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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Frontiers Media S.A.
2021-12-01
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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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language | English |
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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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