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Strain-level characterization of broad host range mobile genetic elements transferring antibiotic resistance from the human microbiome

Author

Listed:
  • Samuel C. Forster

    (Wellcome Sanger Institute
    Centre for Innate Immunity and Infectious Diseases, Hudson Institute of Medical Research
    Monash University)

  • Junyan Liu

    (Wellcome Sanger Institute)

  • Nitin Kumar

    (Wellcome Sanger Institute)

  • Emily L. Gulliver

    (Centre for Innate Immunity and Infectious Diseases, Hudson Institute of Medical Research
    Monash University)

  • Jodee A. Gould

    (Centre for Innate Immunity and Infectious Diseases, Hudson Institute of Medical Research
    Monash University)

  • Alejandra Escobar-Zepeda

    (Wellcome Sanger Institute)

  • Tapoka Mkandawire

    (Wellcome Sanger Institute)

  • Lindsay J. Pike

    (Wellcome Sanger Institute)

  • Yan Shao

    (Wellcome Sanger Institute)

  • Mark D. Stares

    (Wellcome Sanger Institute)

  • Hilary P. Browne

    (Wellcome Sanger Institute)

  • B. Anne Neville

    (Wellcome Sanger Institute)

  • Trevor D. Lawley

    (Wellcome Sanger Institute)

Abstract

Mobile genetic elements (MGEs) carrying antibiotic resistance genes (ARGs) disseminate ARGs when they mobilise into new bacterial hosts. The nature of such horizontal gene transfer (HGT) events between human gut commensals and pathogens remain poorly characterised. Here, we compare 1354 cultured commensal strains (540 species) to 45,403 pathogen strains (12 species) and find 64,188 MGE-mediated ARG transfer events between the two groups using established methods. Among the 5931 MGEs, we find 15 broad host range elements predicted to have crossed different bacterial phyla while also occurring in animal and environmental microbiomes. We experimentally demonstrate that predicted broad host range MGEs can mobilise from commensals Dorea longicatena and Hungatella hathewayi to pathogen Klebsiella oxytoca, crossing phyla simultaneously. Our work establishes the MGE-mediated ARG dissemination network between human gut commensals and pathogens and highlights broad host range MGEs as targets for future ARG dissemination management.

Suggested Citation

  • Samuel C. Forster & Junyan Liu & Nitin Kumar & Emily L. Gulliver & Jodee A. Gould & Alejandra Escobar-Zepeda & Tapoka Mkandawire & Lindsay J. Pike & Yan Shao & Mark D. Stares & Hilary P. Browne & B. A, 2022. "Strain-level characterization of broad host range mobile genetic elements transferring antibiotic resistance from the human microbiome," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29096-9
    DOI: 10.1038/s41467-022-29096-9
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    References listed on IDEAS

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    1. Alyssa G. Kent & Albert C. Vill & Qiaojuan Shi & Michael J. Satlin & Ilana Lauren Brito, 2020. "Widespread transfer of mobile antibiotic resistance genes within individual gut microbiomes revealed through bacterial Hi-C," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    2. Catherine A. Lozupone & Jesse I. Stombaugh & Jeffrey I. Gordon & Janet K. Jansson & Rob Knight, 2012. "Diversity, stability and resilience of the human gut microbiota," Nature, Nature, vol. 489(7415), pages 220-230, September.
    3. Chris S. Smillie & Mark B. Smith & Jonathan Friedman & Otto X. Cordero & Lawrence A. David & Eric J. Alm, 2011. "Ecology drives a global network of gene exchange connecting the human microbiome," Nature, Nature, vol. 480(7376), pages 241-244, December.
    4. Yongfei Hu & Xi Yang & Junjie Qin & Na Lu & Gong Cheng & Na Wu & Yuanlong Pan & Jing Li & Liying Zhu & Xin Wang & Zhiqi Meng & Fangqing Zhao & Di Liu & Juncai Ma & Nan Qin & Chunsheng Xiang & Yonghong, 2013. "Metagenome-wide analysis of antibiotic resistance genes in a large cohort of human gut microbiota," Nature Communications, Nature, vol. 4(1), pages 1-7, October.
    5. Mostafa M. H. Ellabaan & Christian Munck & Andreas Porse & Lejla Imamovic & Morten O. A. Sommer, 2021. "Forecasting the dissemination of antibiotic resistance genes across bacterial genomes," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
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    Cited by:

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    2. Zi-Teng Liu & Rui-Ao Ma & Dong Zhu & Konstantinos T. Konstantinidis & Yong-Guan Zhu & Si-Yu Zhang, 2024. "Organic fertilization co-selects genetically linked antibiotic and metal(loid) resistance genes in global soil microbiome," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. Qiu E. Yang & Xiaodan Ma & Minchun Li & Mengshi Zhao & Lingshuang Zeng & Minzhen He & Hui Deng & Hanpeng Liao & Christopher Rensing & Ville-Petri Friman & Shungui Zhou & Timothy R. Walsh, 2024. "Evolution of triclosan resistance modulates bacterial permissiveness to multidrug resistance plasmids and phages," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    4. Peter J. Diebold & Matthew W. Rhee & Qiaojuan Shi & Nguyen Vinh Trung & Fayaz Umrani & Sheraz Ahmed & Vandana Kulkarni & Prasad Deshpande & Mallika Alexander & Ngo Hoa & Nicholas A. Christakis & Najee, 2023. "Clinically relevant antibiotic resistance genes are linked to a limited set of taxa within gut microbiome worldwide," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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