Emergence of Extensively Drug-Resistant ST170 Citrobacter portucalensis with Plasmids pK218-KPC, pK218-NDM, and pK218-SHV from a Tertiary Hospital, China

ABSTRACT The objective of this study is to characterize the molecular mechanism of a clinical carbapenem-resistant Citrobacter portucalensis strain K218, which coproduces KPC and NDM carbapenemases. K218 was isolated from a patient's blood sample in a Chinese tertiary hospital. Carbapenemases w...

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Main Authors: Xinhua Luo, Lianhua Yu, Jiao Feng, Jin Zhang, Cheng Zheng, Dakang Hu, Piaopiao Dai, Mengqiao Xu, Piaopiao Li, Ronghai Lin, Kai Mu
Format: Article
Language:English
Published: American Society for Microbiology 2022-10-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.02510-22
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author Xinhua Luo
Lianhua Yu
Jiao Feng
Jin Zhang
Cheng Zheng
Dakang Hu
Piaopiao Dai
Mengqiao Xu
Piaopiao Li
Ronghai Lin
Kai Mu
author_facet Xinhua Luo
Lianhua Yu
Jiao Feng
Jin Zhang
Cheng Zheng
Dakang Hu
Piaopiao Dai
Mengqiao Xu
Piaopiao Li
Ronghai Lin
Kai Mu
author_sort Xinhua Luo
collection DOAJ
description ABSTRACT The objective of this study is to characterize the molecular mechanism of a clinical carbapenem-resistant Citrobacter portucalensis strain K218, which coproduces KPC and NDM carbapenemases. K218 was isolated from a patient's blood sample in a Chinese tertiary hospital. Carbapenemases were detected by the immunocolloidal gold technique. The MIC values were determined by VITEK2. Whole-genome sequencing was performed on K218 and sequence data were analyzed using phylogenetics and extensive genomic comparison. This study reveals that K218 contains a single 5.08 Mb chromosome (51.8% GC content) and four plasmids, pK218-KPC (106 Kb), pK218-NDM (111 Kb), pK218-SHV (191 Kb), and pK218-NR (5 Kb). Twenty-nine types of antibiotic resistance genes were carried on K218, including blaKPC-2 harbored on pK218-KPC and blaNDM-1 harbored on pK218-NDM. Detailed comparison of related plasmids of pK218-KPC, pK218-NDM, and pK218-SHV showed that they shared similar conserved backbone regions, respectively. Comprehensive annotation revealed large accessory modules were recombined on the genome of K218. Further analysis speculated that mobile genetic elements bearing abundant resistance genes facilitated the formation of these accessory modules. In conclusion, this study provides an in-depth understanding of the genomic characterization of K218, an extensively drug-resistant C. portucalensis strain coproducing NDM and KPC carbapenemase. To the best of our knowledge, this is the first report of C. portucalensis strain coharboring blaKPC-2 and blaNDM-1 from the clinical setting. IMPORTANCE This is the first report of extensively drug-resistant C. portucalensis harboring both blaKPC-2 and blaNDM-1. This study will not only extend the understanding of the structural dissection of plasmids and chromosomes carried in C. portucalensis, but also expand knowledge of the genetic environment of the blaKPC-2 and blaNDM-1 genes. blaKPC-2 and blaNDM-1 genes have been suggested to facilitate the propagation and persistence of their host bacteria under different antimicrobial selection pressures. Large accessory regions carrying blaKPC-2 and blaNDM-1 genes have become hot spots for transposition and integration, and their structural variation and evolution should receive attention. The multidrug-resistant plasmids pK218-KPC, pK218-NDM, and pK218-SHV with several multidrug resistance regions and the chromosome cK218 with two novel transposons Tn7410 and Tn7411 contribute to the formation of extensively drug-resistant C. portucalensis.
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spelling doaj.art-ad564667a7fb4215ba40a48412955f2c2022-12-22T03:22:08ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-10-0110510.1128/spectrum.02510-22Emergence of Extensively Drug-Resistant ST170 Citrobacter portucalensis with Plasmids pK218-KPC, pK218-NDM, and pK218-SHV from a Tertiary Hospital, ChinaXinhua Luo0Lianhua Yu1Jiao Feng2Jin Zhang3Cheng Zheng4Dakang Hu5Piaopiao Dai6Mengqiao Xu7Piaopiao Li8Ronghai Lin9Kai Mu10Department of Clinical Laboratory Medicine, Taizhou Municipal Hospital, Taizhou, ChinaDepartment of Clinical Laboratory Medicine, Taizhou Municipal Hospital, Taizhou, ChinaInstitutes of Biomedical Sciences, Shanxi University, Taiyuan, ChinaDepartment of Clinical Laboratory Medicine, Taizhou Municipal Hospital, Taizhou, ChinaDepartment of Critical Care Medicine, Taizhou Municipal Hospital, Taizhou, ChinaDepartment of Clinical Laboratory Medicine, Taizhou Municipal Hospital, Taizhou, ChinaDepartment of Clinical Laboratory Medicine, Taizhou Municipal Hospital, Taizhou, ChinaDepartment of Clinical Laboratory Medicine, Taizhou Municipal Hospital, Taizhou, ChinaDepartment of Clinical Laboratory Medicine, Taizhou Municipal Hospital, Taizhou, ChinaDepartment of Critical Care Medicine, Taizhou Municipal Hospital, Taizhou, ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaABSTRACT The objective of this study is to characterize the molecular mechanism of a clinical carbapenem-resistant Citrobacter portucalensis strain K218, which coproduces KPC and NDM carbapenemases. K218 was isolated from a patient's blood sample in a Chinese tertiary hospital. Carbapenemases were detected by the immunocolloidal gold technique. The MIC values were determined by VITEK2. Whole-genome sequencing was performed on K218 and sequence data were analyzed using phylogenetics and extensive genomic comparison. This study reveals that K218 contains a single 5.08 Mb chromosome (51.8% GC content) and four plasmids, pK218-KPC (106 Kb), pK218-NDM (111 Kb), pK218-SHV (191 Kb), and pK218-NR (5 Kb). Twenty-nine types of antibiotic resistance genes were carried on K218, including blaKPC-2 harbored on pK218-KPC and blaNDM-1 harbored on pK218-NDM. Detailed comparison of related plasmids of pK218-KPC, pK218-NDM, and pK218-SHV showed that they shared similar conserved backbone regions, respectively. Comprehensive annotation revealed large accessory modules were recombined on the genome of K218. Further analysis speculated that mobile genetic elements bearing abundant resistance genes facilitated the formation of these accessory modules. In conclusion, this study provides an in-depth understanding of the genomic characterization of K218, an extensively drug-resistant C. portucalensis strain coproducing NDM and KPC carbapenemase. To the best of our knowledge, this is the first report of C. portucalensis strain coharboring blaKPC-2 and blaNDM-1 from the clinical setting. IMPORTANCE This is the first report of extensively drug-resistant C. portucalensis harboring both blaKPC-2 and blaNDM-1. This study will not only extend the understanding of the structural dissection of plasmids and chromosomes carried in C. portucalensis, but also expand knowledge of the genetic environment of the blaKPC-2 and blaNDM-1 genes. blaKPC-2 and blaNDM-1 genes have been suggested to facilitate the propagation and persistence of their host bacteria under different antimicrobial selection pressures. Large accessory regions carrying blaKPC-2 and blaNDM-1 genes have become hot spots for transposition and integration, and their structural variation and evolution should receive attention. The multidrug-resistant plasmids pK218-KPC, pK218-NDM, and pK218-SHV with several multidrug resistance regions and the chromosome cK218 with two novel transposons Tn7410 and Tn7411 contribute to the formation of extensively drug-resistant C. portucalensis.https://journals.asm.org/doi/10.1128/spectrum.02510-22Citrobacter portucalensisblaNDM-1blaKPC-2mobile genetic elementsmultidrug resistance
spellingShingle Xinhua Luo
Lianhua Yu
Jiao Feng
Jin Zhang
Cheng Zheng
Dakang Hu
Piaopiao Dai
Mengqiao Xu
Piaopiao Li
Ronghai Lin
Kai Mu
Emergence of Extensively Drug-Resistant ST170 Citrobacter portucalensis with Plasmids pK218-KPC, pK218-NDM, and pK218-SHV from a Tertiary Hospital, China
Microbiology Spectrum
Citrobacter portucalensis
blaNDM-1
blaKPC-2
mobile genetic elements
multidrug resistance
title Emergence of Extensively Drug-Resistant ST170 Citrobacter portucalensis with Plasmids pK218-KPC, pK218-NDM, and pK218-SHV from a Tertiary Hospital, China
title_full Emergence of Extensively Drug-Resistant ST170 Citrobacter portucalensis with Plasmids pK218-KPC, pK218-NDM, and pK218-SHV from a Tertiary Hospital, China
title_fullStr Emergence of Extensively Drug-Resistant ST170 Citrobacter portucalensis with Plasmids pK218-KPC, pK218-NDM, and pK218-SHV from a Tertiary Hospital, China
title_full_unstemmed Emergence of Extensively Drug-Resistant ST170 Citrobacter portucalensis with Plasmids pK218-KPC, pK218-NDM, and pK218-SHV from a Tertiary Hospital, China
title_short Emergence of Extensively Drug-Resistant ST170 Citrobacter portucalensis with Plasmids pK218-KPC, pK218-NDM, and pK218-SHV from a Tertiary Hospital, China
title_sort emergence of extensively drug resistant st170 citrobacter portucalensis with plasmids pk218 kpc pk218 ndm and pk218 shv from a tertiary hospital china
topic Citrobacter portucalensis
blaNDM-1
blaKPC-2
mobile genetic elements
multidrug resistance
url https://journals.asm.org/doi/10.1128/spectrum.02510-22
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