Developing a framework for tracking antimicrobial resistance gene movement in a persistent environmental reservoir

Abstract Mobile genetic elements are key to the global emergence of antibiotic resistance. We successfully reconstructed the complete bacterial genome and plasmid assemblies of isolates sharing the same bla KPC carbapenemase gene to understand evolution over time in six confined hospital drains over...

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Main Authors: Amy J. Mathers, Thomas J. X. Li, Qijun He, Sharvari Narendra, Nicole Stoesser, David W. Eyre, A. Sarah Walker, Katie E. Barry, Salvador Castañeda-Barba, Fenix W. Huang, Hardik Parikh, Shireen Kotay, Derrick W. Crook, Christian Reidys
Format: Article
Language:English
Published: Nature Portfolio 2024-12-01
Series:npj Antimicrobials and Resistance
Online Access:https://doi.org/10.1038/s44259-024-00069-w
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author Amy J. Mathers
Thomas J. X. Li
Qijun He
Sharvari Narendra
Nicole Stoesser
David W. Eyre
A. Sarah Walker
Katie E. Barry
Salvador Castañeda-Barba
Fenix W. Huang
Hardik Parikh
Shireen Kotay
Derrick W. Crook
Christian Reidys
author_facet Amy J. Mathers
Thomas J. X. Li
Qijun He
Sharvari Narendra
Nicole Stoesser
David W. Eyre
A. Sarah Walker
Katie E. Barry
Salvador Castañeda-Barba
Fenix W. Huang
Hardik Parikh
Shireen Kotay
Derrick W. Crook
Christian Reidys
author_sort Amy J. Mathers
collection DOAJ
description Abstract Mobile genetic elements are key to the global emergence of antibiotic resistance. We successfully reconstructed the complete bacterial genome and plasmid assemblies of isolates sharing the same bla KPC carbapenemase gene to understand evolution over time in six confined hospital drains over five years. From 82 isolates we identified 14 unique strains from 10 species with 113 bla KPC-carrying plasmids across 16 distinct replicon types. To assess dynamic gene movement, we introduced the ‘Composite-Sample Complex’, a novel mathematical approach to using probability to capture the directional movement of antimicrobial resistance genes. The Composite Sample Complex accounts for the co-occurrence of both plasmids and chromosomes within an isolate, and highlights likely gene donors and recipients. From the validated model, we demonstrate frequent transposition events of bla KPC from plasmids to other plasmids, as well as integration into the bacterial chromosome within specific drains. We present a novel approach to estimate the directional movement of antimicrobial resistance via gene mobilization.
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spelling doaj-art-55412fbe301549c48dc7ad27a7f2a76b2025-01-05T12:47:51ZengNature Portfolionpj Antimicrobials and Resistance2731-87452024-12-012111210.1038/s44259-024-00069-wDeveloping a framework for tracking antimicrobial resistance gene movement in a persistent environmental reservoirAmy J. Mathers0Thomas J. X. Li1Qijun He2Sharvari Narendra3Nicole Stoesser4David W. Eyre5A. Sarah Walker6Katie E. Barry7Salvador Castañeda-Barba8Fenix W. Huang9Hardik Parikh10Shireen Kotay11Derrick W. Crook12Christian Reidys13Division of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health SystemDivision of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health SystemBiocomplexity Institute, University of VirginiaDivision of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health SystemNuffield Department of Clinical Medicine, University of OxfordNuffield Department of Clinical Medicine, University of OxfordNuffield Department of Clinical Medicine, University of OxfordDivision of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health SystemDivision of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health SystemDivision of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health SystemDivision of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health SystemDivision of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health SystemNuffield Department of Clinical Medicine, University of OxfordBiocomplexity Institute, University of VirginiaAbstract Mobile genetic elements are key to the global emergence of antibiotic resistance. We successfully reconstructed the complete bacterial genome and plasmid assemblies of isolates sharing the same bla KPC carbapenemase gene to understand evolution over time in six confined hospital drains over five years. From 82 isolates we identified 14 unique strains from 10 species with 113 bla KPC-carrying plasmids across 16 distinct replicon types. To assess dynamic gene movement, we introduced the ‘Composite-Sample Complex’, a novel mathematical approach to using probability to capture the directional movement of antimicrobial resistance genes. The Composite Sample Complex accounts for the co-occurrence of both plasmids and chromosomes within an isolate, and highlights likely gene donors and recipients. From the validated model, we demonstrate frequent transposition events of bla KPC from plasmids to other plasmids, as well as integration into the bacterial chromosome within specific drains. We present a novel approach to estimate the directional movement of antimicrobial resistance via gene mobilization.https://doi.org/10.1038/s44259-024-00069-w
spellingShingle Amy J. Mathers
Thomas J. X. Li
Qijun He
Sharvari Narendra
Nicole Stoesser
David W. Eyre
A. Sarah Walker
Katie E. Barry
Salvador Castañeda-Barba
Fenix W. Huang
Hardik Parikh
Shireen Kotay
Derrick W. Crook
Christian Reidys
Developing a framework for tracking antimicrobial resistance gene movement in a persistent environmental reservoir
npj Antimicrobials and Resistance
title Developing a framework for tracking antimicrobial resistance gene movement in a persistent environmental reservoir
title_full Developing a framework for tracking antimicrobial resistance gene movement in a persistent environmental reservoir
title_fullStr Developing a framework for tracking antimicrobial resistance gene movement in a persistent environmental reservoir
title_full_unstemmed Developing a framework for tracking antimicrobial resistance gene movement in a persistent environmental reservoir
title_short Developing a framework for tracking antimicrobial resistance gene movement in a persistent environmental reservoir
title_sort developing a framework for tracking antimicrobial resistance gene movement in a persistent environmental reservoir
url https://doi.org/10.1038/s44259-024-00069-w
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