Dataset Information

Probable Three-Species In Vivo Transfer of bla_NDM-1 in a Single Patient in Greece: Occurrence of NDM-1-Producing Klebsiella pneumoniae, Proteus mirabilis, and Morganella morganii.

ABSTRACT: NDM carbapenemase-encoding genes disseminate commonly among Enterobacterales through transferable plasmids carrying additional resistance determinants. Apart from the intra-species dissemination, the inter-species exchange of plasmids seems to play an additional important role in the spread of bla_NDM. We here present the genetics related to the isolation of three species (Klebsiella pneumoniae, Proteus mirabilis, and Morganella morganii) harboring the bla_NDM-1 gene from a single patient in Greece. Bacterial identification and antimicrobial susceptibility testing were performed using the Vitek2. Whole genome sequencing and bioinformatic tools were used to identify resistance genes and plasmids. Bla_NDM-1 harboring plasmids were found in all three isolates. Moreover, the plasmid constructs of the respective incomplete or circular contigs showed that the bla_NDM-1 and its neighboring genes form a cluster that was found in all isolates. Our microbiological findings, together with the patient's history, suggest the in vivo transfer of the bla_NDM-1-containing cluster through three different species in a single patient.

SUBMITTER: Meletis G

PROVIDER: S-EPMC10376024 | biostudies-literature | 2023 Jul

REPOSITORIES: biostudies-literature

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Probable Three-Species In Vivo Transfer of blaNDM-1 in a Single Patient in Greece: Occurrence of NDM-1-Producing Klebsiella pneumoniae, Proteus mirabilis, and Morganella morganii.

Meletis Georgios G Malousi Andigoni A Tychala Areti A Kassomenaki Angeliki A Vlachodimou Nikoletta N Mantzana Paraskevi P Metallidis Simeon S Skoura Lemonia L Protonotariou Efthymia E

Antibiotics (Basel, Switzerland) 20230720 7

NDM carbapenemase-encoding genes disseminate commonly among Enterobacterales through transferable plasmids carrying additional resistance determinants. Apart from the intra-species dissemination, the inter-species exchange of plasmids seems to play an additional important role in the spread of blaNDM. We here present the genetics related to the isolation of three species (Klebsiella pneumoniae, Proteus mirabilis, and Morganella morganii) harboring the bl ...[more]

PMID: 37508302

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Project description:The rapid spread of the blaNDM-1 gene is a major public health concern. Here, we describe the multidrug-resistant Proteus mirabilis strain XH1653, which contains a novel SXT/R391 integrative and conjugative element (ICE), harboring two tandem copies of blaNDM-1 and 21 other resistance genes. XH1653 was resistant to all antibiotics tested, apart from aztreonam. Whole-genome data revealed that two copies of blaNDM-1 embedded in the ISCR1 element are located in HS4 of the novel ICE, which we named ICEPmiChnXH1653. A circular intermediate of ICEPmiChnXH1653 was detected by PCR, and conjugation experiments showed that the ICE can be transferred to the Escherichia coli strain EC600 with frequencies of 1.5 × 10-7. In the recipient strain, the ICE exhibited a higher excision frequency and extrachromosomal copy number than the ICE in the donor strain. We also observed that the presence of ICEPmiChnXH1653 has a negative impact on bacterial fitness and leads to changes in the transcriptome of the host. In vitro evolution experiments under nonselective conditions showed that the two tandem copies of the ISCR1 element and the ISVsa3 element can be lost during repeated laboratory passage. This is the first report of a novel SXT/R391 ICE carrying two tandem copies of blaNDM-1, which also illustrates the role that ICEs may play as platforms for the accumulation and transmission of antibiotic resistance genes. IMPORTANCE The occurrence of carbapenemase-producing Proteus mirabilis, especially those strains producing NDM-1 and its variants, is a major public health concern worldwide. The integrative conjugative element (ICE) plays an important role in horizontal acquisition of resistance genes. In this study, we characterized a novel SXT/R391 ICE from a clinical P. mirabilis isolate that we named ICEPmiChnXH1653, which contains two tandem copies of the carbapenemase gene blaNDM-1. We performed an integrative approach to gain insights into different aspects of ICEPmiChnXH1653 evolution and biology and observed that ICEPmiChnXH1653 obtained the carbapenemase gene blaNDM-1 by ISCR1-mediated homologous recombination. Our study reveals that the transmission of blaNDM-1 by ISCR1 elements or ICEs may be an important contributor to the carbapenem resistance development across species, which could improve our understanding of horizontal gene transfer in clinical environments.

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.

Project description:BackgroundThe spread of carbapenemase-producing Enterobacteriaceae (CPE) is a great problem of healthcare worldwide. Study of the spread for bla OXA-48-like genes coding epidemically significant carbapenemases among hospital pathogens is important for the regional and global epidemiology of antimicrobial resistance.MethodsAntibacterial resistant isolates of Klebsiella pneumoniae (n = 95) from 54 patients, P. mirabilis (n = 32) from 20 patients, Enterobacter aerogenes (n = 6) from four patients, and Enterobacter cloacae (n = 4) from four patients were collected from January, 2013 to October, 2014 in neurosurgical intensive care unit (ICU) of the Burdenko Neurosurgery Institute, Moscow. Characteristics of the isolates were done using susceptibility tests, PCR detection of the resistance genes, genotyping, conjugation, DNA sequencing, and bioinformatic analysis.ResultsMajor strains under study were multi drug resistant (MDR), resistant to three or more functional classes of drugs simultaneously-98.9 % K. pneumoniae, 100 % P. mirabilis, one E. aerogenes isolate, and one E. cloacae isolate. Molecular-genetic mechanism of MDR in K. pneumoniae and P. mirabilis isolates were based on carrying of epidemic extended-spectrum beta-lactamase bla CTX-M-15 gene (87.2 and 90.6 % accordingly), carbapenemase bla OXA-48-like gene (55.3 and 23.3 % accordingly), and class 1 (54.8 and 31.3 % accordingly) and class 2 (90.6 % P. mirabilis) integrons. The bla OXA-48-like-positive K. pneumoniae were collected during whole two-year surveillance period, while P. mirabilis and Enterobacter spp. carrying bla OXA-48-like genes were detected only after four and 18 months after the research start, respectively. The bla OXA-48-like gene acquisition was shown for P. mirabilis isolates collected from five patients and for E. cloacae isolate collected from one patient during their stay in the ICU, presumably from bla OXA-48-like-positive K. pneumoniae. The source of the bla OXA-244 gene acquired by E. aerogenes isolates and the time of this event were not recognized.ConclusionsThe expanding of CPE in the surveyed ICU was associated with the spread of bla OXA-48 and bla OXA-244 carbapenemase genes documented not only among K. pneumoniae, well-known bacterial host for such genes, but among P. mirabilis, E. aerogenes, and E. cloacae.

Project description:ObjectiveRegional dissemination is the major cause of the widespread prevalence of a plasmid-encoding NDM-1 enzyme. We investigated the drug resistance, joint efficiency, and gene environment of a Klebsiella pneumoniae strain carrying bla NDM-1 gene.Materials and methodsCarbapenem-non-susceptible strains were analyzed using the VITEK 2 Compact. Strains carrying bla NDM-1 were identified using polymerase chain reaction and sequencing. Antimicrobial susceptibility testing and plasmid conjugation experiments were then conducted. Strains carrying bla NDM-1 were subjected to Southern blot analysis. After the gene mapping of bla NDM-1, library construction, and sequencing, plasmids were subsequently spliced and genotyped using the software Glimmer 3.0, and then analyzed using Mauve software.ResultsAmong 1735 carbapenem-non-susceptible strains, 54 strains of bla NDM-1-positive bacteria were identified, which consisted of 44 strains of K. pneumoniae, 8 strains of Acinetobacter baumannii and 2 strains of Escherichia coli. Strains carrying bla NDM-1 had a resistance rate of more than 50% in most antibiotics. Plasmid conjugation between strains carrying bla NDM-1 and E. coli strain J53 had a success rate of 50%. Southern blot analysis indicated that each strain had multiple plasmids containing bla NDM-1. Among the five plasmids containing bla NDM-1 in K. pneumoniae for sequencing, two plasmids with complete sequences were obtained. The findings were as follows: (i) The p11106 and p12 plasmids were highly similar to pNDM-BTR; (ii) the p11106 and p12 plasmids showed differences in the 20-30 kb region (orf00032-orf00043) from the other six plasmids; and (iii) bla NDM-1 was located at orf00037, while ble was found at orf00038. Two tnpA genes were located in the upstream region, and orf00052 (tnpA) in the 36 kb region was in the downstream sequence.Conclusionbla NDM-1-containing bacteria exhibit multidrug resistance, which rapidly spreads and is transferred through efficient plasmid conjugation; the multidrug resistance of these bacteria may be determined by analyzing their drug-resistant plasmids. The presence of ble and tnpA genes suggests a possible hypothesis that bla NDM-1 originates from A. baumannii, which is retained in K. pneumoniae over a long period by transposition of mobile elements.

Dataset Information

Probable Three-Species In Vivo Transfer of bla_NDM-1 in a Single Patient in Greece: Occurrence of NDM-1-Producing Klebsiella pneumoniae, Proteus mirabilis, and Morganella morganii.

Publications

Probable Three-Species In Vivo Transfer of <i>bla</i><sub>NDM-1</sub> in a Single Patient in Greece: Occurrence of NDM-1-Producing <i>Klebsiella pneumoniae</i>, <i>Proteus mirabilis</i>, and <i>Morganella morganii</i>.

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