Transcriptional Landscape of a blaKPC-2 Plasmid and Response to Imipenem Exposure in Escherichia coli TOP10
The diffusion of KPC-2 carbapenemase is closely related to the spread of Klebsiella pneumoniae of the clonal-group 258 and linked to IncFIIK plasmids. Little is known about the biology of multi-drug resistant plasmids and the reasons of their successful dissemination. Using E. coli TOP10 strain harb...
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Frontiers Media S.A.
2018-12-01
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Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2018.02929/full |
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language |
English |
format |
Article |
sources |
DOAJ |
author |
Agnès B. Jousset Agnès B. Jousset Agnès B. Jousset Agnès B. Jousset Isabelle Rosinski-Chupin Isabelle Rosinski-Chupin Julie Takissian Julie Takissian Philippe Glaser Philippe Glaser Rémy A. Bonnin Rémy A. Bonnin Rémy A. Bonnin Thierry Naas Thierry Naas Thierry Naas Thierry Naas |
spellingShingle |
Agnès B. Jousset Agnès B. Jousset Agnès B. Jousset Agnès B. Jousset Isabelle Rosinski-Chupin Isabelle Rosinski-Chupin Julie Takissian Julie Takissian Philippe Glaser Philippe Glaser Rémy A. Bonnin Rémy A. Bonnin Rémy A. Bonnin Thierry Naas Thierry Naas Thierry Naas Thierry Naas Transcriptional Landscape of a blaKPC-2 Plasmid and Response to Imipenem Exposure in Escherichia coli TOP10 Frontiers in Microbiology carbapenemase KPC-producing plasmids transcriptome RNA-seq oxidative-stress |
author_facet |
Agnès B. Jousset Agnès B. Jousset Agnès B. Jousset Agnès B. Jousset Isabelle Rosinski-Chupin Isabelle Rosinski-Chupin Julie Takissian Julie Takissian Philippe Glaser Philippe Glaser Rémy A. Bonnin Rémy A. Bonnin Rémy A. Bonnin Thierry Naas Thierry Naas Thierry Naas Thierry Naas |
author_sort |
Agnès B. Jousset |
title |
Transcriptional Landscape of a blaKPC-2 Plasmid and Response to Imipenem Exposure in Escherichia coli TOP10 |
title_short |
Transcriptional Landscape of a blaKPC-2 Plasmid and Response to Imipenem Exposure in Escherichia coli TOP10 |
title_full |
Transcriptional Landscape of a blaKPC-2 Plasmid and Response to Imipenem Exposure in Escherichia coli TOP10 |
title_fullStr |
Transcriptional Landscape of a blaKPC-2 Plasmid and Response to Imipenem Exposure in Escherichia coli TOP10 |
title_full_unstemmed |
Transcriptional Landscape of a blaKPC-2 Plasmid and Response to Imipenem Exposure in Escherichia coli TOP10 |
title_sort |
transcriptional landscape of a blakpc-2 plasmid and response to imipenem exposure in escherichia coli top10 |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Microbiology |
issn |
1664-302X |
publishDate |
2018-12-01 |
description |
The diffusion of KPC-2 carbapenemase is closely related to the spread of Klebsiella pneumoniae of the clonal-group 258 and linked to IncFIIK plasmids. Little is known about the biology of multi-drug resistant plasmids and the reasons of their successful dissemination. Using E. coli TOP10 strain harboring a multi-replicon IncFIIK-IncFIB blaKPC−2-gene carrying plasmid pBIC1a from K. pneumoniae ST-258 clinical isolate BIC-1, we aimed to identify basal gene expression and the effects of imipenem exposure using whole transcriptome approach by RNA sequencing (RNA-Seq). Independently of the antibiotic pressure, most of the plasmid-backbone genes were expressed at low levels. The most expressed pBIC1a genes were involved in antibiotic resistance (blaKPC−2, blaTEM and aph(3′)-I), in plasmid replication and conjugation, or associated to mobile elements. After antibiotic exposure, 34% of E. coli (pBIC1a) genome was differentially expressed. Induction of oxidative stress response was evidenced, with numerous upregulated genes of the SoxRS/OxyR oxydative stress regulons, the Fur regulon (for iron uptake machinery), and IscR regulon (for iron sulfur cluster synthesis). Nine genes carried by pBIC1a were up-regulated, including the murein DD-endopeptidase mepM and the copper resistance operon. Despite the presence of a carbapenemase, we observed a major impact on E. coli (pBIC1a) whole transcriptome after imipenem exposure, but no effect on the level of transcription of antimicrobial resistance genes. We describe adaptive responses of E. coli to imipenem-induced stress, and identified plasmid-encoded genes that could be involved in resistance to stressful environments. |
topic |
carbapenemase KPC-producing plasmids transcriptome RNA-seq oxidative-stress |
url |
https://www.frontiersin.org/article/10.3389/fmicb.2018.02929/full |
work_keys_str_mv |
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doaj-8a6e7319933b4072b65e4cba0519e6a42020-11-24T21:59:00ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-12-01910.3389/fmicb.2018.02929425853Transcriptional Landscape of a blaKPC-2 Plasmid and Response to Imipenem Exposure in Escherichia coli TOP10Agnès B. Jousset0Agnès B. Jousset1Agnès B. Jousset2Agnès B. Jousset3Isabelle Rosinski-Chupin4Isabelle Rosinski-Chupin5Julie Takissian6Julie Takissian7Philippe Glaser8Philippe Glaser9Rémy A. Bonnin10Rémy A. Bonnin11Rémy A. Bonnin12Thierry Naas13Thierry Naas14Thierry Naas15Thierry Naas16Department of Bacteriology-Parasitology-Hygiene, Bicêtre Hospital, Assistance Publique-Hôpitaux de Paris, Le Kremlin-Bicêtre, FranceAssociated French National Reference Center for Antibiotic Resistance, Le Kremlin-Bicêtre, FranceEA7361 “Structure, dynamic, function and expression of broad spectrum β-lactamases”, Faculty of Medicine, Paris-Sud University, Le Kremlin-Bicêtre, FranceJoint Research Unit Evolution and Ecology of Resistance to Antibiotics, Institut Pasteur-APHP-University Paris Sud, Paris, FranceJoint Research Unit Evolution and Ecology of Resistance to Antibiotics, Institut Pasteur-APHP-University Paris Sud, Paris, FranceCNRS, UMRS 3525, Paris, FranceEA7361 “Structure, dynamic, function and expression of broad spectrum β-lactamases”, Faculty of Medicine, Paris-Sud University, Le Kremlin-Bicêtre, FranceJoint Research Unit Evolution and Ecology of Resistance to Antibiotics, Institut Pasteur-APHP-University Paris Sud, Paris, FranceJoint Research Unit Evolution and Ecology of Resistance to Antibiotics, Institut Pasteur-APHP-University Paris Sud, Paris, FranceCNRS, UMRS 3525, Paris, FranceAssociated French National Reference Center for Antibiotic Resistance, Le Kremlin-Bicêtre, FranceEA7361 “Structure, dynamic, function and expression of broad spectrum β-lactamases”, Faculty of Medicine, Paris-Sud University, Le Kremlin-Bicêtre, FranceJoint Research Unit Evolution and Ecology of Resistance to Antibiotics, Institut Pasteur-APHP-University Paris Sud, Paris, FranceDepartment of Bacteriology-Parasitology-Hygiene, Bicêtre Hospital, Assistance Publique-Hôpitaux de Paris, Le Kremlin-Bicêtre, FranceAssociated French National Reference Center for Antibiotic Resistance, Le Kremlin-Bicêtre, FranceEA7361 “Structure, dynamic, function and expression of broad spectrum β-lactamases”, Faculty of Medicine, Paris-Sud University, Le Kremlin-Bicêtre, FranceJoint Research Unit Evolution and Ecology of Resistance to Antibiotics, Institut Pasteur-APHP-University Paris Sud, Paris, FranceThe diffusion of KPC-2 carbapenemase is closely related to the spread of Klebsiella pneumoniae of the clonal-group 258 and linked to IncFIIK plasmids. Little is known about the biology of multi-drug resistant plasmids and the reasons of their successful dissemination. Using E. coli TOP10 strain harboring a multi-replicon IncFIIK-IncFIB blaKPC−2-gene carrying plasmid pBIC1a from K. pneumoniae ST-258 clinical isolate BIC-1, we aimed to identify basal gene expression and the effects of imipenem exposure using whole transcriptome approach by RNA sequencing (RNA-Seq). Independently of the antibiotic pressure, most of the plasmid-backbone genes were expressed at low levels. The most expressed pBIC1a genes were involved in antibiotic resistance (blaKPC−2, blaTEM and aph(3′)-I), in plasmid replication and conjugation, or associated to mobile elements. After antibiotic exposure, 34% of E. coli (pBIC1a) genome was differentially expressed. Induction of oxidative stress response was evidenced, with numerous upregulated genes of the SoxRS/OxyR oxydative stress regulons, the Fur regulon (for iron uptake machinery), and IscR regulon (for iron sulfur cluster synthesis). Nine genes carried by pBIC1a were up-regulated, including the murein DD-endopeptidase mepM and the copper resistance operon. Despite the presence of a carbapenemase, we observed a major impact on E. coli (pBIC1a) whole transcriptome after imipenem exposure, but no effect on the level of transcription of antimicrobial resistance genes. We describe adaptive responses of E. coli to imipenem-induced stress, and identified plasmid-encoded genes that could be involved in resistance to stressful environments.https://www.frontiersin.org/article/10.3389/fmicb.2018.02929/fullcarbapenemaseKPC-producing plasmidstranscriptomeRNA-seqoxidative-stress |