Nicola Segata

doi:10.1038/s41586-022-05620-1

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 BinettiJimmy 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, Nicola Segata

Research output: Contribution to journal › Article › peer-review

157 Citations (Scopus)

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.

Original language	English
Pages (from-to)	125-135
Number of pages	11
Journal	Nature
Volume	614
Issue number	7946
DOIs	https://doi.org/10.1038/s41586-022-05620-1
Publication status	Published - 2 Feb 2023

Keywords

Female
Humans
Infant
Bacteria/classification
Gastrointestinal Microbiome/genetics
Metagenome
Microbiota/genetics
Mothers
Mouth/microbiology
Infectious Disease Transmission, Vertical
Family Characteristics
Aging
Disease Transmission, Infectious
Time Factors
Microbial Viability
Home Environment

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1038/s41586-022-05620-1

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Valles-Colomer, M., Blanco-Míguez, A., Manghi, P., Asnicar, F., Dubois, L., Golzato, D., Armanini, F., Cumbo, F., Huang, K. D., Manara, S., Masetti, G., Pinto, F., Piperni, E., Punčochář, M., Ricci, L., Zolfo, M., Farrant, O., Goncalves, A., Selma-Royo, M., ... Segata, N. (2023). The person-to-person transmission landscape of the gut and oral microbiomes. Nature, 614(7946), 125-135. https://doi.org/10.1038/s41586-022-05620-1

@article{78c5b198a9ac4ed49162bf3180c4538b,

title = "The person-to-person transmission landscape of the gut and oral microbiomes",

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.",

keywords = "Female, Humans, Infant, Bacteria/classification, Gastrointestinal Microbiome/genetics, Metagenome, Microbiota/genetics, Mothers, Mouth/microbiology, Infectious Disease Transmission, Vertical, Family Characteristics, Aging, Disease Transmission, Infectious, Time Factors, Microbial Viability, Home Environment",

author = "Mireia Valles-Colomer and Aitor Blanco-M{\'i}guez and Paolo Manghi and Francesco Asnicar and Leonard Dubois and Davide Golzato and Federica Armanini and Fabio Cumbo and Huang, {Kun D} and Serena Manara and Giulia Masetti and Federica Pinto and Elisa Piperni and Michal Pun{\v c}och{\'a}{\v r} and Liviana Ricci and Moreno Zolfo and Olivia Farrant and Adriana Goncalves and Marta Selma-Royo and Binetti, {Ana G} and Becerra, {Jimmy E} and Bei Han and John Lusingu and John Amuasi and Loredana Amoroso and Alessia Visconti and Steves, {Claire M} and Mario Falchi and Michele Filosi and Adrian Tett and Anna Last and Qian Xu and Nan Qin and Huanlong Qin and J{\"u}rgen May and Daniel Eibach and Corrias, {Maria Valeria} and Mirco Ponzoni and Edoardo Pasolli and Spector, {Tim D} and Enrico Domenici and Collado, {Maria Carmen} and Nicola Segata",

note = "Funding Information: We thank all study participants for their commitment; N. Volfovsky, P. Feliciano and A. Packer from the Simons Foundations for their kind support with the SPARK collection data; the LaBSSAH—CIBIO Next Generation Sequencing Facility of the University of Trento (V. de Sanctis, R. Bertorelli, P. Cavallerio and C. Valentini) for sequencing the metagenomic libraries. This work was supported by the European Research Council (ERC-STG project MetaPG-716575 and ERC-CoG microTOUCH-101045015) to N.S. and by EMBO ALTF 593–2020 to M.V.-C. The work was also partially supported by MIUR {\textquoteleft}Futuro in Ricerca{\textquoteright} (grant no. RBFR13EWWI_001) to N.S., by the European H2020 programme (ONCOBIOME-825410 project, MASTER-818368 project, and IHMCSA-964590) to N.S., by the National Cancer Institute of the National Institutes of Health (1U01CA230551) to N.S., by the Premio Internazionale Lombardia e Ricerca 2019 to N.S., by the Simons Foundation (award ID 648614) to E.D. and N.S., and by the European Research Council (ERC-STG project Mami-639226) to M.C.C. Funding Information: We thank all study participants for their commitment; N. Volfovsky, P. Feliciano and A. Packer from the Simons Foundations for their kind support with the SPARK collection data; the LaBSSAH—CIBIO Next Generation Sequencing Facility of the University of Trento (V. de Sanctis, R. Bertorelli, P. Cavallerio and C. Valentini) for sequencing the metagenomic libraries. This work was supported by the European Research Council (ERC-STG project MetaPG-716575 and ERC-CoG microTOUCH-101045015) to N.S. and by EMBO ALTF 593–2020 to M.V.-C. The work was also partially supported by MIUR {\textquoteleft}Futuro in Ricerca{\textquoteright} (grant no. RBFR13EWWI_001) to N.S., by the European H2020 programme (ONCOBIOME-825410 project, MASTER-818368 project, and IHMCSA-964590) to N.S., by the National Cancer Institute of the National Institutes of Health (1U01CA230551) to N.S., by the Premio Internazionale Lombardia e Ricerca 2019 to N.S., by the Simons Foundation (award ID 648614) to E.D. and N.S., and by the European Research Council (ERC-STG project Mami-639226) to M.C.C. Publisher Copyright: {\textcopyright} 2023, The Author(s).",

year = "2023",

month = feb,

day = "2",

doi = "10.1038/s41586-022-05620-1",

language = "English",

volume = "614",

pages = "125--135",

journal = "Nature",

issn = "0028-0836",

publisher = "Springer Nature",

number = "7946",

}

Valles-Colomer, M, Blanco-Míguez, A, Manghi, P, Asnicar, F, Dubois, L, Golzato, D, Armanini, F, Cumbo, F, Huang, KD, Manara, S, Masetti, G, Pinto, F, Piperni, E, Punčochář, M, Ricci, L, Zolfo, M, Farrant, O, Goncalves, A, Selma-Royo, M, Binetti, AG, Becerra, JE, Han, B, Lusingu, J, Amuasi, J, Amoroso, L, Visconti, A , Steves, CM , Falchi, M, Filosi, M, Tett, A, Last, A, Xu, Q, Qin, N, Qin, H, May, J, Eibach, D, Corrias, MV, Ponzoni, M, Pasolli, E, Spector, TD, Domenici, E, Collado, MC & Segata, N 2023, 'The person-to-person transmission landscape of the gut and oral microbiomes', Nature, vol. 614, no. 7946, pp. 125-135. https://doi.org/10.1038/s41586-022-05620-1

TY - JOUR

T1 - The person-to-person transmission landscape of the gut and oral microbiomes

AU - Valles-Colomer, Mireia

AU - Blanco-Míguez, Aitor

AU - Manghi, Paolo

AU - Asnicar, Francesco

AU - Dubois, Leonard

AU - Golzato, Davide

AU - Armanini, Federica

AU - Cumbo, Fabio

AU - Huang, Kun D

AU - Manara, Serena

AU - Masetti, Giulia

AU - Pinto, Federica

AU - Piperni, Elisa

AU - Punčochář, Michal

AU - Ricci, Liviana

AU - Zolfo, Moreno

AU - Farrant, Olivia

AU - Goncalves, Adriana

AU - Selma-Royo, Marta

AU - Binetti, Ana G

AU - Becerra, Jimmy E

AU - Han, Bei

AU - Lusingu, John

AU - Amuasi, John

AU - Amoroso, Loredana

AU - Visconti, Alessia

AU - Steves, Claire M

AU - Falchi, Mario

AU - Filosi, Michele

AU - Tett, Adrian

AU - Last, Anna

AU - Xu, Qian

AU - Qin, Nan

AU - Qin, Huanlong

AU - May, Jürgen

AU - Eibach, Daniel

AU - Corrias, Maria Valeria

AU - Ponzoni, Mirco

AU - Pasolli, Edoardo

AU - Spector, Tim D

AU - Domenici, Enrico

AU - Collado, Maria Carmen

AU - Segata, Nicola

N1 - Funding Information: We thank all study participants for their commitment; N. Volfovsky, P. Feliciano and A. Packer from the Simons Foundations for their kind support with the SPARK collection data; the LaBSSAH—CIBIO Next Generation Sequencing Facility of the University of Trento (V. de Sanctis, R. Bertorelli, P. Cavallerio and C. Valentini) for sequencing the metagenomic libraries. This work was supported by the European Research Council (ERC-STG project MetaPG-716575 and ERC-CoG microTOUCH-101045015) to N.S. and by EMBO ALTF 593–2020 to M.V.-C. The work was also partially supported by MIUR ‘Futuro in Ricerca’ (grant no. RBFR13EWWI_001) to N.S., by the European H2020 programme (ONCOBIOME-825410 project, MASTER-818368 project, and IHMCSA-964590) to N.S., by the National Cancer Institute of the National Institutes of Health (1U01CA230551) to N.S., by the Premio Internazionale Lombardia e Ricerca 2019 to N.S., by the Simons Foundation (award ID 648614) to E.D. and N.S., and by the European Research Council (ERC-STG project Mami-639226) to M.C.C. Funding Information: We thank all study participants for their commitment; N. Volfovsky, P. Feliciano and A. Packer from the Simons Foundations for their kind support with the SPARK collection data; the LaBSSAH—CIBIO Next Generation Sequencing Facility of the University of Trento (V. de Sanctis, R. Bertorelli, P. Cavallerio and C. Valentini) for sequencing the metagenomic libraries. This work was supported by the European Research Council (ERC-STG project MetaPG-716575 and ERC-CoG microTOUCH-101045015) to N.S. and by EMBO ALTF 593–2020 to M.V.-C. The work was also partially supported by MIUR ‘Futuro in Ricerca’ (grant no. RBFR13EWWI_001) to N.S., by the European H2020 programme (ONCOBIOME-825410 project, MASTER-818368 project, and IHMCSA-964590) to N.S., by the National Cancer Institute of the National Institutes of Health (1U01CA230551) to N.S., by the Premio Internazionale Lombardia e Ricerca 2019 to N.S., by the Simons Foundation (award ID 648614) to E.D. and N.S., and by the European Research Council (ERC-STG project Mami-639226) to M.C.C. Publisher Copyright: © 2023, The Author(s).

PY - 2023/2/2

Y1 - 2023/2/2

N2 - 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.

AB - 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.

KW - Female

KW - Humans

KW - Infant

KW - Bacteria/classification

KW - Gastrointestinal Microbiome/genetics

KW - Metagenome

KW - Microbiota/genetics

KW - Mothers

KW - Mouth/microbiology

KW - Infectious Disease Transmission, Vertical

KW - Family Characteristics

KW - Aging

KW - Disease Transmission, Infectious

KW - Time Factors

KW - Microbial Viability

KW - Home Environment

UR - http://www.scopus.com/inward/record.url?scp=85146395298&partnerID=8YFLogxK

U2 - 10.1038/s41586-022-05620-1

DO - 10.1038/s41586-022-05620-1

M3 - Article

C2 - 36653448

SN - 0028-0836

VL - 614

SP - 125

EP - 135

JO - Nature

JF - Nature

IS - 7946

ER -

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

Abstract

Keywords

UN SDGs

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