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Characterization of bla CTX-M-27/F1:A2:B20 Plasmids Harbored by Escherichia coli Sequence Type 131 Sublineage C1/H30R Isolates Spreading among Elderly Japanese in Nonacute-Care Settings.

ABSTRACT: We characterized 29 bla CTX-M-27-harboring plasmids of Escherichia coli sequence type 131 (ST131) sublineage C1/H30R isolates from healthy individuals and long-term-care facility (LTCF) residents. Most (27/29) plasmids were of the FIA, FIB, and FII multireplicon type with the same plasmid multilocus sequence typing (pMLST). Several plasmids (7/23) from LTCF residents harbored only bla CTX-M-27 as the resistance gene; however, their fundamental structures were very similar to those of previously isolated bla CTX-M-27/F1:A2:B20 plasmids, suggesting their prevalence as a newly arising public health concern.

SUBMITTER: Matsuo N

PROVIDER: S-EPMC7179624 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Characterization of blaCTX-M-27/F1:A2:B20 Plasmids Harbored by Escherichia coli Sequence Type 131 Sublineage C1/H30R Isolates Spreading among Elderly Japanese in Nonacute-Care Settings.

Matsuo Nao N Nonogaki Rina R Hayashi Michiko M Wachino Jun-Ichi JI Suzuki Masahiro M Arakawa Yoshichika Y Kawamura Kumiko K

Antimicrobial agents and chemotherapy 20200421 5

We characterized 29 blaCTX-M-27-harboring plasmids of Escherichia coli sequence type 131 (ST131) sublineage C1/H30R isolates from healthy individuals and long-term-care facility (LTCF) residents. Most (27/29) plasmids were of the FIA, FIB, and FII multireplicon type with the same plasmid multilocus sequence typing (pMLST). Several plasmids (7/23) from LTCF residents harbored only blaCTX-M-27 as the resistance gene; however, their fundamental stru ...[more]

PMID: 32152084

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Project description:Escherichia coli sequence type 131 (ST131) has contributed to the spread of extended-spectrum beta-lactamase (ESBL) and has emerged as the dominant cause of hospital- and community-acquired urinary tract infections. Here, we report for the first time an in-depth analysis of whole-genome sequencing (WGS) of 4 ESBL-producing E. coli ST131 isolates recovered from patients in two hospitals in Armenia using Illumina short-read sequencing for accurate base calling to determine their genotype and to infer their phylogeny and using Oxford Nanopore Technologies long-read sequencing to resolve plasmid and chromosomal genetic elements. Genotypically, the four Armenian isolates were identified as part of the H30Rx/clade C2 (n = 2) and H41/clade A (n = 2) lineages and were phylogenetically closely related to isolates from the European Nucleotide Archive (ENA) database previously recovered from patients in the United States, Australia, and New Zealand. The Armenian isolates recovered in this study had chromosomal integration of the blaCTX-M-15 gene in the H30Rx isolates and a high number of virulence genes found in the H41 isolates associated with the carriage of a rare genomic island (in the context of E. coli ST131) containing the S fimbrial, salmochelin siderophore, and microcin H47 virulence genes. Furthermore, our data show the evolution of the IncF[2:A2:B20] plasmid harboring both blaCTX-M-15 and blaCTX-M-27 genes, derived from the recombination of genes from an IncF[F2:A-:B-] blaCTX-M-15-associated plasmid into the IncF[F1:A2:B20] blaCTX-M-27-associated plasmid backbone seen in two genetically closely related H41 Armenian isolates. IMPORTANCE Combining short and long reads from whole-genome sequencing analysis provided a genetic context for uncommon genes of clinical importance to better understand transmission and evolutionary features of ESBL-producing uropathogenic E. coli (UPEC) ST131 isolates recovered in Armenia. Using hybrid genome assembly in countries lacking genomic surveillance studies can inform us about new lineages not seen in other countries with genes encoding high virulence and antibiotic resistance harbored on mobile genetic elements.

Project description:ObjectiveEscherichia coli is a common Gram-negative human pathogen. The emergence of E. coli with multiple-antibiotic-resistant phenotypes has become a serious health concern. This study reports the whole-genome sequences of third-generation cephalosporin-resistant (3GC-R) and multidrug-resistant (MDR) E. coli EC6868 and explores the acquired antibiotic-resistance genes (ARGs) as well as their genetic contexts.MethodsE. coli EC6868 was isolated from a vaginal secretion sample of a pregnant patient in China. The antimicrobial susceptibility was assessed, and whole-genome sequencing was conducted. The acquired ARGs, insertion sequence (IS) elements, and integrons within the genome of E. coli EC6868 were identified, and the genetic contexts associated with the ARGs were analyzed systematically.ResultsE. coli EC6868 was determined to belong to ST69 and harbored a 144.9-kb IncF plasmid (pEC6868-1) with three replicons (Col156, IncFIBAP001918, and IncFII). The ESBL gene blaCTX-M-27 was located on the structure "∆ISEcp1-blaCTX-M-27-IS903B", which was widely present in the species of Enterobacteriales. Other ARGs carried by plasmid pEC6868-1 were mainly located on the 18.9-kb IS26-composite transposon (five copies of intact IS26 and one copy of truncated IS26) composing of IS26-mphA-mrx(A)-mphR(A)-IS6100, ∆TnAs3-eamA-tet(A)-tetR(A)-aph(6)-Id-aph(3")-Ib-sul2-IS26, and a class 1 integron, which was widely present on IncF plasmids of E. coli, mainly distributed in ST131, ST38, and ST405. Notably, pEC6868 in our study was the first report on a plasmid harboring the 18.9-kb structure in E. coli ST69 in China.ConclusionThe 3GC-R E. coli ST69 strain with an MDR IncF plasmid carrying blaCTX-M-27 and other ARGs, conferring resistance to aminoglycosides, macrolides, sulfonamides, tetracycline, and trimethoprim, was identified in a hospital in China. Mobile genetic elements including ISEcp1, IS903B, IS26, Tn3, IS6100 and class 1 integron were found within the MDR region, which could play important roles in the global dissemination of these resistance genes.

Project description:Two diverse conjugative plasmids can interact within bacterial cells. However, to the best of our knowledge, the interaction between blaCTX-M-bearing IncFII plasmid and mcr-1-carrying IncI2 plasmid colocated on the same bacterial host has not been reported. This study was initiated to explore the interaction and to analyze the reasons that these two plasmids are often coresident in multidrug-resistant Escherichia coli. To assess the interactions on plasmid stabilities, fitness costs, and transfer rates, we constructed two groups of isogenic derivatives, C600FII, C600I2, and C600FII+I2 of E. coli C600 and J53FII, J53I2, and J53FII+I2 of E. coli J53, respectively. We found that carriage of FII and I2 plasmids, independently and together, had not impaired the growth of the bacterial host. It was difficult for the single plasmid FII or I2 in E. coli C600 to reach stable persistence for a long time in an antibiotic-free environment, while the stability would be striking improved when they coresided. Meanwhile, plasmids FII and I2, whether together or apart, could notably enhance the fitness advantage of the host; moreover, E. coli coharboring plasmids FII and I2 presented more obvious fitness advantage than that carrying single plasmid FII. Coresident plasmids FII and I2 could accelerate horizontal cotransfer by conjugation. The transfer rates from a strain carrying coresident FII and I2 plasmids increased significantly when it mated with a recipient cell carrying one of them. Our findings highlight the advantages of coinhabitant FII and I2 plasmids in E. coli to drive the persistence and spread of plasmid-carried blaCTX-M and mcr-1 genes, although the molecular mechanisms of their coresidence warrant further study. IMPORTANCE More and more Enterobacteriaceae carry both blaCTX-M and mcr-1, which are usually located on IncFII-type and IncI2-type plasmids in the same bacterial host, respectively. However, the study on advantages of coresident plasmids in bacterial host is still sparse. Here, we investigated the stability, fitness cost, and cotransfer traits associated with coresident IncFII-type and IncI2-type plasmids in E. coli. Our results show that coinhabitant plasmids in E. coli are more stable, confer more fitness advantages, and are easier to transfer and cotransfer than a single plasmid IncFII or IncI2. Our findings confirm the advantages of coresident plasmids of blaCTX-M-bearing IncFII and mcr-1-bearing IncI2 in clinical E. coli, which will pose a serious threat to clinical therapy and public health.

Dataset Information

Characterization of bla CTX-M-27/F1:A2:B20 Plasmids Harbored by Escherichia coli Sequence Type 131 Sublineage C1/H30R Isolates Spreading among Elderly Japanese in Nonacute-Care Settings.

Publications

Characterization of <i>bla</i><sub>CTX-M-27</sub>/F1:A2:B20 Plasmids Harbored by Escherichia coli Sequence Type 131 Sublineage C1/<i>H</i>30R Isolates Spreading among Elderly Japanese in Nonacute-Care Settings.

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