A single Proteus mirabilis lineage from human and animal sources: a hidden reservoir of OXA-23 or OXA-58 carbapenemases in Enterobacterales

Abstract In Enterobacterales, the most common carbapenemases are Ambler’s class A (KPC-like), class B (NDM-, VIM- or IMP-like) or class D (OXA-48-like) enzymes. This study describes the characterization of twenty-four OXA-23 or OXA-58 producing-Proteus mirabilis isolates recovered from human and vet...

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Main Authors: Rémy A. Bonnin, Delphine Girlich, Agnès B. Jousset, Lauraine Gauthier, Gaëlle Cuzon, Pierre Bogaerts, Marisa Haenni, Jean-Yves Madec, Elodie Couvé-Deacon, Olivier Barraud, Nicolas Fortineau, Philippe Glaser, Youri Glupczynski, Laurent Dortet, Thierry Naas
Format: Article
Language:English
Published: Nature Portfolio 2020-06-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-020-66161-z
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author Rémy A. Bonnin
Delphine Girlich
Agnès B. Jousset
Lauraine Gauthier
Gaëlle Cuzon
Pierre Bogaerts
Marisa Haenni
Jean-Yves Madec
Elodie Couvé-Deacon
Olivier Barraud
Nicolas Fortineau
Philippe Glaser
Youri Glupczynski
Laurent Dortet
Thierry Naas
author_facet Rémy A. Bonnin
Delphine Girlich
Agnès B. Jousset
Lauraine Gauthier
Gaëlle Cuzon
Pierre Bogaerts
Marisa Haenni
Jean-Yves Madec
Elodie Couvé-Deacon
Olivier Barraud
Nicolas Fortineau
Philippe Glaser
Youri Glupczynski
Laurent Dortet
Thierry Naas
author_sort Rémy A. Bonnin
collection DOAJ
description Abstract In Enterobacterales, the most common carbapenemases are Ambler’s class A (KPC-like), class B (NDM-, VIM- or IMP-like) or class D (OXA-48-like) enzymes. This study describes the characterization of twenty-four OXA-23 or OXA-58 producing-Proteus mirabilis isolates recovered from human and veterinary samples from France and Belgium. Twenty-two P. mirabilis isolates producing either OXA-23 (n = 21) or OXA-58 (n = 1), collected between 2013 and 2018, as well as 2 reference strains isolated in 1996 and 2015 were fully sequenced. Phylogenetic analysis revealed that 22 of the 24 isolates, including the isolate from 1996, belonged to a single lineage that has disseminated in humans and animals over a long period of time. The bla OXA-23 gene was located on the chromosome and was part of a composite transposon, Tn6703, bracketed by two copies of IS15∆II. Sequencing using Pacbio long read technology of OXA-23-producing P. mirabilis VAC allowed the assembly of a 55.5-kb structure encompassing the bla OXA-23 gene in that isolate. By contrast to the bla OXA-23 genes, the bla OXA-58 gene of P. mirabilis CNR20130297 was identified on a 6-kb plasmid. The acquisition of the bla OXA-58 gene on this plasmid involved XerC-XerD recombinases. Our results suggest that a major clone of OXA-23-producing P. mirabilis is circulating in France and Belgium since 1996.
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spelling doaj.art-a61067770b2c4ff9b0017099f69997912022-12-21T23:09:55ZengNature PortfolioScientific Reports2045-23222020-06-011011910.1038/s41598-020-66161-zA single Proteus mirabilis lineage from human and animal sources: a hidden reservoir of OXA-23 or OXA-58 carbapenemases in EnterobacteralesRémy A. Bonnin0Delphine Girlich1Agnès B. Jousset2Lauraine Gauthier3Gaëlle Cuzon4Pierre Bogaerts5Marisa Haenni6Jean-Yves Madec7Elodie Couvé-Deacon8Olivier Barraud9Nicolas Fortineau10Philippe Glaser11Youri Glupczynski12Laurent Dortet13Thierry Naas14UMR 1184, Team Resist, INSERM, Paris-Saclay University, Faculty of MedicineUMR 1184, Team Resist, INSERM, Paris-Saclay University, Faculty of MedicineUMR 1184, Team Resist, INSERM, Paris-Saclay University, Faculty of MedicineUMR 1184, Team Resist, INSERM, Paris-Saclay University, Faculty of MedicineUMR 1184, Team Resist, INSERM, Paris-Saclay University, Faculty of MedicineBelgian National Reference Laboratory for Monitoring of Antimicrobial Resistance in Gram-Negative Bacteria, CHU UCL NamurUnité Antibiorésistance et Virulence Bactériennes, Université de Lyon - ANSES Laboratoire de LyonUnité Antibiorésistance et Virulence Bactériennes, Université de Lyon - ANSES Laboratoire de LyonUniversité de Limoges, INSERM, CHU LimogesUniversité de Limoges, INSERM, CHU LimogesUMR 1184, Team Resist, INSERM, Paris-Saclay University, Faculty of MedicineJoint research Unit EERA « Evolution and Ecology of Resistance to Antibiotics », Institut Pasteur-APHP-University Paris SudBelgian National Reference Laboratory for Monitoring of Antimicrobial Resistance in Gram-Negative Bacteria, CHU UCL NamurUMR 1184, Team Resist, INSERM, Paris-Saclay University, Faculty of MedicineUMR 1184, Team Resist, INSERM, Paris-Saclay University, Faculty of MedicineAbstract In Enterobacterales, the most common carbapenemases are Ambler’s class A (KPC-like), class B (NDM-, VIM- or IMP-like) or class D (OXA-48-like) enzymes. This study describes the characterization of twenty-four OXA-23 or OXA-58 producing-Proteus mirabilis isolates recovered from human and veterinary samples from France and Belgium. Twenty-two P. mirabilis isolates producing either OXA-23 (n = 21) or OXA-58 (n = 1), collected between 2013 and 2018, as well as 2 reference strains isolated in 1996 and 2015 were fully sequenced. Phylogenetic analysis revealed that 22 of the 24 isolates, including the isolate from 1996, belonged to a single lineage that has disseminated in humans and animals over a long period of time. The bla OXA-23 gene was located on the chromosome and was part of a composite transposon, Tn6703, bracketed by two copies of IS15∆II. Sequencing using Pacbio long read technology of OXA-23-producing P. mirabilis VAC allowed the assembly of a 55.5-kb structure encompassing the bla OXA-23 gene in that isolate. By contrast to the bla OXA-23 genes, the bla OXA-58 gene of P. mirabilis CNR20130297 was identified on a 6-kb plasmid. The acquisition of the bla OXA-58 gene on this plasmid involved XerC-XerD recombinases. Our results suggest that a major clone of OXA-23-producing P. mirabilis is circulating in France and Belgium since 1996.https://doi.org/10.1038/s41598-020-66161-z
spellingShingle Rémy A. Bonnin
Delphine Girlich
Agnès B. Jousset
Lauraine Gauthier
Gaëlle Cuzon
Pierre Bogaerts
Marisa Haenni
Jean-Yves Madec
Elodie Couvé-Deacon
Olivier Barraud
Nicolas Fortineau
Philippe Glaser
Youri Glupczynski
Laurent Dortet
Thierry Naas
A single Proteus mirabilis lineage from human and animal sources: a hidden reservoir of OXA-23 or OXA-58 carbapenemases in Enterobacterales
Scientific Reports
title A single Proteus mirabilis lineage from human and animal sources: a hidden reservoir of OXA-23 or OXA-58 carbapenemases in Enterobacterales
title_full A single Proteus mirabilis lineage from human and animal sources: a hidden reservoir of OXA-23 or OXA-58 carbapenemases in Enterobacterales
title_fullStr A single Proteus mirabilis lineage from human and animal sources: a hidden reservoir of OXA-23 or OXA-58 carbapenemases in Enterobacterales
title_full_unstemmed A single Proteus mirabilis lineage from human and animal sources: a hidden reservoir of OXA-23 or OXA-58 carbapenemases in Enterobacterales
title_short A single Proteus mirabilis lineage from human and animal sources: a hidden reservoir of OXA-23 or OXA-58 carbapenemases in Enterobacterales
title_sort single proteus mirabilis lineage from human and animal sources a hidden reservoir of oxa 23 or oxa 58 carbapenemases in enterobacterales
url https://doi.org/10.1038/s41598-020-66161-z
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