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An XDR Pseudomonas aeruginosa ST463 Strain with an IncP-2 Plasmid Containing a Novel Transposon Tn6485f Encoding bla_IMP-45 and bla_AFM-1 and a Second Plasmid with Two Copies of bla_KPC-2.

ABSTRACT: The increased carbapenem resistance among Pseudomonas aeruginosa has become a serious health issue worldwide. We reported an extensively drug-resistant (XDR) P. aeruginosa PA30 isolate which belonged to sequence type ST463 and contained an IncP-2 plasmid (pPA30_1) carrying two genes, namely, bla_IMP-45 and bla_AFM-1, which encoded the metallo-β-lactamases AFM-1 and IMP-45, respectively. Additionally, the strain had a plasmid (pPA30_2) with two copies of the bla_KPC-2 genes embedded. The plasmid pPA30_1 was highly similar to the previously reported plasmid pHS17-127, which has the same genetic architecture. This plasmid contained bla_IMP-45, located in a second gene cassette of the integron In786, carried by a Tn1403-derivative transposon acquiring an ISCR27n3-bla_AFM-1 structure. Interestingly, the transposon in pPA30_1 acquired an extra ISCR1-qnrVC6 module and formed a novel transposon, which was subsequently annotated as Tn6485f. The bla_KPC-2 genes in pPA30_2 underwent duplication due to the inversion of the IS26-bla_KPC-2-IS26 element, which resulted in two copies of bla_KPC-2. IMPORTANCE The ST463 clone is an emerging high-risk sequence type that is spreading with bla_KPC-2-containing plasmids. The core bla_KPC-2 genetic platform is ISKpn27-bla_KPC-2-ISKpn6 in almost all samples, and the adjacent region beyond the core platform varies by IS26-mediated inversion or duplication events, amplifying the bla_KPC-2 gene copies. The ST463 P. aeruginosa strain PA30 in our study contains another two metallo-β-lactamase genes, namely, bla_IMP-45 and bla_AFM-1, in a novel transposon Tn6485f that is harbored by the IncP-2 megaplasmid. The pPA30_1 carrying bla_IMP-45 and bla_AFM-1 is highly related to pHS17-127 from the ST369 P. aeruginosa strain, indicating the putative dissemination of the megaplasmid between different clones.

SUBMITTER: Fang Y

PROVIDER: S-EPMC9927494 | biostudies-literature | 2023 Feb

REPOSITORIES: biostudies-literature

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An XDR Pseudomonas aeruginosa ST463 Strain with an IncP-2 Plasmid Containing a Novel Transposon Tn6485f Encoding blaIMP-45 and blaAFM-1 and a Second Plasmid with Two Copies of blaKPC-2.

Fang Yinfei Y Wang Nanfei N Wu Zhaoxia Z Zhu Yijun Y Ma Yongjun Y Li Yue Y Cai Heng H Zhang Piaopiao P Leptihn Sebastian S Yu Yunsong Y Hua Xiaoting X Tu Yuexing Y

Microbiology spectrum 20230118 1

The increased carbapenem resistance among Pseudomonas aeruginosa has become a serious health issue worldwide. We reported an extensively drug-resistant (XDR) P. aeruginosa PA30 isolate which belonged to sequence type ST463 and contained an IncP-2 plasmid (pPA30_1) carrying two genes, namely, blaIMP-45 and blaAFM-1, which encoded the metallo-β-lactamases AFM-1 and IMP-45, respectively. Additionally, the strain had a plasmid (pPA30_2) with two copies of the b ...[more]

PMID: 36651737

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Project description:Carbapenemase is the predominant enzyme in the mechanism leading to Enterobacterales resistance to carbapenems, but only a limited number of isolates harbor double classes/types of carbapenemase. Here, an IMP-4 and NDM-1 producer named Klebsiella michiganensis 7525 is reported, and the co-harboring plasmid is further characterized. K. michiganensis 7525 was positive for the blaIMP-4 and blaNDM-1 genes by the NG-Test Carba-5 method and PCR followed by sequencing, and both were located on the same plasmid (designated pKOX7525_1) according to S1-PFGE with Southern blot experiments. pKOX7525_1 was capable of transconjugation with an efficiency of 4.3 × 10-8 in a filter mating experiment. Whole-genome sequencing and bioinformatics analysis confirmed that the plasmid was novel, clustered to the incompatibility type of IncHIB/IncFIA/IncR and presented high similarity to a blaIMP-4-carrying IncHIB plasmid (pA) published with 79% coverage and 100% sequence identify. In contrast, a large-fragment insertion and inversion mediated by IS26 was observed on the plasmid, which introduced a genetic hybrid zone with multiple resistance genes, including blaNDM-1, to the plasmid. In the transconjugants, the presence of pKOX7525_1 had a negative impact on bacterial fitness. In vitro evolution experiments showed that pKOX7525_1 in the transconjugant could not be stably inherited after 10 days of passage and that blaNDM-1 could be lost during repeated laboratory passage. Our study not only reports a novel plasmid co-harboring blaIMP-4 and blaNDM-1 but also highlights the putative pathway of plasmid formation and evolution by means of genetic rearrangement through sequence insertion and homologue recombination, which may have critical value for plasmid research and increase awareness of carbapenem-resistant Enterobacteriaceae (CRE). IMPORTANCE In this study, we characterized a novel plasmid from a carbapenem-resistant K. michiganensis (CRKM) isolate, which harbors two metallo-β-lactamases (MBLs), IMP-4 and NDM-1, is capable of transconjugation and contains three replicons. Our results first expand the diversity of plasmids co-harboring carbapenemase genes in Enterobacterales, which exhibits epidemic importance in bacterial resistance. Additionally, we investigated the origin and formation of this MBL double-positive plasmid based on comparative genomics analysis, which indicated that IS26 plays a vital role through continuous genetic rearrangements. Moreover, this plasmid is unstable in transconjugants during passage at the multidrug-resistant (MDR) region of blaNDM-1, with fluctuating stability under varying antibiotic selection, highlighting auspicious considerations regarding recognition of the complexity and plasticity of plasmids in evolution and re-emphasizing clinical infection control inspired by CRE.

Dataset Information

An XDR Pseudomonas aeruginosa ST463 Strain with an IncP-2 Plasmid Containing a Novel Transposon Tn6485f Encoding bla_IMP-45 and bla_AFM-1 and a Second Plasmid with Two Copies of bla_KPC-2.

Publications

An XDR Pseudomonas aeruginosa ST463 Strain with an IncP-2 Plasmid Containing a Novel Transposon Tn<i>6485f</i> Encoding <i>bla</i><sub>IMP-45</sub> and <i>bla</i><sub>AFM-1</sub> and a Second Plasmid with Two Copies of <i>bla</i><sub>KPC-2</sub>.

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