Undetectable Production of the VIM-1 Carbapenemase in an Atlantibacter hermannii Clinical Isolate

The differential expression of VIM-1 in Atlantibacter hermannii WEB-2 and Enterobacter hormaechei ssp. hoffmannii WEB-1 clinical isolates from a rectal swab of a hospitalized patient in France was investigated. A. hermannii WEB-2 was resistant to all β-lactams except carbapenems. It produced ESBL SH...

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Main Authors: Delphine Girlich, Rémy A. Bonnin, Alexis Proust, Thierry Naas, Laurent Dortet
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-12-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.741972/full
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author Delphine Girlich
Rémy A. Bonnin
Rémy A. Bonnin
Alexis Proust
Thierry Naas
Thierry Naas
Thierry Naas
Laurent Dortet
Laurent Dortet
Laurent Dortet
author_facet Delphine Girlich
Rémy A. Bonnin
Rémy A. Bonnin
Alexis Proust
Thierry Naas
Thierry Naas
Thierry Naas
Laurent Dortet
Laurent Dortet
Laurent Dortet
author_sort Delphine Girlich
collection DOAJ
description The differential expression of VIM-1 in Atlantibacter hermannii WEB-2 and Enterobacter hormaechei ssp. hoffmannii WEB-1 clinical isolates from a rectal swab of a hospitalized patient in France was investigated. A. hermannii WEB-2 was resistant to all β-lactams except carbapenems. It produced ESBL SHV-12, but the Carba NP test failed to detect any carbapenemase activity despite the production of VIM-1. Conversely, E. hormaechei WEB-1, previously recovered from the same patient, was positive for the detection of carbapenemase activity. The blaVIM–1 gene was located on a plasmid and embedded within class 1 integron. Both plasmids were of the same IncA incompatibility group and conferred the same resistance pattern when electroporated in Escherichia coli TOP10 or Enterobacter cloacae CIP7933. Quantitative RT-PCR experiments indicated a weaker replication of pWEB-2 in A. hermannii as compared to E. hormaechei. An isogenic mutant of A. hermannii WEB-2 selected after sequential passages with increased concentrations of imipenem possessed higher MICs for carbapenems and cephalosporins including cefiderocol, higher levels of the blaVIM–1 gene transcripts, and detectable carbapenemase activity using the Carba NP test. Assessment of read coverage demonstrated that a duplication of the region surrounding blaVIM–1 gene occurred in the A. hermannii mutant with detectable carbapenemase activity. The lack of detection of the VIM-1 carbapenemase activity in A. hermannii WEB-2 isolate was likely due to a weak replication of the IncA plasmid harboring the blaVIM–1 gene. Imipenem as selective pressure led to a duplication of this gene on the plasmid and to the restoration of a significant carbapenem-hydrolyzing phenotype.
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spelling doaj.art-04df141b9f8f4794ac245194670cb8b92022-12-21T18:46:00ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-12-011210.3389/fmicb.2021.741972741972Undetectable Production of the VIM-1 Carbapenemase in an Atlantibacter hermannii Clinical IsolateDelphine Girlich0Rémy A. Bonnin1Rémy A. Bonnin2Alexis Proust3Thierry Naas4Thierry Naas5Thierry Naas6Laurent Dortet7Laurent Dortet8Laurent Dortet9LabEx Lermit, Faculty of Medicine, INSERM UMR 1184—Team RESIST, Université Paris-Sud, Université Paris-Saclay, Le Kremlin-Bicêtre, FranceLabEx Lermit, Faculty of Medicine, INSERM UMR 1184—Team RESIST, Université Paris-Sud, Université Paris-Saclay, Le Kremlin-Bicêtre, FranceAssociated French National Reference Center for Antibiotic Resistance: Carbapenemase-Producing Enterobacteriaceae, Le Kremlin-Bicêtre, FranceDepartment of Hormonal Biochemistry, Hôpital de Bicêtre, Assistance Publique—Hôpitaux de Paris, Le Kremlin-Bicêtre, FranceLabEx Lermit, Faculty of Medicine, INSERM UMR 1184—Team RESIST, Université Paris-Sud, Université Paris-Saclay, Le Kremlin-Bicêtre, FranceAssociated French National Reference Center for Antibiotic Resistance: Carbapenemase-Producing Enterobacteriaceae, Le Kremlin-Bicêtre, FranceBacteriology-Hygiene Unit, Assistance Publique - Hôpitaux de Paris, Bicêtre Hospital, Le Kremlin-Bicêtre, FranceLabEx Lermit, Faculty of Medicine, INSERM UMR 1184—Team RESIST, Université Paris-Sud, Université Paris-Saclay, Le Kremlin-Bicêtre, FranceAssociated French National Reference Center for Antibiotic Resistance: Carbapenemase-Producing Enterobacteriaceae, Le Kremlin-Bicêtre, FranceBacteriology-Hygiene Unit, Assistance Publique - Hôpitaux de Paris, Bicêtre Hospital, Le Kremlin-Bicêtre, FranceThe differential expression of VIM-1 in Atlantibacter hermannii WEB-2 and Enterobacter hormaechei ssp. hoffmannii WEB-1 clinical isolates from a rectal swab of a hospitalized patient in France was investigated. A. hermannii WEB-2 was resistant to all β-lactams except carbapenems. It produced ESBL SHV-12, but the Carba NP test failed to detect any carbapenemase activity despite the production of VIM-1. Conversely, E. hormaechei WEB-1, previously recovered from the same patient, was positive for the detection of carbapenemase activity. The blaVIM–1 gene was located on a plasmid and embedded within class 1 integron. Both plasmids were of the same IncA incompatibility group and conferred the same resistance pattern when electroporated in Escherichia coli TOP10 or Enterobacter cloacae CIP7933. Quantitative RT-PCR experiments indicated a weaker replication of pWEB-2 in A. hermannii as compared to E. hormaechei. An isogenic mutant of A. hermannii WEB-2 selected after sequential passages with increased concentrations of imipenem possessed higher MICs for carbapenems and cephalosporins including cefiderocol, higher levels of the blaVIM–1 gene transcripts, and detectable carbapenemase activity using the Carba NP test. Assessment of read coverage demonstrated that a duplication of the region surrounding blaVIM–1 gene occurred in the A. hermannii mutant with detectable carbapenemase activity. The lack of detection of the VIM-1 carbapenemase activity in A. hermannii WEB-2 isolate was likely due to a weak replication of the IncA plasmid harboring the blaVIM–1 gene. Imipenem as selective pressure led to a duplication of this gene on the plasmid and to the restoration of a significant carbapenem-hydrolyzing phenotype.https://www.frontiersin.org/articles/10.3389/fmicb.2021.741972/fullβ-lactamasecarbapenemasetranscriptionEnterobacterplasmid
spellingShingle Delphine Girlich
Rémy A. Bonnin
Rémy A. Bonnin
Alexis Proust
Thierry Naas
Thierry Naas
Thierry Naas
Laurent Dortet
Laurent Dortet
Laurent Dortet
Undetectable Production of the VIM-1 Carbapenemase in an Atlantibacter hermannii Clinical Isolate
Frontiers in Microbiology
β-lactamase
carbapenemase
transcription
Enterobacter
plasmid
title Undetectable Production of the VIM-1 Carbapenemase in an Atlantibacter hermannii Clinical Isolate
title_full Undetectable Production of the VIM-1 Carbapenemase in an Atlantibacter hermannii Clinical Isolate
title_fullStr Undetectable Production of the VIM-1 Carbapenemase in an Atlantibacter hermannii Clinical Isolate
title_full_unstemmed Undetectable Production of the VIM-1 Carbapenemase in an Atlantibacter hermannii Clinical Isolate
title_short Undetectable Production of the VIM-1 Carbapenemase in an Atlantibacter hermannii Clinical Isolate
title_sort undetectable production of the vim 1 carbapenemase in an atlantibacter hermannii clinical isolate
topic β-lactamase
carbapenemase
transcription
Enterobacter
plasmid
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.741972/full
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