{"title":"In-host intra- and inter-species transfer of bla<sub>KPC-2</sub> and bla<sub>NDM-1</sub> in Serratia marcescens and its local and global epidemiology.","authors":"Feilong Zhang, Zhihua Li, Xinmeng Liu, Ziyao Li, Zichen Lei, Jiankang Zhao, Yulin Zhang, Yongli Wu, Xinrui Yang, Binghuai Lu","doi":"10.1016/j.ijantimicag.2024.107327","DOIUrl":null,"url":null,"abstract":"<p><strong>Objectives: </strong>This study aimed to investigate interspecies transfer of resistance gene bla<sub>NDM-1</sub> and intraspecies transfer of bla<sub>KPC-2</sub> in Serratia marcescens, and explore the epidemical and evolutionary characteristics of carbapenemase-producing S. marcescens (CPSM) regionally and globally.</p><p><strong>Methods: </strong>Interspecies and intraspecies transfer of bla<sub>KPC-2</sub>- or bla<sub>NDM-1</sub> were identified by antimicrobial susceptibility testing, plasmid conjugation and curing, discovery of transposable units (TUs), outer membrane vesicles (OMVs), qPCR, whole-genome sequencing and bioinformatic analysis. The genomic evolution of CPSM strains was explored by cgSNP and maximum-likelihood phylogenetic tree.</p><p><strong>Results: </strong>CPSM S50079 strain, co-carrying bla<sub>KPC-2</sub> and bla<sub>NDM-1</sub> on one plasmid, was isolated from the blood of a patient with acute pancreatitis and could generate TUs carrying either bla<sub>KPC-2</sub> or bla<sub>NDM-1</sub>. We identified the interspecies transfer of bla<sub>NDM-1</sub>-carrying plasmid from Providencia rettgeri P50213, producing the identical bla<sub>NDM-1</sub>-carrying TUs, to S. marcescens S50079K, an S50079 variant via plasmid curing, through bla<sub>NDM-1</sub>-harboring plasmid conjugation and OMVs transfer. Furthermore, the intraspecies transfer of bla<sub>KPC-2</sub>, mediated by IS26 from plasmid to chromosome in S50079, was identified. Likely, in another lung transplant patient, interspecies transfer of bla<sub>NDM-1</sub> carried by IncX3 plasmid was also identified among S. marcescens and Citrobacter freundii as well as Enterobacter hormaechei via plasmid transfer. Furthermore, 11 CPSM from 349 non-repetitive S. marcescens strains were identified in the same hospital and clonal dissemination, with carbapenemase evolution from bla<sub>KPC-2</sub> to both bla<sub>KPC-2</sub> and bla<sub>NDM-1</sub> was found in the 8 CPSM across four years. Finally, the analysis of 236 global CPSM from 835 non-repetitive S. marcescens genomes, retrieved from NCBI database, revealed long-term spread and evolution worldwide, and would cause the convergence of more carbapenemase genes.</p><p><strong>Conclusions: </strong>Interspecies transfer of resistance gene bla<sub>NDM-1</sub> and intraspecies transfer of resistance gene bla<sub>KPC-2</sub> in CPSM were identified. Nosocomial and global dissemination of CPSM were revealed and more urgent surveillance was acquired.</p>","PeriodicalId":13818,"journal":{"name":"International Journal of Antimicrobial Agents","volume":null,"pages":null},"PeriodicalIF":4.9000,"publicationDate":"2024-09-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"International Journal of Antimicrobial Agents","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1016/j.ijantimicag.2024.107327","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"INFECTIOUS DISEASES","Score":null,"Total":0}
引用次数: 0
Abstract
Objectives: This study aimed to investigate interspecies transfer of resistance gene blaNDM-1 and intraspecies transfer of blaKPC-2 in Serratia marcescens, and explore the epidemical and evolutionary characteristics of carbapenemase-producing S. marcescens (CPSM) regionally and globally.
Methods: Interspecies and intraspecies transfer of blaKPC-2- or blaNDM-1 were identified by antimicrobial susceptibility testing, plasmid conjugation and curing, discovery of transposable units (TUs), outer membrane vesicles (OMVs), qPCR, whole-genome sequencing and bioinformatic analysis. The genomic evolution of CPSM strains was explored by cgSNP and maximum-likelihood phylogenetic tree.
Results: CPSM S50079 strain, co-carrying blaKPC-2 and blaNDM-1 on one plasmid, was isolated from the blood of a patient with acute pancreatitis and could generate TUs carrying either blaKPC-2 or blaNDM-1. We identified the interspecies transfer of blaNDM-1-carrying plasmid from Providencia rettgeri P50213, producing the identical blaNDM-1-carrying TUs, to S. marcescens S50079K, an S50079 variant via plasmid curing, through blaNDM-1-harboring plasmid conjugation and OMVs transfer. Furthermore, the intraspecies transfer of blaKPC-2, mediated by IS26 from plasmid to chromosome in S50079, was identified. Likely, in another lung transplant patient, interspecies transfer of blaNDM-1 carried by IncX3 plasmid was also identified among S. marcescens and Citrobacter freundii as well as Enterobacter hormaechei via plasmid transfer. Furthermore, 11 CPSM from 349 non-repetitive S. marcescens strains were identified in the same hospital and clonal dissemination, with carbapenemase evolution from blaKPC-2 to both blaKPC-2 and blaNDM-1 was found in the 8 CPSM across four years. Finally, the analysis of 236 global CPSM from 835 non-repetitive S. marcescens genomes, retrieved from NCBI database, revealed long-term spread and evolution worldwide, and would cause the convergence of more carbapenemase genes.
Conclusions: Interspecies transfer of resistance gene blaNDM-1 and intraspecies transfer of resistance gene blaKPC-2 in CPSM were identified. Nosocomial and global dissemination of CPSM were revealed and more urgent surveillance was acquired.
期刊介绍:
The International Journal of Antimicrobial Agents is a peer-reviewed publication offering comprehensive and current reference information on the physical, pharmacological, in vitro, and clinical properties of individual antimicrobial agents, covering antiviral, antiparasitic, antibacterial, and antifungal agents. The journal not only communicates new trends and developments through authoritative review articles but also addresses the critical issue of antimicrobial resistance, both in hospital and community settings. Published content includes solicited reviews by leading experts and high-quality original research papers in the specified fields.