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Characterization of a novel bla NDM-5-harboring IncFII plasmid and an mcr-1-bearing IncI2 plasmid in a single Escherichia coli ST167 clinical isolate.

ABSTRACT: Background and purpose:The spread of the plasmid-mediated, colistin-resistance gene mcr-1 into New Delhi metallo-?-lactamase (NDM)-producing bacterial isolates can cause untreatable infections. In this study, we conducted a molecular characterization of a novel, conjugative, bla NDM-5-positive IncFII plasmid (pNDM-EC16-50) together with an mcr-1-bearing IncI2 plasmid in a single Escherichia coli ST167 clinical isolate EC16-50. Methods and results:EC16-50, which belongs to the E. coli strain ST167 and phylogroup A, was identified to co-produce NDM-5 and MCR-1. S1-PFGE and Southern blotting showed that bla NDM-5 and mcr-1 genes were located oñ95 kb and ~65 kb plasmids, respectively. A conjugation assay revealed that both bla NDM-5- and mcr-1-bearing plasmids were self-transmissible. Comparative plasmid analysis suggested that bla NDM-5-harboring F2:A-:B-plasmid might have evolved from the well-reported NDM-carrying pMC-NDM-like plasmid via recombination with a locally emerged pSJ_94 plasmid, whereas the mcr-1-carrying IncI2 plasmid was similar to previously reported mcr-1-bearing plasmids in China. Conclusion and impact:This study represents the first report of the NDM-5 carrying Inc-FII- but not IncX3-type plasmid in an MCR-1-producing E. coli isolate. More striking was the dissemination of mcr-1 in a successful epidemic NDM-5-producing E. coli clone ST167, which could facilitate the spread of colistin resistance in carbapenemase-producing E. coli isolates.

SUBMITTER: Xu L

PROVIDER: S-EPMC6402710 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Characterization of a novel bla NDM-5-harboring IncFII plasmid and an mcr-1-bearing IncI2 plasmid in a single Escherichia coli ST167 clinical isolate.

Xu Lijuan L Wang Ping P Cheng Jing J Qin Shangshang S Xie Weihong W

Infection and drug resistance 20190301

<h4>Background and purpose</h4>The spread of the plasmid-mediated, colistin-resistance gene mcr-1 into New Delhi metallo-β-lactamase (NDM)-producing bacterial isolates can cause untreatable infections. In this study, we conducted a molecular characterization of a novel, conjugative, bla NDM-5-positive IncFII plasmid (pNDM-EC16-50) together with an mcr-1-bearing IncI2 plasmid in a single Escherichia coli ST167 clinical isolate EC16-50.<h4>Methods and results ...[more]

PMID: 30881056

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Project description:Providencia rettgeri has recently gained increased importance owing to the New Delhi metallo-β-lactamase (NDM) and other β-lactamases produced by its clinical isolates. These enzymes reduce the efficiency of antimicrobial therapy. Herein, we reported the findings of whole-genome sequence analysis and a comprehensive pan-genome analysis performed on a multidrug-resistant P. rettgeri 18004577 clinical strain recovered from the urine of a hospitalized patient in Shandong, China, in 2018. Providencia rettgeri 18004577 was found to have a genome assembly size of 4.6 Mb with a G + C content of 41%; a circular plasmid p18004577_NDM of 273.3 Kb, harboring an accessory multidrug-resistant region; and a circular, stable IncT plasmid p18004577_Rts of 146.2 Kb. Additionally, various resistance genes were identified in its genome, including bla NDM-1, bla OXA-10, bla PER-4, aph(3')-VI, ant(2'')-Ia, ant(3')-Ia, sul1, catB8, catA1, mph(E), and tet. Conjugation experiments and whole-genome sequencing revealed that the bla NDM-1 gene could be transferred to the transconjugant via the formation of pJ18004577_NDM, a novel hybrid plasmid. Based on the genetic comparison, the main possible formation process for pJ18004577_NDM was the insertion of the [ΔISKox2-IS26-ΔISKox2]-aph(3')-VI-bla NDM-1 translocatable unit module from p18004577_NDM into plasmid p18004577_Rts in the Russian doll insertion structure (ΔISKox2-IS26-ΔISKox2), which played a role similar to that of IS26 using the "copy-in" route in the mobilization of [aph(3')-VI]-bla NDM-1. The array, multiplicity, and diversity of the resistance and virulence genes in this strain necessitate stringent infection control, antibiotic stewardship, and periodic resistance surveillance/monitoring policies to preempt further horizontal and vertical spread of the resistance genes. Roary analysis based on 30 P. rettgeri strains pan genome identified 415 core, 756 soft core, 5,744 shell, and 12,967 cloud genes, highlighting the "close" nature of P. rettgeri pan-genome. After a comprehensive pan-genome analysis, representative biological information was revealed that included phylogenetic distances, presence or absence of genes across the P. rettgeri bacteria clade, and functional distribution of proteins. Moreover, pan-genome analysis has been shown to be an effective approach to better understand P. rettgeri bacteria because it helps develop various tailored therapeutic strategies based on their biological similarities and differences.

Project description:Our objective was to characterize the genetic features of plasmids harbored by two genetically related, MCR-1 and NDM-5-producing Escherichia coli strains recovered from a chicken meat sample. The genetic profiles of all plasmids harbored by the two test strains, namely, 1106 and 1107, were determined by whole-genome sequencing, S1-pulsed-field gel electrophoresis (PFGE), Southern hybridization, and bioinformatics analysis. The transferability of plasmids harbored by the two strains was assessed by filter mating assay. Strains 1106 and 1107 were resistant to almost all the antibiotics, including colistin and fosfomycin, but remained susceptible to amikacin and tigecycline. The plasmids of p1107-NDM-5 and p1106-NDM-5 both contain a class I integron which lacks the ISAba125 element. The backbone of p1106-IncFII exhibited a high degree of similarity with that of p1106-NDM-5 and p1107-NDM-5, implying that events of plasmid fusion and resolution were involved in the formation of the two plasmids. The plasmids p1106-IncHI2MCR and p1107-IncHI2MCR belong to an IncHI2 replicon type, with three copies of ISApl1 being observed in p1106-IncHI2MCR, implying that the mcr-1 gene was transferable among bacteria that reside in the same food matrix. In this study, p1106-IncFIB, p1107-99K, p1107-111K, and p1107-118K were all found to be phage-like plasmids, with p1106-IncFIB and p1107-118K containing several virulence genes, including iroBCDEN, iucABCD, sitABCD, hlyF, and iss. Surprisingly, resistance genes such as aph(3')-Ia, sul3, and aac(3')-IId could also be found in p1107-118K, but resistance genes were not detected in other phage-like plasmids. In conclusion, enhanced surveillance is required to monitor and control the dissemination of various resistance determinants among foodborne pathogens. IMPORTANCE Carbapenem and colistin are last-resort antibiotics used to treat serious clinical infections caused by multidrug-resistant (MDR) bacterial pathogens. Plasmids encoding resistance to carbapenems and colistin have been reported in clinical pathogens in recent years, and yet few studies reported cocarriage of mcr and blaNDM genes in Escherichia coli strains of food origin. How plasmids encoding these two important resistance determinants are being evolved and transmitted in bacterial pathogens is not well understood. In this study, we investigated the genetic features of plasmids harbored by two nonclonal, mcr-1- and blaNDM-5-bearing E. coli strains (1106 and 1107) recovered from a fresh chicken meat sample to understand and provide evidence of the level and dynamics of MDR plasmid transmission. Our data confirmed that active plasmid fusion and resolution events were involved in the formation of plasmids that harbor multiple resistance genes, which provide insights into the further control of plasmid evolution in bacterial pathogens.

Project description:The global spread of colistin or carbapenem-resistant Enterobacteriaceae (CRE) has been a pressing threat to public health. Members of Enterobacteriaceae, especially Proteus mirabilis and Escherichia coli, have been prevalent foodborne pathogens and such pathogens from fresh vegetables have triggered foodborne illness in China. However, reports about CRE, especially P. mirabilis from fresh vegetables, are still lacking. In this study, we identified five blaNDM-positive P. mirabilis and five blaNDM-positive generic E. coli concurrently from five fresh vegetables in two markets from China, and four of the five E. coli also carried mcr-1. The 10 isolates were characterized with methods including antimicrobial susceptibility testing, conjugation, whole-genome sequencing and phylogenetic analysis. All 10 isolates were multidrug-resistant (MDR). blaNDM-5 in five E. coli isolates and one P. mirabilis carrying blaNDM-5 was located on similarly transferable IncX3 plasmids, while transferably untypable plasmids were the carriers of blaNDM-1 in four P. mirabilis isolates from different types of vegetables/markets. mcr-1 in the four blaNDM-5-positive E. coli was located on similarly non-conjugative IncHI2 MDR plasmids lacking transfer region. Notably, ISCR1 complex class 1 integron capable of capturing blaNDM-1 was found on all untypable plasmids from P. mirabilis, and five copies of ISCR1 complex class 1 integron containing blaNDM-1 even occurred in one P. mirabilis, which showed high-level carbapenem resistance. Plasmid and phylogenetic analysis revealed that the blaNDM-positive P. mirabilis and E. coli from fresh vegetables might be derived from animals and transmitted to humans via the food chain. The concurrence of blaNDM-positive P. mirabilis and E. coli carrying both mcr-1 and blaNDM in different types of fresh vegetables eaten raw is alarming and threatens food safety. Sustained surveillance of these foodborne pathogens among fresh vegetables is urgent to ensure the health of food consumers. We report for the first time the concurrence of blaNDM-positive P. mirabilis and mcr-1-bearing E. coli carrying blaNDM from the same fresh vegetables.

Dataset Information

Characterization of a novel bla NDM-5-harboring IncFII plasmid and an mcr-1-bearing IncI2 plasmid in a single Escherichia coli ST167 clinical isolate.

Publications

Characterization of a novel <i>bla</i> <sub>NDM-5</sub>-harboring IncFII plasmid and an <i>mcr-1</i>-bearing IncI2 plasmid in a single <i>Escherichia coli</i> ST167 clinical isolate.

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