Chromosomally and Plasmid-Located mcr in Salmonella from Animals and Food Products in China

ABSTRACT This study aimed to investigate the prevalence and genomic characteristics of the colistin resistance gene mcr in Salmonella enterica in China. In total, 445 S. enterica isolates from animals and food products were screened through PCR and sequencing for the presence of mcr. The mcr genes w...

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Main Authors: Cai-Yue Mei, Yue Jiang, Qin-Chun Ma, Meng-Jun Lu, Han Wu, Zhen-Yu Wang, Xinan Jiao, Jing Wang
Format: Article
Language:English
Published: American Society for Microbiology 2022-12-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.02773-22
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author Cai-Yue Mei
Yue Jiang
Qin-Chun Ma
Meng-Jun Lu
Han Wu
Zhen-Yu Wang
Xinan Jiao
Jing Wang
author_facet Cai-Yue Mei
Yue Jiang
Qin-Chun Ma
Meng-Jun Lu
Han Wu
Zhen-Yu Wang
Xinan Jiao
Jing Wang
author_sort Cai-Yue Mei
collection DOAJ
description ABSTRACT This study aimed to investigate the prevalence and genomic characteristics of the colistin resistance gene mcr in Salmonella enterica in China. In total, 445 S. enterica isolates from animals and food products were screened through PCR and sequencing for the presence of mcr. The mcr genes were detected in nine Salmonella strains (2.02%), with complete mcr-1 in S. enterica serovar Indiana (n = 1) and an S. Typhimurium monophasic variant (S. 4,[5],12:i:-; n = 1), mcr-4.3 in S. enterica serovar London (n = 1), and an incomplete mcr-1 in S. Indiana (n = 6). They exhibited MIC values of 0.25 to 8 mg/L to colistin and showed resistance to multiple antimicrobial agents. Whole-genome sequencing was performed on mcr-positive Salmonella strains using Illumina HiSeq or PacBio single-molecule real-time sequencing. The complete mcr-1 gene was located on conjugative IncN1-IncHI2 plasmid and IncX4 plasmid, respectively, with high similarity to other mcr-1-bearing plasmids belonging to the same incompatibility type. Together with an additional 13 antimicrobial resistance genes, the incomplete mcr-1 was embedded in an 81,442-bp multiresistance region on the chromosome in S. Indiana YZ20MCS6. The Δmcr-1-pap2 segment and a set of tellurite resistance determinants (terYXWZABCDEF) in six S. Indiana strains were similar to other IncHI2 plasmid backbones. The mcr-4.3 gene was located on an untyped plasmid pYULZMPS10. Although low prevalence of mcr was observed in Salmonella, continuous surveillance of this gene in Salmonella is required. Plasmids play an important role in mcr transmission, and mcr-1, although incomplete, can be captured by chromosomes with the help of mobile elements. IMPORTANCE Colistin is a last-resort antibiotic for severe infections caused by multidrug-resistant (MDR) Gram-negative pathogens. Colistin resistance genes mcr, particularly mcr-1, have been found in Enterobacteriaceae around the world, mainly in Escherichia coli and Salmonella. Salmonella enterica is a major foodborne pathogen, with MDR Salmonella being considered a “Serious Threat Level pathogen” by the Centers for Disease Control and Prevention. Therefore, the prevalence of mcr in Salmonella strains must be monitored. In this study, a low mcr prevalence (2.02%) was observed in Salmonella strains from animals and food products, with plasmid-borne mcr-1 in S. enterica serovar Indiana and an S. Typhimurium monophasic variant (S. 4,[5],12:i:-) and chromosomally located mcr-1 in S. Indiana. The mcr-4.3 gene was first identified in S. enterica serovar London associated with an untyped plasmid. Although this study reports a low mcr prevalence in Salmonella, the transmission ability of mcr-positive Salmonella strains to humans via the food chain is a public health concern.
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spelling doaj.art-ff7c827cd6f14787854631f082ad4d892022-12-22T03:55:10ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-12-0110610.1128/spectrum.02773-22Chromosomally and Plasmid-Located mcr in Salmonella from Animals and Food Products in ChinaCai-Yue Mei0Yue Jiang1Qin-Chun Ma2Meng-Jun Lu3Han Wu4Zhen-Yu Wang5Xinan Jiao6Jing Wang7Jiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, ChinaJiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, ChinaJiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, ChinaJiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, ChinaJiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, ChinaJiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, ChinaJiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, ChinaJiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, ChinaABSTRACT This study aimed to investigate the prevalence and genomic characteristics of the colistin resistance gene mcr in Salmonella enterica in China. In total, 445 S. enterica isolates from animals and food products were screened through PCR and sequencing for the presence of mcr. The mcr genes were detected in nine Salmonella strains (2.02%), with complete mcr-1 in S. enterica serovar Indiana (n = 1) and an S. Typhimurium monophasic variant (S. 4,[5],12:i:-; n = 1), mcr-4.3 in S. enterica serovar London (n = 1), and an incomplete mcr-1 in S. Indiana (n = 6). They exhibited MIC values of 0.25 to 8 mg/L to colistin and showed resistance to multiple antimicrobial agents. Whole-genome sequencing was performed on mcr-positive Salmonella strains using Illumina HiSeq or PacBio single-molecule real-time sequencing. The complete mcr-1 gene was located on conjugative IncN1-IncHI2 plasmid and IncX4 plasmid, respectively, with high similarity to other mcr-1-bearing plasmids belonging to the same incompatibility type. Together with an additional 13 antimicrobial resistance genes, the incomplete mcr-1 was embedded in an 81,442-bp multiresistance region on the chromosome in S. Indiana YZ20MCS6. The Δmcr-1-pap2 segment and a set of tellurite resistance determinants (terYXWZABCDEF) in six S. Indiana strains were similar to other IncHI2 plasmid backbones. The mcr-4.3 gene was located on an untyped plasmid pYULZMPS10. Although low prevalence of mcr was observed in Salmonella, continuous surveillance of this gene in Salmonella is required. Plasmids play an important role in mcr transmission, and mcr-1, although incomplete, can be captured by chromosomes with the help of mobile elements. IMPORTANCE Colistin is a last-resort antibiotic for severe infections caused by multidrug-resistant (MDR) Gram-negative pathogens. Colistin resistance genes mcr, particularly mcr-1, have been found in Enterobacteriaceae around the world, mainly in Escherichia coli and Salmonella. Salmonella enterica is a major foodborne pathogen, with MDR Salmonella being considered a “Serious Threat Level pathogen” by the Centers for Disease Control and Prevention. Therefore, the prevalence of mcr in Salmonella strains must be monitored. In this study, a low mcr prevalence (2.02%) was observed in Salmonella strains from animals and food products, with plasmid-borne mcr-1 in S. enterica serovar Indiana and an S. Typhimurium monophasic variant (S. 4,[5],12:i:-) and chromosomally located mcr-1 in S. Indiana. The mcr-4.3 gene was first identified in S. enterica serovar London associated with an untyped plasmid. Although this study reports a low mcr prevalence in Salmonella, the transmission ability of mcr-positive Salmonella strains to humans via the food chain is a public health concern.https://journals.asm.org/doi/10.1128/spectrum.02773-22Salmonellamcr-1mcr-4.3plasmidchromosome
spellingShingle Cai-Yue Mei
Yue Jiang
Qin-Chun Ma
Meng-Jun Lu
Han Wu
Zhen-Yu Wang
Xinan Jiao
Jing Wang
Chromosomally and Plasmid-Located mcr in Salmonella from Animals and Food Products in China
Microbiology Spectrum
Salmonella
mcr-1
mcr-4.3
plasmid
chromosome
title Chromosomally and Plasmid-Located mcr in Salmonella from Animals and Food Products in China
title_full Chromosomally and Plasmid-Located mcr in Salmonella from Animals and Food Products in China
title_fullStr Chromosomally and Plasmid-Located mcr in Salmonella from Animals and Food Products in China
title_full_unstemmed Chromosomally and Plasmid-Located mcr in Salmonella from Animals and Food Products in China
title_short Chromosomally and Plasmid-Located mcr in Salmonella from Animals and Food Products in China
title_sort chromosomally and plasmid located mcr in salmonella from animals and food products in china
topic Salmonella
mcr-1
mcr-4.3
plasmid
chromosome
url https://journals.asm.org/doi/10.1128/spectrum.02773-22
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