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Plasmid overlap and evolution between Enterobacterales isolates from bloodstream infections and non-human compartments

View ORCID ProfileWilliam Matlock, Samuel Lipworth, Kevin K. Chau, Manal Abu Oun, Leanne Barker, James Kavanagh, Monique Andersson, Sarah Oakley, Marcus Morgan, Derrick W. Crook, Daniel S. Read, Muna Anjum, Liam P. Shaw, View ORCID ProfileNicole Stoesser, REHAB Consortium
doi: https://doi.org/10.1101/2022.05.06.490774
William Matlock
1Nuffield Department of Medicine, University of Oxford, Oxford, UK
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  • For correspondence: william.matlock@ndm.ox.ac.uk nicole.stoesser@ndm.ox.ac.uk
Samuel Lipworth
1Nuffield Department of Medicine, University of Oxford, Oxford, UK
2Oxford University Hospitals NHS Foundation Trust, Oxford, UK
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Kevin K. Chau
1Nuffield Department of Medicine, University of Oxford, Oxford, UK
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Manal Abu Oun
3Animal and Plant Health Agency, Addlestone, UK
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Leanne Barker
1Nuffield Department of Medicine, University of Oxford, Oxford, UK
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James Kavanagh
1Nuffield Department of Medicine, University of Oxford, Oxford, UK
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Monique Andersson
2Oxford University Hospitals NHS Foundation Trust, Oxford, UK
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Sarah Oakley
2Oxford University Hospitals NHS Foundation Trust, Oxford, UK
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Marcus Morgan
2Oxford University Hospitals NHS Foundation Trust, Oxford, UK
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Derrick W. Crook
1Nuffield Department of Medicine, University of Oxford, Oxford, UK
2Oxford University Hospitals NHS Foundation Trust, Oxford, UK
4NIHR Health Protection Research Unit in Healthcare Associated Infections and Antimicrobial Resistance at University of Oxford in partnership with Public Health England, Oxford, UK
5NIHR Biomedical Research Centre, Oxford, UK
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Daniel S. Read
6Centre for Ecology and Hydrology, Wallingford, UK
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Muna Anjum
3Animal and Plant Health Agency, Addlestone, UK
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Liam P. Shaw
7Department of Zoology, University of Oxford, Oxford, UK
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Nicole Stoesser
1Nuffield Department of Medicine, University of Oxford, Oxford, UK
2Oxford University Hospitals NHS Foundation Trust, Oxford, UK
4NIHR Health Protection Research Unit in Healthcare Associated Infections and Antimicrobial Resistance at University of Oxford in partnership with Public Health England, Oxford, UK
5NIHR Biomedical Research Centre, Oxford, UK
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  • ORCID record for Nicole Stoesser
  • For correspondence: william.matlock@ndm.ox.ac.uk nicole.stoesser@ndm.ox.ac.uk
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Abstract

Horizontal gene transfer in Enterobacterales allows mobile genetic elements to move between strains, species, and genera. In particular, the movement of plasmids is a known route for rapid dissemination of antimicrobial resistance (AMR) genes. However, it is difficult to establish to what extent plasmids are shared between Enterobacterales causing human infections and those from non-human sources, such as livestock or the environment. While some previous studies have found only limited evidence for genetic overlap, these have often been limited in size, restricted to drug-resistant isolates, and have used fragmented genome assemblies. Here, we report a collection of geographically and temporally restricted isolates from human bloodstream infections (BSI), environmental soils, livestock (cattle, pigs, poultry, sheep), wastewater (influent, effluent), and rivers. Isolates were all collected between 2008-2018 from sampling sites <60km apart. The combined dataset contains 1,458 complete Enterobacterales genomes, including 3,697 circularised plasmids of which one third were unclassifiable. We find eight groups of near-identical plasmids seen in both human BSI and non-human isolates, of which two are conjugative F-type plasmids carrying AMR genes. We cluster plasmids based on alignment-free distances and find that 73/247 (30%) plasmid clusters contain plasmids from both human BSI and non-human isolates. Pangenome-style analyses of the 69 most prevalent clusters (1,832/3,697 plasmids) reveals sets of shared core genes alongside accessory gene repertoires. Core-gene phylogenies suggest an intertwined ecology where well-conserved putative plasmid ‘backbones’ carry diverse accessory functions, potentially linked to niche adaptation. Furthermore, we show that closely related human and non-human plasmids are frequently found across distantly related bacterial hosts. Our findings underline the importance of diverse sampling in ‘One Health’ approaches for AMR management.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://github.com/wtmatlock/oxfordshire-overlap

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Plasmid overlap and evolution between Enterobacterales isolates from bloodstream infections and non-human compartments
William Matlock, Samuel Lipworth, Kevin K. Chau, Manal Abu Oun, Leanne Barker, James Kavanagh, Monique Andersson, Sarah Oakley, Marcus Morgan, Derrick W. Crook, Daniel S. Read, Muna Anjum, Liam P. Shaw, Nicole Stoesser, REHAB Consortium
bioRxiv 2022.05.06.490774; doi: https://doi.org/10.1101/2022.05.06.490774
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Plasmid overlap and evolution between Enterobacterales isolates from bloodstream infections and non-human compartments
William Matlock, Samuel Lipworth, Kevin K. Chau, Manal Abu Oun, Leanne Barker, James Kavanagh, Monique Andersson, Sarah Oakley, Marcus Morgan, Derrick W. Crook, Daniel S. Read, Muna Anjum, Liam P. Shaw, Nicole Stoesser, REHAB Consortium
bioRxiv 2022.05.06.490774; doi: https://doi.org/10.1101/2022.05.06.490774

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