Distribution and Transmission of Colistin Resistance Genes mcr-1 and mcr-3 among Nontyphoidal Salmonella Isolates in China from 2011 to 2020

ABSTRACT Mobile colistin resistance (mcr) genes are present mainly in plasmids and can disseminate clonally or horizontally via either plasmids or insertion sequences in different genomic locations among the Enterobacteriaceae. A nationwide large-scale study on mcr prevalence and transmission in non...

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Main Authors: Tingting Yang, Weiwei Li, Qingpo Cui, Xiaoxia Qin, Bosheng Li, Xiugui Li, Huayun Jia, Xiaorong Yang, Chengwei Liu, Yang Wang, Shaolin Wang, Jianzhong Shen, Yunchang Guo, Zhangqi Shen
Format: Article
Language:English
Published: American Society for Microbiology 2023-02-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.03833-22
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author Tingting Yang
Weiwei Li
Qingpo Cui
Xiaoxia Qin
Bosheng Li
Xiugui Li
Huayun Jia
Xiaorong Yang
Chengwei Liu
Yang Wang
Shaolin Wang
Jianzhong Shen
Yunchang Guo
Zhangqi Shen
author_facet Tingting Yang
Weiwei Li
Qingpo Cui
Xiaoxia Qin
Bosheng Li
Xiugui Li
Huayun Jia
Xiaorong Yang
Chengwei Liu
Yang Wang
Shaolin Wang
Jianzhong Shen
Yunchang Guo
Zhangqi Shen
author_sort Tingting Yang
collection DOAJ
description ABSTRACT Mobile colistin resistance (mcr) genes are present mainly in plasmids and can disseminate clonally or horizontally via either plasmids or insertion sequences in different genomic locations among the Enterobacteriaceae. A nationwide large-scale study on mcr prevalence and transmission in nontyphoidal Salmonella isolates is still lacking. Here, we identified 140 mcr-positive Salmonella isolates out of 7,106 isolates from 29 provinces in China from 2011 to 2020. We aligned short reads to putative plasmids from long-read hybrid assemblies and predicted the plasmid backbones of non-long-read sequencing isolates to elucidate mcr transmission patterns. The mcr-1 and mcr-3 genes are transmitted on similar high-risk clones (sequence type 34 [ST34]) but through plasmids of various replicon types. Furthermore, the ban on colistin use in food animals can lead to a decrease in the mcr-positive Salmonella prevalence among diarrheal patients, related mainly to IncHI2A_IncHI2 plasmids. We provide a framework for plasmid data incorporation into genomic surveillance systems, contributing to a better understanding of mcr spread and transmission. IMPORTANCE Nontyphoidal Salmonella is one of four major causative agents of diarrheal diseases globally, with most cases of salmonellosis being mild. Antimicrobial treatments are required for cases of life-threatening infections, and colistin is one of the last-line antibiotics for the treatment of multidrug-resistant Salmonella infections. However, the efficacy of colistin has been compromised by the emergence of various mcr genes. To elucidate the transmission of mcr genes in Salmonella isolates, our study analyzed 7,106 Salmonella strains from 29 provinces in China from 2011 to 2020. The results showed that mcr genes are transmitted on similar high-risk clones (ST34) but through plasmids of various replicon types. In addition, our data illustrated that the ban on the use of colistin in food animals led to a significant decrease in mcr-positive isolates. Our findings offer an essential step toward a more comprehensive understanding of the spread and transmission of mcr genes.
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spelling doaj.art-831f397de7a64a44a5f1ca3276a3f9d52023-02-14T14:15:49ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-02-0111110.1128/spectrum.03833-22Distribution and Transmission of Colistin Resistance Genes mcr-1 and mcr-3 among Nontyphoidal Salmonella Isolates in China from 2011 to 2020Tingting Yang0Weiwei Li1Qingpo Cui2Xiaoxia Qin3Bosheng Li4Xiugui Li5Huayun Jia6Xiaorong Yang7Chengwei Liu8Yang Wang9Shaolin Wang10Jianzhong Shen11Yunchang Guo12Zhangqi Shen13Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaNational Health Commission Key Laboratory of Food Safety Risk Assessment, Chinese Academy of Medical Science Research Unit (No. 2019RU014), China National Center for Food Safety Risk Assessment, Beijing, ChinaBeijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaBeijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaGuangdong Provincial Center for Disease Control and Prevention, Guangzhou, ChinaGuangxi Provincial Center for Disease Control and Prevention, Nanning, ChinaHunan Provincial Center for Disease Control and Prevention, Changsha, ChinaSichuan Provincial Center for Disease Control and Prevention, Chengdu, ChinaJiangxi Provincial Center for Disease Control and Prevention, Jiangxi, ChinaBeijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaBeijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaBeijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaNational Health Commission Key Laboratory of Food Safety Risk Assessment, Chinese Academy of Medical Science Research Unit (No. 2019RU014), China National Center for Food Safety Risk Assessment, Beijing, ChinaBeijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaABSTRACT Mobile colistin resistance (mcr) genes are present mainly in plasmids and can disseminate clonally or horizontally via either plasmids or insertion sequences in different genomic locations among the Enterobacteriaceae. A nationwide large-scale study on mcr prevalence and transmission in nontyphoidal Salmonella isolates is still lacking. Here, we identified 140 mcr-positive Salmonella isolates out of 7,106 isolates from 29 provinces in China from 2011 to 2020. We aligned short reads to putative plasmids from long-read hybrid assemblies and predicted the plasmid backbones of non-long-read sequencing isolates to elucidate mcr transmission patterns. The mcr-1 and mcr-3 genes are transmitted on similar high-risk clones (sequence type 34 [ST34]) but through plasmids of various replicon types. Furthermore, the ban on colistin use in food animals can lead to a decrease in the mcr-positive Salmonella prevalence among diarrheal patients, related mainly to IncHI2A_IncHI2 plasmids. We provide a framework for plasmid data incorporation into genomic surveillance systems, contributing to a better understanding of mcr spread and transmission. IMPORTANCE Nontyphoidal Salmonella is one of four major causative agents of diarrheal diseases globally, with most cases of salmonellosis being mild. Antimicrobial treatments are required for cases of life-threatening infections, and colistin is one of the last-line antibiotics for the treatment of multidrug-resistant Salmonella infections. However, the efficacy of colistin has been compromised by the emergence of various mcr genes. To elucidate the transmission of mcr genes in Salmonella isolates, our study analyzed 7,106 Salmonella strains from 29 provinces in China from 2011 to 2020. The results showed that mcr genes are transmitted on similar high-risk clones (ST34) but through plasmids of various replicon types. In addition, our data illustrated that the ban on the use of colistin in food animals led to a significant decrease in mcr-positive isolates. Our findings offer an essential step toward a more comprehensive understanding of the spread and transmission of mcr genes.https://journals.asm.org/doi/10.1128/spectrum.03833-22nontyphoidal Salmonellamcrcolistinplasmidgenome
spellingShingle Tingting Yang
Weiwei Li
Qingpo Cui
Xiaoxia Qin
Bosheng Li
Xiugui Li
Huayun Jia
Xiaorong Yang
Chengwei Liu
Yang Wang
Shaolin Wang
Jianzhong Shen
Yunchang Guo
Zhangqi Shen
Distribution and Transmission of Colistin Resistance Genes mcr-1 and mcr-3 among Nontyphoidal Salmonella Isolates in China from 2011 to 2020
Microbiology Spectrum
nontyphoidal Salmonella
mcr
colistin
plasmid
genome
title Distribution and Transmission of Colistin Resistance Genes mcr-1 and mcr-3 among Nontyphoidal Salmonella Isolates in China from 2011 to 2020
title_full Distribution and Transmission of Colistin Resistance Genes mcr-1 and mcr-3 among Nontyphoidal Salmonella Isolates in China from 2011 to 2020
title_fullStr Distribution and Transmission of Colistin Resistance Genes mcr-1 and mcr-3 among Nontyphoidal Salmonella Isolates in China from 2011 to 2020
title_full_unstemmed Distribution and Transmission of Colistin Resistance Genes mcr-1 and mcr-3 among Nontyphoidal Salmonella Isolates in China from 2011 to 2020
title_short Distribution and Transmission of Colistin Resistance Genes mcr-1 and mcr-3 among Nontyphoidal Salmonella Isolates in China from 2011 to 2020
title_sort distribution and transmission of colistin resistance genes mcr 1 and mcr 3 among nontyphoidal salmonella isolates in china from 2011 to 2020
topic nontyphoidal Salmonella
mcr
colistin
plasmid
genome
url https://journals.asm.org/doi/10.1128/spectrum.03833-22
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