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Genomic Characterization of mcr-1-Carrying Foodborne Salmonella enterica serovar Typhimurium and Identification of a Transferable Plasmid Carrying mcr-1, blaCTX-M-14, qnrS2, and oqxAB Genes From Ready-to-Eat Pork Product in China

ABSTRACT: Salmonella enterica resistant to colistin, third-generation cephalosporins (3GCs), and fluoroquinolones (FQs) has been deemed a high-priority pathogen by the World Health Organization (WHO). The objective of this study was to characterize 11 mcr-1-harboring Salmonella enterica serovar Typhimurium isolates from raw pork and ready-to-eat (RTE) pork products in Guangzhou, China. All isolates were multi-drug resistant and contained 6–24 antibiotic-resistant genes. The mcr-1 gene was localized in the most conserved structure (mcr-1-orf ) in eight isolates and in mobile structure (ISApl1-mcr-1-orf ) in three isolates. One raw pork isolate SH16SF0850, co-harbored mcr-1, blaCTX−M−14, and oqxAB genes. One isolate 17Sal008 carried mcr-1, blaCTX−M−14, qnrS2, and oqxAB genes located on a 298,622 bp IncHI2 plasmid pSal008, which was obtained from an RTE pork product for the first time. The pSal008 was closely related to a plasmid in an S. typhimurium isolate from a 1-year-old diarrheal outpatient in China and was found to be transferable to Escherichia coli J53 by conjugation. Genome sequence comparisons by core-genome Multi Locus Sequence Typing (cgMLST) based on all S. typhimurium isolates from China inferred highly probably epidemiological links between selected pork isolates and no possible epidemiologically links between RTE pork isolate 17Sal008 and other isolates. Our findings indicate that raw pork and pork products are potential reservoirs of mcr-1-harboring S. typhimurium and highlight the necessity for continuous monitoring of colistin, 3GCs, and FQs resistant S. typhimurium from different origins.

SUBMITTER: Li L

PROVIDER: S-EPMC9277226 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:One mcr-1-carrying ST34-type Salmonella Typhimurium WW012 was cultured from 3,200 ready-to-eat (RTE) pork samples in 2014 in China. Broth dilution method was applied to obtain the antimicrobial susceptibility of Salmonella Typhimurium WW012. Broth matting assays were carried out to detect transferability of this phenotype and whole-genome sequencing was performed to analyze its genomic characteristic. Thirty out of 3,200 RTE samples were positive for Salmonella and the three most frequent serotypes were identified as S. Derby (n = 8), S. Typhimurium (n = 6), and S. Enteritidis (n = 6). One S. Typhimurium isolate (S. Typhimurium WW012) cultured from RTE prepared pork was found to contain the mcr-1 gene. S. Typhimurium WW012 expressed a level of high resistance to seven different antimicrobial compounds in addition to colistin (MIC = 8 mg/L). A single plasmid, pWW012 (151,609-bp) was identified and found to be of an IncHI2/HI2A type that encoded a mcr-1 gene along with six additional antimicrobial resistance genes. Plasmid pWW012 contained an IS30-mcr-1-orf-orf-IS30 composite transposon that can be successfully transferred to Escherichia coli J53. When assessed further, the latter demonstrated considerable similarity to three plasmids pHYEC7-mcr-1, pSCC4, and pHNSHP45-2, respectively. Furthermore, plasmid pWW012 also contained a multidrug resistance (MDR) genetic structure IS26-aadA2-cmlA2-aadA1-IS406-sul3-IS26-dfrA12-aadA2-IS26, which showed high similarity to two plasmids, pHNLDF400 and pHNSHP45-2, respectively. Moreover, genes mapping to the chromosome (4,991,167-bp) were found to carry 28 mutations, related to two component regulatory systems (pmrAB, phoPQ) leading to modifications of lipid A component of the lipopolysaccharide structure. Additionally, one mutation (D87N) in the quinolone resistance determining region (QRDR) gene of gyrA was identified in this mcr-1 harboring S. Typhimurium. In addition, various virulence factors and heavy metal resistance-encoding genes were also identified on the genome of S. Typhimurium WW012. This is the first report of the complete nucleotide sequence of mcr-1-carrying MDR S. Typhimurium strain from RTE pork in China.

Project description:BackgroundPolymyxins are currently regarded as a possible last-resort therapy to eradicate multidrug-resistant (MDR) gram-negative bacteria. Meanwhile, the old antimicrobial agent fosfomycin has recently been reintroduced into clinical use for the treatment of extended-spectrum β-lactamase (ESBL)-producing and carbapenem-resistant Enterobacteriaceae. This study investigated a multidrug-resistant Salmonella 4,[5],12:i:- strain from a food catering handler, which had the potential to act as a vehicle for transmitting MDR foodborne pathogens.MethodsA Salmonella 4,[5],12:i:- YZU1189 strain was isolated from the fecal sample of a food catering worker according to the standard protocol of the Salmonella detection method from World Health Organization in 2003. Serotyping of YZU1189 was performed according to the Kauffmann-White scheme. The antimicrobial resistance phenotype of the strain was determined by the agar dilution method according to the instruction from Clinical and Laboratory Standards Institute (CLSI). Plasmid conjugation was performed between the donor strain Salmonella 4,[5],12:i:- YZU1189 and the recipient strain Escherichia coli C600. The genetic locations of mcr-1, bla CTX-M-14 and fosA3 genes were determined by the whole genome sequence analysis.ResultsSalmonella 4,[5],12:i:- YZU1189 was an ESBL-producing stain isolated from a healthy catering worker. The strain displayed resistance to aminoglycosides, beta-lactams, polymyxins, fosfomycins, phenicols, trimethoprims, sulfonamides, tetracyclines and fluoroquinolones. Whole genome sequence analysis and plasmid conjugation revealed that the strain had a transferable IncHI2 plasmid carrying the mcr-1, bla CTX-M-14 and fosA3 genes. Sequence homology analysis showed that this plasmid possessed high sequence similarity to previously reported mcr-1, bla CTX-M-14 and fosA3 positive plasmids in China.ConclusionThis study reported a the multidrug-resistant Salmonella 4,[5],12:i:- isolate harboring mcr-1, bla CTX-M-14 and fosA3 from human for the first time in China. The occurrence of mcr-1 and fosA3 genes in the transferable IncHI2 plasmid pYZU1189 from the ESBL-producing Salmonella 4,[5],12:i:- isolate showed a potential threat to public health. Great concern should be taken for the spread of multidrug-resistant ESBL-producing Salmonella isolates from food catering workers to consumers.

Project description:Colistin is an important antibiotic currently used to manage infections caused by multidrug-resistant pathogens in both humans and livestock animals. A new mobile colistin-resistance (mcr-9) gene was recently discovered; this discovery highlighted the need for rigorous monitoring of bacterial resistance against colistin. Salmonella is one of the major pathogens responsible for foodborne illnesses; however, there is minimal information regarding the presence of mcr genes in foodborne Salmonella strains. The aim of this study was to investigate the presence of mcr genes among 178 Salmonella strains isolated from chicken meat in Korea. Antimicrobial susceptibility was measured using the broth microdilution method. Bioinformatics characterization of colistin-resistant strains and genetic environment of the mcr-9 gene were analyzed using next-generation sequencing. Transferability of the mcr-9 carrying colistin-resistant Salmonella strain was tested using broth-mating conjugation. Thirteen of the 178 Salmonella isolates showed colistin resistance, but only one strain, Salmonella Dessau ST14 (KUFSE-SAL043) from a traditional chicken market in Korea, carried an mcr family gene, mcr-9. This strain also carried other acquired antimicrobial resistance genes such as blaTEM-1B, qnrS1, and aac(6')-Iaa. Only the IncX1 plasmid replicon type was detected in this strain. In the strain KUFSE-SAL043, the mcr-9 gene was located between two insertion sequences, IS903B and IS26, followed by the downstream regulatory genes qseB-like and qseC-like, which were located between IS1R and ΔIS1R. Conjugation tests revealed that the mcr-9 gene was successfully transferred to Escherichia coli J53 at a mean frequency of 2.03 × 10-7. This is the first report of a transferable mcr-9 gene in Salmonella isolated from chicken meat in Korea, highlighting the possibility of transfer of colistin resistance. Therefore, the wide use of colistin should be reconsidered, and a One Health perspective should be adopted to monitor the antimicrobial resistance of Enterobacteriaceae strains in humans, livestock, and the environment.

Dataset Information

Genomic Characterization of mcr-1-Carrying Foodborne Salmonella enterica serovar Typhimurium and Identification of a Transferable Plasmid Carrying mcr-1, blaCTX-M-14, qnrS2, and oqxAB Genes From Ready-to-Eat Pork Product in China

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