Population-level impacts of antibiotic usage on the human gut microbiome.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
02 03 2023
Historique:
received: 16 11 2021
accepted: 06 02 2023
entrez: 2 3 2023
pubmed: 3 3 2023
medline: 7 3 2023
Statut: epublish

Résumé

The widespread usage of antimicrobials has driven the evolution of resistance in pathogenic microbes, both increased prevalence of antimicrobial resistance genes (ARGs) and their spread across species by horizontal gene transfer (HGT). However, the impact on the wider community of commensal microbes associated with the human body, the microbiome, is less well understood. Small-scale studies have determined the transient impacts of antibiotic consumption but we conduct an extensive survey of ARGs in 8972 metagenomes to determine the population-level impacts. Focusing on 3096 gut microbiomes from healthy individuals not taking antibiotics we demonstrate highly significant correlations between both the total ARG abundance and diversity and per capita antibiotic usage rates across ten countries spanning three continents. Samples from China were notable outliers. We use a collection of 154,723 human-associated metagenome assembled genomes (MAGs) to link these ARGs to taxa and detect HGT. This reveals that the correlations in ARG abundance are driven by multi-species mobile ARGs shared between pathogens and commensals, within a highly connected central component of the network of MAGs and ARGs. We also observe that individual human gut ARG profiles cluster into two types or resistotypes. The less frequent resistotype has higher overall ARG abundance, is associated with certain classes of resistance, and is linked to species-specific genes in the Proteobacteria on the periphery of the ARG network.

Identifiants

pubmed: 36864029
doi: 10.1038/s41467-023-36633-7
pii: 10.1038/s41467-023-36633-7
pmc: PMC9981903
doi:

Substances chimiques

Anti-Bacterial Agents 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1191

Informations de copyright

© 2023. The Author(s).

Références

PLoS One. 2012;7(2):e30126
pubmed: 22319561
Proc Natl Acad Sci U S A. 2020 Nov 17;117(46):29063-29068
pubmed: 33139558
Nat Microbiol. 2018 Jan;3(1):8-16
pubmed: 29255284
Nature. 2016 Jul 21;535(7612):435-439
pubmed: 27409808
Lancet Microbe. 2021 Apr;2(4):e151-e158
pubmed: 33821248
Nucleic Acids Res. 2022 Jan 7;50(D1):D912-D917
pubmed: 34850947
Environ Sci Technol. 2022 Nov 1;56(21):14982-14993
pubmed: 35759608
Nat Biotechnol. 2017 Sep 12;35(9):833-844
pubmed: 28898207
Nature. 2011 May 12;473(7346):174-80
pubmed: 21508958
ISME J. 2016 Mar;10(3):707-20
pubmed: 26359913
R Soc Open Sci. 2016 Jan 20;3(1):140536
pubmed: 26909160
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
pubmed: 15034147
Bioinformatics. 2012 Dec 1;28(23):3150-2
pubmed: 23060610
Microbiol Mol Biol Rev. 2014 Mar;78(1):1-39
pubmed: 24600039
Nat Commun. 2021 Jul 7;12(1):4060
pubmed: 34234115
Nat Microbiol. 2018 Nov;3(11):1255-1265
pubmed: 30349083
Nat Methods. 2017 Oct 31;14(11):1023-1024
pubmed: 29088129
Nature. 2011 Oct 30;480(7376):241-4
pubmed: 22037308
Gut Microbes. 2014 Mar-Apr;5(2):245-9
pubmed: 24637798
Nucleic Acids Res. 2017 Jan 4;45(D1):D566-D573
pubmed: 27789705
Microbiome. 2020 Jan 7;8(1):2
pubmed: 31910889
NAR Genom Bioinform. 2021 Jan 06;3(1):lqaa109
pubmed: 33575651
Genome Res. 2013 Jul;23(7):1163-9
pubmed: 23568836
Gastroenterology. 2020 Feb;158(3):610-624.e13
pubmed: 31605691
Gut. 2019 Oct;68(10):1781-1790
pubmed: 30658995
Nat Biotechnol. 2017 Nov;35(11):1026-1028
pubmed: 29035372
Nat Rev Microbiol. 2010 Aug;8(8):552-63
pubmed: 20601965
Nat Methods. 2013 Sep;10(9):881-4
pubmed: 23892899
Philos Trans R Soc Lond B Biol Sci. 2015 Jun 5;370(1670):20140087
pubmed: 25918444
Proc Natl Acad Sci U S A. 2011 Mar 15;108 Suppl 1:4554-61
pubmed: 20847294
Nucleic Acids Res. 2015 Jan;43(Database issue):D261-9
pubmed: 25428365
ISME J. 2015 Jan;9(1):207-16
pubmed: 25003965
Elife. 2018 Dec 18;7:
pubmed: 30560781
Open Biol. 2019 Sep 27;9(9):190128
pubmed: 31506017
Microbiome. 2018 Jul 21;6(1):130
pubmed: 30031405
Methods Mol Biol. 2020;2075:265-283
pubmed: 31584169
Br J Pharmacol. 2008 Mar;153 Suppl 1:S347-57
pubmed: 18193080
Nat Commun. 2020 Sep 1;11(1):4379
pubmed: 32873785
Genome Med. 2021 Jun 7;13(1):79
pubmed: 34092249
mBio. 2018 Dec 11;9(6):
pubmed: 30538187
Nat Commun. 2019 Mar 8;10(1):1124
pubmed: 30850636
Gigascience. 2022 Jul 30;11:
pubmed: 35906888
Microbiol Mol Biol Rev. 2010 Sep;74(3):417-33
pubmed: 20805405
Science. 2006 Jan 20;311(5759):374-7
pubmed: 16424339
Gene. 2016 May 1;581(2):178-82
pubmed: 26827794
PeerJ. 2016 Oct 18;4:e2584
pubmed: 27781170
Nat Microbiol. 2019 Jan;4(1):112-123
pubmed: 30478291
Nat Methods. 2015 Jan;12(1):59-60
pubmed: 25402007
Lancet Infect Dis. 2019 Jan;19(1):56-66
pubmed: 30409683
PLoS Biol. 2016 Aug 19;14(8):e1002533
pubmed: 27541692
Nature. 2017 Nov 23;551(7681):507-511
pubmed: 29143816
PLoS One. 2010 Mar 10;5(3):e9490
pubmed: 20224823
Cell. 2019 Jan 24;176(3):649-662.e20
pubmed: 30661755
Proc Natl Acad Sci U S A. 2015 May 5;112(18):5649-54
pubmed: 25792457
BMC Bioinformatics. 2010 Mar 08;11:119
pubmed: 20211023
PLoS Med. 2016 Nov 29;13(11):e1002184
pubmed: 27898664
Bioessays. 2014 Mar;36(3):316-29
pubmed: 24474281
Philos Trans R Soc Lond B Biol Sci. 2017 Dec 5;372(1735):
pubmed: 29061896
Appl Environ Microbiol. 2016 Oct 27;82(22):6672-6681
pubmed: 27613679
Nat Commun. 2021 Apr 23;12(1):2435
pubmed: 33893312
Nucleic Acids Res. 2006 Jan 1;34(Database issue):D32-6
pubmed: 16381877

Auteurs

Kihyun Lee (K)

Department of Systems Biotechnology and Center for Antibiotic Resistome, Chung-Ang University, Anseong, 17546, Republic of Korea.
CJ Bioscience, Seoul, 04527, Republic of Korea.

Sebastien Raguideau (S)

Organisms and Ecosystems, Earlham Institute, Norwich, NR4 7UZ, UK.

Kimmo Sirén (K)

Section for Evolutionary Genomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.

Francesco Asnicar (F)

Department of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy.

Fabio Cumbo (F)

Department of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy.

Falk Hildebrand (F)

Organisms and Ecosystems, Earlham Institute, Norwich, NR4 7UZ, UK.
Gut Microbes and Health, Quadram Institute, Norwich, NR4 7UQ, UK.

Nicola Segata (N)

Department of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy.

Chang-Jun Cha (CJ)

Department of Systems Biotechnology and Center for Antibiotic Resistome, Chung-Ang University, Anseong, 17546, Republic of Korea. cjcha@cau.ac.kr.

Christopher Quince (C)

Organisms and Ecosystems, Earlham Institute, Norwich, NR4 7UZ, UK. christopher.quince@earlham.ac.uk.
Gut Microbes and Health, Quadram Institute, Norwich, NR4 7UQ, UK. christopher.quince@earlham.ac.uk.
Warwick Medical School, University of Warwick, Coventry, CV4 7HL, UK. christopher.quince@earlham.ac.uk.

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