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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American Society for Microbiology
2023-02-01
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Series: | Microbiology Spectrum |
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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. |
first_indexed | 2024-04-10T15:21:39Z |
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institution | Directory Open Access Journal |
issn | 2165-0497 |
language | English |
last_indexed | 2024-04-10T15:21:39Z |
publishDate | 2023-02-01 |
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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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