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 Publishing Group 2020-06-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-020-66161-z
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spelling doaj-a61067770b2c4ff9b0017099f69997912021-06-13T11:48:10ZengNature Publishing GroupScientific 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
collection DOAJ
language English
format Article
sources DOAJ
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
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
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
title 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_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_sort single proteus mirabilis lineage from human and animal sources: a hidden reservoir of oxa-23 or oxa-58 carbapenemases in enterobacterales
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2020-06-01
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.
url https://doi.org/10.1038/s41598-020-66161-z
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