Enterobacterales plasmid sharing amongst human bloodstream infections, livestock, wastewater, and waterway niches in Oxfordshire, UK

  1. William Matlock  Is a corresponding author
  2. Samuel Lipworth
  3. Kevin K Chau
  4. Manal AbuOun
  5. Leanne Barker
  6. James Kavanagh
  7. Monique Andersson
  8. Sarah Oakley
  9. Marcus Morgan
  10. Derrick W Crook
  11. Daniel S Read
  12. Muna Anjum
  13. Liam P Shaw
  14. Nicole Stoesser  Is a corresponding author
  15. REHAB Consortium
  1. University of Oxford, United Kingdom
  2. Animal and Plant Health Agency, United Kingdom
  3. Oxford University Hospitals NHS Trust, United Kingdom
  4. Centre for Ecology and Hydrology, United Kingdom

Abstract

Plasmids enable the dissemination of antimicrobial resistance (AMR) in common Enterobacterales pathogens, representing a major public health challenge. However, the extent of plasmid sharing and evolution between Enterobacterales causing human infections and other niches remains unclear, including the emergence of resistance plasmids. Dense, unselected sampling is highly relevant to developing our understanding of plasmid epidemiology and designing appropriate interventions to limit the emergence and dissemination of plasmid-associated AMR. We established a geographically and temporally restricted collection of human bloodstream infection (BSI)-associated, livestock-associated (cattle, pig, poultry, and sheep faeces, farm soils) and wastewater treatment work (WwTW)-associated (influent, effluent, waterways upstream/downstream of effluent outlets) Enterobacterales. Isolates were collected between 2008-2020 from sites <60km apart in Oxfordshire, UK. Pangenome analysis of plasmid clusters revealed shared 'backbones', with phylogenies suggesting an intertwined ecology where well-conserved plasmid backbones carry diverse accessory functions, including AMR genes. Many plasmid 'backbones' were seen across species and niches, raising the possibility that plasmid movement between these followed by rapid accessory gene change could be relatively common. Overall, the signature of identical plasmid sharing is likely to be a highly transient one, implying that plasmid movement might be occurring at greater rates than previously estimated, raising a challenge for future genomic One Health studies.

Data availability

Accessions for existing BSI and REHAB reads and assemblies can be found in Lipworth et al., 2021 (BioProject PRJNA604975) and Shaw et al., 2021 (BioProject PRJNA605147) respectively. Analysis scripts can be found in the GitHub repository https://github.com/wtmatlock/oxfordshire-overlap.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. William Matlock

    Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
    For correspondence
    william.matlock@ndm.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5608-0423
  2. Samuel Lipworth

    Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Kevin K Chau

    Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Manal AbuOun

    Animal and Plant Health Agency, Addlestone, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Leanne Barker

    Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. James Kavanagh

    Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Monique Andersson

    Clinical infection, Oxford University Hospitals NHS Trust, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Sarah Oakley

    Clinical infection, Oxford University Hospitals NHS Trust, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Marcus Morgan

    Clinical infection, Oxford University Hospitals NHS Trust, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  10. Derrick W Crook

    Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0590-2850
  11. Daniel S Read

    Centre for Ecology and Hydrology, Wallingford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  12. Muna Anjum

    Animal and Plant Health Agency, Addlestone, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  13. Liam P Shaw

    Department of Biology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  14. Nicole Stoesser

    Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
    For correspondence
    nicole.stoesser@ndm.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4508-7969
  15. REHAB Consortium

Funding

Medical Research Foundation (MRF-145-0004-TPG-AVISO)

  • William Matlock

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Marc J Bonten, University Medical Center Utrecht, Netherlands

Publication history

  1. Received: December 1, 2022
  2. Accepted: March 22, 2023
  3. Accepted Manuscript published: March 24, 2023 (version 1)

Copyright

© 2023, Matlock et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. William Matlock
  2. Samuel Lipworth
  3. Kevin K Chau
  4. Manal AbuOun
  5. Leanne Barker
  6. James Kavanagh
  7. Monique Andersson
  8. Sarah Oakley
  9. Marcus Morgan
  10. Derrick W Crook
  11. Daniel S Read
  12. Muna Anjum
  13. Liam P Shaw
  14. Nicole Stoesser
  15. REHAB Consortium
(2023)
Enterobacterales plasmid sharing amongst human bloodstream infections, livestock, wastewater, and waterway niches in Oxfordshire, UK
eLife 12:e85302.
https://doi.org/10.7554/eLife.85302

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