Elevated rates of horizontal gene transfer in the industrialized human microbiome

Mathieu Groussin; Mathilde Poyet; Ainara Sistiaga; Sean M. Kearney; Katya Moniz; Mary Noel; Jeff Hooker; Sean M. Gibbons; Laure Segurel; Alain Froment; Rihlat Said Mohamed; Alain Fezeu; Vanessa A. Juimo; Sophie Lafosse; Francis E. Tabe; Catherine Girard; Deborah Iqaluk; Le Thanh Tu Nguyen; B. Jesse Shapiro; Jenni Lehtimäki; Lasse Ruokolainen; Pinja P. Kettunen; Tommi Vatanen; Shani Sigwazi; Audax Mabulla; Manuel Domínguez-Rodrigo; Yvonne A. Nartey; Adwoa Agyei-Nkansah; Amoako Duah; Yaw A. Awuku; Kenneth A. Valles; Shadrack O. Asibey; Mary Y. Afihene; Lewis R. Roberts; Amelie Plymoth; Charles A. Onyekwere; Roger E. Summons; Ramnik J. Xavier; Eric J. Alm

doi:10.1016/j.cell.2021.02.052

Elevated rates of horizontal gene transfer in the industrialized human microbiome

Mathieu Groussin^*, Mathilde Poyet, Ainara Sistiaga, Sean M. Kearney, Katya Moniz, Mary Noel, Jeff Hooker, Sean M. Gibbons, Laure Segurel, Alain Froment, Rihlat Said Mohamed, Alain Fezeu, Vanessa A. Juimo, Sophie Lafosse, Francis E. Tabe, Catherine Girard, Deborah Iqaluk, Le Thanh Tu Nguyen, B. Jesse Shapiro, Jenni LehtimäkiLasse Ruokolainen, Pinja P. Kettunen, Tommi Vatanen, Shani Sigwazi, Audax Mabulla, Manuel Domínguez-Rodrigo, Yvonne A. Nartey, Adwoa Agyei-Nkansah, Amoako Duah, Yaw A. Awuku, Kenneth A. Valles, Shadrack O. Asibey, Mary Y. Afihene, Lewis R. Roberts, Amelie Plymoth, Charles A. Onyekwere, Roger E. Summons, Ramnik J. Xavier, Eric J. Alm

^*Corresponding author for this work

Section for Hologenomics

Research output: Contribution to journal › Journal article › Research › peer-review

184 Citations (Scopus)

41 Downloads (Pure)

Abstract

Industrialization has impacted the human gut ecosystem, resulting in altered microbiome composition and diversity. Whether bacterial genomes may also adapt to the industrialization of their host populations remains largely unexplored. Here, we investigate the extent to which the rates and targets of horizontal gene transfer (HGT) vary across thousands of bacterial strains from 15 human populations spanning a range of industrialization. We show that HGTs have accumulated in the microbiome over recent host generations and that HGT occurs at high frequency within individuals. Comparison across human populations reveals that industrialized lifestyles are associated with higher HGT rates and that the functions of HGTs are related to the level of host industrialization. Our results suggest that gut bacteria continuously acquire new functionality based on host lifestyle and that high rates of HGT may be a recent development in human history linked to industrialization.

Original language	English
Journal	Cell
Volume	184
Issue number	8
Pages (from-to)	2053-2067.e18
ISSN	0092-8674
DOIs	https://doi.org/10.1016/j.cell.2021.02.052
Publication status	Published - 2021

Keywords

antimicrobial resistance
bacterial genomics
culturomics
horizontal gene transfer
host-microbe interactions
human gut microbiome
industrialization
lifestyle
urbanization
virulence

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10.1016/j.cell.2021.02.052Licence: CC BY-NC-ND

Elevated rates of horizontal gene transfer in the industrialized human microbiomeFinal published version, 31.1 MBLicence: CC BY-NC-ND

Cite this

Groussin, M., Poyet, M., Sistiaga, A., Kearney, S. M., Moniz, K., Noel, M., Hooker, J., Gibbons, S. M., Segurel, L., Froment, A., Mohamed, R. S., Fezeu, A., Juimo, V. A., Lafosse, S., Tabe, F. E., Girard, C., Iqaluk, D., Nguyen, L. T. T., Shapiro, B. J., ... Alm, E. J. (2021). Elevated rates of horizontal gene transfer in the industrialized human microbiome. Cell, 184(8), 2053-2067.e18. https://doi.org/10.1016/j.cell.2021.02.052

Groussin, M, Poyet, M, Sistiaga, A, Kearney, SM, Moniz, K, Noel, M, Hooker, J, Gibbons, SM, Segurel, L, Froment, A, Mohamed, RS, Fezeu, A, Juimo, VA, Lafosse, S, Tabe, FE, Girard, C, Iqaluk, D, Nguyen, LTT, Shapiro, BJ, Lehtimäki, J, Ruokolainen, L, Kettunen, PP, Vatanen, T, Sigwazi, S, Mabulla, A, Domínguez-Rodrigo, M, Nartey, YA, Agyei-Nkansah, A, Duah, A, Awuku, YA, Valles, KA, Asibey, SO, Afihene, MY, Roberts, LR, Plymoth, A, Onyekwere, CA, Summons, RE, Xavier, RJ & Alm, EJ 2021, 'Elevated rates of horizontal gene transfer in the industrialized human microbiome', Cell, vol. 184, no. 8, pp. 2053-2067.e18. https://doi.org/10.1016/j.cell.2021.02.052

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title = "Elevated rates of horizontal gene transfer in the industrialized human microbiome",

abstract = "Industrialization has impacted the human gut ecosystem, resulting in altered microbiome composition and diversity. Whether bacterial genomes may also adapt to the industrialization of their host populations remains largely unexplored. Here, we investigate the extent to which the rates and targets of horizontal gene transfer (HGT) vary across thousands of bacterial strains from 15 human populations spanning a range of industrialization. We show that HGTs have accumulated in the microbiome over recent host generations and that HGT occurs at high frequency within individuals. Comparison across human populations reveals that industrialized lifestyles are associated with higher HGT rates and that the functions of HGTs are related to the level of host industrialization. Our results suggest that gut bacteria continuously acquire new functionality based on host lifestyle and that high rates of HGT may be a recent development in human history linked to industrialization.",

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author = "Mathieu Groussin and Mathilde Poyet and Ainara Sistiaga and Kearney, {Sean M.} and Katya Moniz and Mary Noel and Jeff Hooker and Gibbons, {Sean M.} and Laure Segurel and Alain Froment and Mohamed, {Rihlat Said} and Alain Fezeu and Juimo, {Vanessa A.} and Sophie Lafosse and Tabe, {Francis E.} and Catherine Girard and Deborah Iqaluk and Nguyen, {Le Thanh Tu} and Shapiro, {B. Jesse} and Jenni Lehtim{\"a}ki and Lasse Ruokolainen and Kettunen, {Pinja P.} and Tommi Vatanen and Shani Sigwazi and Audax Mabulla and Manuel Dom{\'i}nguez-Rodrigo and Nartey, {Yvonne A.} and Adwoa Agyei-Nkansah and Amoako Duah and Awuku, {Yaw A.} and Valles, {Kenneth A.} and Asibey, {Shadrack O.} and Afihene, {Mary Y.} and Roberts, {Lewis R.} and Amelie Plymoth and Onyekwere, {Charles A.} and Summons, {Roger E.} and Xavier, {Ramnik J.} and Alm, {Eric J.}",

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AU - Groussin, Mathieu

AU - Poyet, Mathilde

AU - Sistiaga, Ainara

AU - Kearney, Sean M.

AU - Moniz, Katya

AU - Noel, Mary

AU - Hooker, Jeff

AU - Gibbons, Sean M.

AU - Segurel, Laure

AU - Froment, Alain

AU - Mohamed, Rihlat Said

AU - Fezeu, Alain

AU - Juimo, Vanessa A.

AU - Lafosse, Sophie

AU - Tabe, Francis E.

AU - Girard, Catherine

AU - Iqaluk, Deborah

AU - Nguyen, Le Thanh Tu

AU - Shapiro, B. Jesse

AU - Lehtimäki, Jenni

AU - Ruokolainen, Lasse

AU - Kettunen, Pinja P.

AU - Vatanen, Tommi

AU - Sigwazi, Shani

AU - Mabulla, Audax

AU - Domínguez-Rodrigo, Manuel

AU - Nartey, Yvonne A.

AU - Agyei-Nkansah, Adwoa

AU - Duah, Amoako

AU - Awuku, Yaw A.

AU - Valles, Kenneth A.

AU - Asibey, Shadrack O.

AU - Afihene, Mary Y.

AU - Roberts, Lewis R.

AU - Plymoth, Amelie

AU - Onyekwere, Charles A.

AU - Summons, Roger E.

AU - Xavier, Ramnik J.

AU - Alm, Eric J.

PY - 2021

Y1 - 2021

N2 - Industrialization has impacted the human gut ecosystem, resulting in altered microbiome composition and diversity. Whether bacterial genomes may also adapt to the industrialization of their host populations remains largely unexplored. Here, we investigate the extent to which the rates and targets of horizontal gene transfer (HGT) vary across thousands of bacterial strains from 15 human populations spanning a range of industrialization. We show that HGTs have accumulated in the microbiome over recent host generations and that HGT occurs at high frequency within individuals. Comparison across human populations reveals that industrialized lifestyles are associated with higher HGT rates and that the functions of HGTs are related to the level of host industrialization. Our results suggest that gut bacteria continuously acquire new functionality based on host lifestyle and that high rates of HGT may be a recent development in human history linked to industrialization.

AB - Industrialization has impacted the human gut ecosystem, resulting in altered microbiome composition and diversity. Whether bacterial genomes may also adapt to the industrialization of their host populations remains largely unexplored. Here, we investigate the extent to which the rates and targets of horizontal gene transfer (HGT) vary across thousands of bacterial strains from 15 human populations spanning a range of industrialization. We show that HGTs have accumulated in the microbiome over recent host generations and that HGT occurs at high frequency within individuals. Comparison across human populations reveals that industrialized lifestyles are associated with higher HGT rates and that the functions of HGTs are related to the level of host industrialization. Our results suggest that gut bacteria continuously acquire new functionality based on host lifestyle and that high rates of HGT may be a recent development in human history linked to industrialization.

KW - antimicrobial resistance

KW - bacterial genomics

KW - culturomics

KW - horizontal gene transfer

KW - host-microbe interactions

KW - human gut microbiome

KW - industrialization

KW - lifestyle

KW - urbanization

KW - virulence

U2 - 10.1016/j.cell.2021.02.052

DO - 10.1016/j.cell.2021.02.052

M3 - Journal article

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AN - SCOPUS:85104057213

SN - 0092-8674

VL - 184

SP - 2053-2067.e18

JO - Cell

JF - Cell

IS - 8

ER -