Enterobacterales plasmid sharing amongst human bloodstream infections, livestock, wastewater, and waterway niches in Oxfordshire, UK
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 t...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2023-03-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/85302 |
| _version_ | 1827593207882448896 |
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| author | William Matlock Samuel Lipworth Kevin K Chau Manal AbuOun 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 |
| author_facet | William Matlock Samuel Lipworth Kevin K Chau Manal AbuOun 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 |
| author_sort | William Matlock |
| collection | DOAJ |
| description | 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 essential 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 and 2020 from sites <60 km 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. |
| first_indexed | 2024-03-09T02:07:09Z |
| format | Article |
| id | doaj.art-e3bd1e1c87d8403d99468a1752dfeab3 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-03-09T02:07:09Z |
| publishDate | 2023-03-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-e3bd1e1c87d8403d99468a1752dfeab32023-12-07T16:13:17ZengeLife Sciences Publications LtdeLife2050-084X2023-03-011210.7554/eLife.85302Enterobacterales plasmid sharing amongst human bloodstream infections, livestock, wastewater, and waterway niches in Oxfordshire, UKWilliam Matlock0https://orcid.org/0000-0001-5608-0423Samuel Lipworth1Kevin K Chau2Manal AbuOun3Leanne Barker4James Kavanagh5Monique Andersson6Sarah Oakley7Marcus Morgan8Derrick W Crook9https://orcid.org/0000-0002-0590-2850Daniel S Read10Muna Anjum11Liam P Shaw12Nicole Stoesser13https://orcid.org/0000-0002-4508-7969REHAB ConsortiumNuffield Department of Medicine, University of Oxford, Oxford, United KingdomNuffield Department of Medicine, University of Oxford, Oxford, United Kingdom; Oxford University Hospitals NHS Trust, Oxford, United KingdomNuffield Department of Medicine, University of Oxford, Oxford, United KingdomAnimal and Plant Health Agency, Addlestone, United KingdomNuffield Department of Medicine, University of Oxford, Oxford, United KingdomNuffield Department of Medicine, University of Oxford, Oxford, United KingdomOxford University Hospitals NHS Trust, Oxford, United KingdomOxford University Hospitals NHS Trust, Oxford, United KingdomOxford University Hospitals NHS Trust, Oxford, United KingdomNuffield Department of Medicine, University of Oxford, Oxford, United Kingdom; Oxford University Hospitals NHS Trust, Oxford, United Kingdom; NIHR Biomedical Research Centre, Oxford, United KingdomCentre for Ecology and Hydrology, Wallingford, United KingdomAnimal and Plant Health Agency, Addlestone, United KingdomDepartment of Biology, University of Oxford, Oxford, United KingdomNuffield Department of Medicine, University of Oxford, Oxford, United Kingdom; Oxford University Hospitals NHS Trust, Oxford, United Kingdom; NIHR Biomedical Research Centre, Oxford, United KingdomPlasmids 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 essential 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 and 2020 from sites <60 km 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.https://elifesciences.org/articles/85302plasmidEnterobacteralesantimicrobial resistancebloodstream infectionsOne Healthgenomic epidemiology |
| spellingShingle | William Matlock Samuel Lipworth Kevin K Chau Manal AbuOun 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 Enterobacterales plasmid sharing amongst human bloodstream infections, livestock, wastewater, and waterway niches in Oxfordshire, UK eLife plasmid Enterobacterales antimicrobial resistance bloodstream infections One Health genomic epidemiology |
| title | Enterobacterales plasmid sharing amongst human bloodstream infections, livestock, wastewater, and waterway niches in Oxfordshire, UK |
| title_full | Enterobacterales plasmid sharing amongst human bloodstream infections, livestock, wastewater, and waterway niches in Oxfordshire, UK |
| title_fullStr | Enterobacterales plasmid sharing amongst human bloodstream infections, livestock, wastewater, and waterway niches in Oxfordshire, UK |
| title_full_unstemmed | Enterobacterales plasmid sharing amongst human bloodstream infections, livestock, wastewater, and waterway niches in Oxfordshire, UK |
| title_short | Enterobacterales plasmid sharing amongst human bloodstream infections, livestock, wastewater, and waterway niches in Oxfordshire, UK |
| title_sort | enterobacterales plasmid sharing amongst human bloodstream infections livestock wastewater and waterway niches in oxfordshire uk |
| topic | plasmid Enterobacterales antimicrobial resistance bloodstream infections One Health genomic epidemiology |
| url | https://elifesciences.org/articles/85302 |
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