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IS26 Is Responsible for the Evolution and Transmission of bla_NDM-Harboring Plasmids in Escherichia coli of Poultry Origin in China.

ABSTRACT: Carbapenem-resistant Enterobacteriaceae are some of the most important pathogens responsible for nosocomial infections, which can be challenging to treat. The bla_NDM carbapenemase genes, which are expressed by New Delhi metallo-β-lactamase (NDM)-producing Escherichia coli isolates, have been found in humans, environmental samples, and multiple other sources worldwide. Importantly, these genes have also been found in farm animals, which are considered an NDM reservoir and an important source of human infections. However, the dynamic evolution of bla_NDM genetic contexts and bla_NDM-harboring plasmids has not been directly observed, making it difficult to assess the extent of horizontal dissemination of the bla_NDM gene. In this study, we detected NDM-1 (n = 1), NDM-5 (n = 24), and NDM-9 (n = 8) variants expressed by E. coli strains isolated from poultry in China from 2016 to 2017. By analyzing the immediate genetic environment of the bla_NDM genes, we found that IS26 was associated with multiple types of bla_NDM multidrug resistance regions, and we identified various IS26-derived circular intermediates. Importantly, in E. coli strain GD33, we propose that IncHI2 and IncI1 plasmids can fuse when IS26 is present. Our analysis of the IS26 elements flanking bla_NDM allowed us to propose an important role for IS26 elements in the evolution of multidrug-resistant regions (MRRs) and in the dissemination of bla_NDM. To the best of our knowledge, this is the first description of the dynamic evolution of bla_NDM genetic contexts and bla_NDM-harboring plasmids. These findings could help proactively limit the transmission of these NDM-producing isolates from food animals to humans. IMPORTANCE Carbapenem resistance in members of the order Enterobacterales is a growing public health problem that is associated with high mortality in developing and industrialized countries. Moreover, in the field of veterinary medicine, the occurrence of New Delhi metallo-β-lactamase-producing Escherichia coli isolates in animals, especially food-producing animals, has become a growing concern in recent years. The wide dissemination of bla_NDM is closely related to mobile genetic elements (MGEs) and plasmids. Although previous analyses have explored the association of many different MGEs with mobilization of bla_NDM, little is known about the evolution of various genetic contexts of bla_NDM in E. coli. Here, we report the important role of IS26 in forming multiple types of bla_NDM multidrug resistance cassettes and the dynamic recombination of plasmids bearing bla_NDM. These results suggest that significant attention should be paid to monitoring the transmission and further evolution of bla_NDM-harboring plasmids among E. coli strains of food animal origin.

SUBMITTER: Zhao QY

PROVIDER: S-EPMC8407110 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:New Delhi metallo-β-lactamases (NDMs), including at least 28 variants, are a rapidly emerging family of β-lactamases worldwide, with a variety of infections caused by NDM-positive strains usually associated with very poor prognosis and high mortality. NDMs are the most prevalent carbapenemases in Escherichia coli (E. coli) worldwide, especially in China. The vast majority of bla NDM cases occur on plasmids, which play a vital role in the dissemination of bla NDM. To systematically explore the relationships between plasmids and bla NDM genes in E. coli and obtain an overall picture of the conjugative and mobilizable bla NDM-positive plasmids, we analyzed the variants of bla NDM, replicon types, phylogenetic patterns, conjugative transfer modules, host STs, and geographical distributions of 114 bla NDM-positive plasmids, which were selected from 3786 plasmids from 1346 complete whole genomes of E. coli from the GenBank database. We also established links among the characteristics of bla NDM-positive plasmids in E. coli. Eight variants of bla NDM were found among the 114 bla NDM-positive plasmids, with bla NDM - 5 (74 bla NDM - 5 genes in 73 plasmids), and bla NDM - 1 (31 bla NDM - 1 genes in 28 plasmids) being the most dominant. The variant bla NDM - 5 was mainly carried by the IncX3 plasmids and IncF plasmids in E. coli, the former were mainly geographically distributed in East Asia (especially in China) and the United States, and the latter were widely distributed worldwide. IncC plasmids were observed to be the predominant carriers of bla NDM - 1 genes in E. coli, which were mainly geographically distributed in the United States and China. Other bla NDM - 1-carrying plasmids also included IncM2, IncN2, and IncHI1. Moreover, the overall picture of the conjugative and mobilizable bla NDM-positive plasmids in E. coli was described in our study. Our findings enhance our understanding of the genetic diversity and characteristics of bla NDM-positive plasmids in in E. coli.

Project description:Although the prevalence of carbapenem-resistant Enterobacterales remains low in Japan, these bacteria are a growing problem worldwide, owing to their multidrug resistance phenotype. We isolated a multidrug-resistant Providencia rettgeri strain, NR1418, harboring a rare blaIMP variant, blaIMP-70, a novel blaCTX-M variant, designated blaCTX-M-253, and blaMOX-1. This strain is resistant to β-lactams, amikacin, levofloxacin, and colistin. Genomic analysis revealed that NR1418 carries two plasmids, designated pNR1418-1 and pNR1418-2. The pNR1418-1 plasmid harbors blaCTX-M-253, blaTEM-1, and blaMOX-1, while the pNR1418-2 plasmid harbors blaIMP-70, which is located in a class 1 integron. Both plasmids exhibit high similarities with the plasmid of the P. rettgeri isolate BML2526, which also harbors blaIMP-70 and was identified in the same region of Japan as NR1418 at a different point in time. This indicates the possibility of the emergence and evolution of IMP-70-producing P. rettgeri and suggests that the plasmid of BML2526 may have occurred following recombination of the two plasmids harbored by NR1418. Further, blaIMP-70 and blaCTX-M-253 were found on unique plasmids, indicating that they likely evolved through mutations and recombination. IMPORTANCE Although Providencia rettgeri is an opportunistic pathogen, its intrinsic resistance to colistin and tigecycline makes the treatment of carbapenem-resistant P. rettgeri challenging. We isolated a multidrug-resistant P. rettgeri strain which harbored a rare blaIMP variant, blaIMP-70, a novel blaCTX-M variant, blaCTX-M-253, and blaMOX-1 from a urinary sample obtained in Osaka, Japan. We investigated its genetic structure and evaluated the evolution of the plasmids carrying these genes. We show that blaIMP-70, blaCTX-M-253, and blaMOX-1 are present on unique plasmids and that they have high similarities to the plasmid of another IMP-70-producing P. rettgeri isolate that was identified as being from the same location. The evolution of plasmids through mutations and recombination may play a role in the development and spread of multidrug resistance.

Project description:Aim of this study was to genetically characterize two carbapenemase-producing Escherichia coli strains obtained from a pediatric patient affected by diarrhea, expressing OXA-181 and/or NDM-5 type enzymes. The above microorganisms were collected in the same Desenzano hospital (Northern Italy) where the bla NDM- 5 gene was detected for the first time in Italy 3 years ago. One strain (5P), belonged to sequence type ST405/ST477 (according to Pasture/Oxford schemes) and serotype O102:H6. It was characterized by a 130562 bp multi-replicon plasmid IncFII/IncFIA/IncFIB (pVSI_NDM-5) enclosing two main antibiotic resistance islands: (i) ARI-I, 10030 bp in size, carried genes coding for β-lactam- (bla OXA- 1, bla CTX-M- 15), fluoroquinolone/aminoglycoside- (aac(6')-lb-cr) and phenicol- resistance (catB3), (ii) ARI-II, 15326 bp in size, carried genes coding for sulfonamide- (sul1), β-lactam- (bla NDM- 5, bla TEM- 1 B), phenicol- (catB3), trimethoprim- (dfrA17), antiseptic- (qacEΔ1), and aminoglycoside- (aadA5, rmtB) resistance. The other isolate (5M), belonged to sequence type ST2659/ST759 and serotype O50/02:H18, and carried four plasmids: a 153866 bp multi-replicon IncFII/IncFIA/IncFIB (pISV_IncFII_NDM-5), an 89866 bp IncI1 plasmid, a 51480 bp IncX3 plasmid (pISV_IncX3_OXA181), and a 41143 bp IncI plasmid (pISV_IncI_CMY-42). pISV_IncFII_NDM-5 carried two main antibiotic resistance islands: (i) ARI-III, 12220 bp in size, carried genes coding for β-lactam- (bla OXA- 1), fluoroquinolone/aminoglycoside- (aac(6')-lb-cr), tetracycline- (tet(B)) and phenicol- resistance (catB3, catA1), and ii) ARI-IV, 26527 bp in size, carried determinants coding for macrolide- (erm(B), mph(A)), sulfonamide- (sul1), beta-lactam- (bla NDM- 5, bla TEM- 1 B), trimethoprim- (dfrA14, dfrA12), antiseptic- (qacEΔ1), and aminoglycoside- resistance (aadA5). pISV_IncI_CMY-42 harbored the bla CMY- 42 gene coding for beta-lactam resistance, pISV_IncX3_OXA181 harbored genes encoding fluoroquinolone- (qnrS1) and beta-lactams- resistance (bla OXA- 181). In conclusion, the detection of two different NDM-5 E. coli strains from a pediatric patient with a history of travel to the Far East countries strongly highlight an increasing trend and risk of importation from such areas.

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IS26 Is Responsible for the Evolution and Transmission of bla_NDM-Harboring Plasmids in Escherichia coli of Poultry Origin in China.

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Dataset Information

IS26 Is Responsible for the Evolution and Transmission of blaNDM-Harboring Plasmids in Escherichia coli of Poultry Origin in China.

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OmicsDI is part of the ELIXIR infrastructure

Tweets

IS26 Is Responsible for the Evolution and Transmission of bla_NDM-Harboring Plasmids in Escherichia coli of Poultry Origin in China.