The plasmidome associated with Gram-negative bloodstream infections: A large-scale observational study using complete plasmid assemblies

Abstract Plasmids carry genes conferring antimicrobial resistance and other clinically important traits, and contribute to the rapid dissemination of such genes. Previous studies using complete plasmid assemblies, which are essential for reliable inference, have been small and/or limited to plasmids...

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Main Authors: Samuel Lipworth, William Matlock, Liam Shaw, Karina-Doris Vihta, Gillian Rodger, Kevin Chau, Leanne Barker, Sophie George, James Kavanagh, Timothy Davies, Alison Vaughan, Monique Andersson, Katie Jeffery, Sarah Oakley, Marcus Morgan, Susan Hopkins, Timothy Peto, Derrick Crook, A. Sarah Walker, Nicole Stoesser
Format: Article
Language:English
Published: Nature Portfolio 2024-02-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-45761-7
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author Samuel Lipworth
William Matlock
Liam Shaw
Karina-Doris Vihta
Gillian Rodger
Kevin Chau
Leanne Barker
Sophie George
James Kavanagh
Timothy Davies
Alison Vaughan
Monique Andersson
Katie Jeffery
Sarah Oakley
Marcus Morgan
Susan Hopkins
Timothy Peto
Derrick Crook
A. Sarah Walker
Nicole Stoesser
author_facet Samuel Lipworth
William Matlock
Liam Shaw
Karina-Doris Vihta
Gillian Rodger
Kevin Chau
Leanne Barker
Sophie George
James Kavanagh
Timothy Davies
Alison Vaughan
Monique Andersson
Katie Jeffery
Sarah Oakley
Marcus Morgan
Susan Hopkins
Timothy Peto
Derrick Crook
A. Sarah Walker
Nicole Stoesser
author_sort Samuel Lipworth
collection DOAJ
description Abstract Plasmids carry genes conferring antimicrobial resistance and other clinically important traits, and contribute to the rapid dissemination of such genes. Previous studies using complete plasmid assemblies, which are essential for reliable inference, have been small and/or limited to plasmids carrying antimicrobial resistance genes (ARGs). In this study, we sequenced 1,880 complete plasmids from 738 isolates from bloodstream infections in Oxfordshire, UK. The bacteria had been originally isolated in 2009 (194 isolates) and 2018 (368 isolates), plus a stratified selection from intervening years (176 isolates). We demonstrate that plasmids are largely, but not entirely, constrained to a single host species, although there is substantial overlap between species of plasmid gene-repertoire. Most ARGs are carried by a relatively small number of plasmid groups with biological features that are predictable. Plasmids carrying ARGs (including those encoding carbapenemases) share a putative ‘backbone’ of core genes with those carrying no such genes. These findings suggest that future surveillance should, in addition to tracking plasmids currently associated with clinically important genes, focus on identifying and monitoring the dissemination of high-risk plasmid groups with the potential to rapidly acquire and disseminate these genes.
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spelling doaj.art-c56d4a213dff4d18a116a92ca0f309492024-04-14T11:22:07ZengNature PortfolioNature Communications2041-17232024-02-0115111110.1038/s41467-024-45761-7The plasmidome associated with Gram-negative bloodstream infections: A large-scale observational study using complete plasmid assembliesSamuel Lipworth0William Matlock1Liam Shaw2Karina-Doris Vihta3Gillian Rodger4Kevin Chau5Leanne Barker6Sophie George7James Kavanagh8Timothy Davies9Alison Vaughan10Monique Andersson11Katie Jeffery12Sarah Oakley13Marcus Morgan14Susan Hopkins15Timothy Peto16Derrick Crook17A. Sarah Walker18Nicole Stoesser19Nuffield Department of Medicine, University of OxfordNuffield Department of Medicine, University of OxfordDepartment of Zoology, University of OxfordDepartment of Engineering Science, University of OxfordNuffield Department of Medicine, University of OxfordNuffield Department of Medicine, University of OxfordNuffield Department of Medicine, University of OxfordNuffield Department of Medicine, University of OxfordNuffield Department of Medicine, University of OxfordNuffield Department of Medicine, University of OxfordNuffield Department of Medicine, University of OxfordOxford University Hospitals NHS Foundation TrustOxford University Hospitals NHS Foundation TrustOxford University Hospitals NHS Foundation TrustOxford University Hospitals NHS Foundation TrustNational Infection Service, United Kingdom Health Security AgencyNuffield Department of Medicine, University of OxfordNuffield Department of Medicine, University of OxfordNuffield Department of Medicine, University of OxfordNuffield Department of Medicine, University of OxfordAbstract Plasmids carry genes conferring antimicrobial resistance and other clinically important traits, and contribute to the rapid dissemination of such genes. Previous studies using complete plasmid assemblies, which are essential for reliable inference, have been small and/or limited to plasmids carrying antimicrobial resistance genes (ARGs). In this study, we sequenced 1,880 complete plasmids from 738 isolates from bloodstream infections in Oxfordshire, UK. The bacteria had been originally isolated in 2009 (194 isolates) and 2018 (368 isolates), plus a stratified selection from intervening years (176 isolates). We demonstrate that plasmids are largely, but not entirely, constrained to a single host species, although there is substantial overlap between species of plasmid gene-repertoire. Most ARGs are carried by a relatively small number of plasmid groups with biological features that are predictable. Plasmids carrying ARGs (including those encoding carbapenemases) share a putative ‘backbone’ of core genes with those carrying no such genes. These findings suggest that future surveillance should, in addition to tracking plasmids currently associated with clinically important genes, focus on identifying and monitoring the dissemination of high-risk plasmid groups with the potential to rapidly acquire and disseminate these genes.https://doi.org/10.1038/s41467-024-45761-7
spellingShingle Samuel Lipworth
William Matlock
Liam Shaw
Karina-Doris Vihta
Gillian Rodger
Kevin Chau
Leanne Barker
Sophie George
James Kavanagh
Timothy Davies
Alison Vaughan
Monique Andersson
Katie Jeffery
Sarah Oakley
Marcus Morgan
Susan Hopkins
Timothy Peto
Derrick Crook
A. Sarah Walker
Nicole Stoesser
The plasmidome associated with Gram-negative bloodstream infections: A large-scale observational study using complete plasmid assemblies
Nature Communications
title The plasmidome associated with Gram-negative bloodstream infections: A large-scale observational study using complete plasmid assemblies
title_full The plasmidome associated with Gram-negative bloodstream infections: A large-scale observational study using complete plasmid assemblies
title_fullStr The plasmidome associated with Gram-negative bloodstream infections: A large-scale observational study using complete plasmid assemblies
title_full_unstemmed The plasmidome associated with Gram-negative bloodstream infections: A large-scale observational study using complete plasmid assemblies
title_short The plasmidome associated with Gram-negative bloodstream infections: A large-scale observational study using complete plasmid assemblies
title_sort plasmidome associated with gram negative bloodstream infections a large scale observational study using complete plasmid assemblies
url https://doi.org/10.1038/s41467-024-45761-7
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