Elevated rates of horizontal gene transfer in the industrialized human microbiome

Elevated rates of horizontal gene transfer in the industrialized human microbiome

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...

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Published in:Cell Vol. 184; no. 8; pp. 2053 - 2067.e18
Main Authors: Groussin, Mathieu, Poyet, Mathilde, Sistiaga, Ainara, Kearney, Sean M., Moniz, Katya, Noel, Mary, Hooker, Jeff, Gibbons, Sean M., Segurel, Laure, Froment, Alain, Mohamed, Rihlat Said, Fezeu, Alain, Juimo, Vanessa A., Lafosse, Sophie, Tabe, Francis E., Girard, Catherine, Iqaluk, Deborah, Nguyen, Le Thanh Tu, Shapiro, B. Jesse, Lehtimäki, Jenni, Ruokolainen, Lasse, Kettunen, Pinja P., Vatanen, Tommi, Sigwazi, Shani, Mabulla, Audax, Domínguez-Rodrigo, Manuel, Nartey, Yvonne A., Agyei-Nkansah, Adwoa, Duah, Amoako, Awuku, Yaw A., Valles, Kenneth A., Asibey, Shadrack O., Afihene, Mary Y., Roberts, Lewis R., Plymoth, Amelie, Onyekwere, Charles A., Summons, Roger E., Xavier, Ramnik J., Alm, Eric J.
Format: Journal Article
Language:English
Published: United States Elsevier Inc 15-04-2021
Elsevier
Subjects:
antimicrobial resistance
bacterial genomics
culturomics
horizontal gene transfer
host-microbe interactions
human gut microbiome
industrialization
Life Sciences
lifestyle
Medicin och hälsovetenskap
urbanization
virulence
bacterial genomics
virulence
antimicrobial resistance
host-microbe interactions
urbanization
horizontal gene transfer
culturomics
human gut microbiome
industrialization
lifestyle
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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. [Display omitted] •Thousands of gut bacterial genomes from worldwide human populations were sequenced•HGT occurs at high frequency in the gut microbiome of individual persons•HGT occurs more frequently in the microbiome of industrialized and urban populations•Transferred gene functions in the microbiome reflect the lifestyle of the host A worldwide microbiome analysis from 15 populations along the industrialization gradient reveals that horizontal gene transfer occurs on short timescales and that microbiomes continuously acquire new functionality based on host lifestyle.
AbstractList 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.
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. [Display omitted] •Thousands of gut bacterial genomes from worldwide human populations were sequenced•HGT occurs at high frequency in the gut microbiome of individual persons•HGT occurs more frequently in the microbiome of industrialized and urban populations•Transferred gene functions in the microbiome reflect the lifestyle of the host A worldwide microbiome analysis from 15 populations along the industrialization gradient reveals that horizontal gene transfer occurs on short timescales and that microbiomes continuously acquire new functionality based on host lifestyle.
Author Gibbons, Sean M.
Sigwazi, Shani
Domínguez-Rodrigo, Manuel
Awuku, Yaw A.
Nguyen, Le Thanh Tu
Vatanen, Tommi
Iqaluk, Deborah
Valles, Kenneth A.
Alm, Eric J.
Onyekwere, Charles A.
Poyet, Mathilde
Sistiaga, Ainara
Juimo, Vanessa A.
Ruokolainen, Lasse
Kearney, Sean M.
Hooker, Jeff
Moniz, Katya
Summons, Roger E.
Agyei-Nkansah, Adwoa
Girard, Catherine
Groussin, Mathieu
Mabulla, Audax
Asibey, Shadrack O.
Lehtimäki, Jenni
Froment, Alain
Nartey, Yvonne A.
Afihene, Mary Y.
Tabe, Francis E.
Mohamed, Rihlat Said
Segurel, Laure
Plymoth, Amelie
Xavier, Ramnik J.
Fezeu, Alain
Shapiro, B. Jesse
Noel, Mary
Lafosse, Sophie
Roberts, Lewis R.
Kettunen, Pinja P.
Duah, Amoako
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  surname: Mohamed
  fullname: Mohamed, Rihlat Said
  organization: SA MRC / Wits Developmental Pathways for Health Research Unit, Department of Paediatrics, School of Clinical Medicine, Faculty of Health Sciences, University of Witwatersrand, Johannesburg, South Africa
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/33794144$$D View this record in MEDLINE/PubMed
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Issue 8
Keywords bacterial genomics
virulence
antimicrobial resistance
host-microbe interactions
urbanization
horizontal gene transfer
culturomics
human gut microbiome
industrialization
lifestyle
Language English
License This is an open access article under the CC BY-NC-ND license.
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Snippet Industrialization has impacted the human gut ecosystem, resulting in altered microbiome composition and diversity. Whether bacterial genomes may also adapt to...
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SubjectTerms antimicrobial resistance
bacterial genomics
culturomics
horizontal gene transfer
host-microbe interactions
human gut microbiome
industrialization
Life Sciences
lifestyle
Medicin och hälsovetenskap
urbanization
virulence
Title Elevated rates of horizontal gene transfer in the industrialized human microbiome
URI https://dx.doi.org/10.1016/j.cell.2021.02.052
https://www.ncbi.nlm.nih.gov/pubmed/33794144
https://u-paris.hal.science/hal-03247961
http://kipublications.ki.se/Default.aspx?queryparsed=id:146455682
Volume 184
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