Prevalence and Characteristic of Swine-Origin mcr-1-Positive Escherichia coli in Northeastern China

The emergence of the plasmid-mediated colistin resistance gene mcr-1 is threatening the last-line role of colistin in human medicine. With mcr-1-positive Escherichia coli (E. coli) isolated from food animal being frequently reported in China, the prevalence of mcr-1 in food animal has attracted publ...

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Main Authors: Ping Cheng, Yuqi Yang, Sai Cao, Haibin Liu, Xiaoting Li, Jichao Sun, Fulei Li, Muhammad Ishfaq, Xiuying Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.712707/full
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language English
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author Ping Cheng
Yuqi Yang
Sai Cao
Haibin Liu
Xiaoting Li
Jichao Sun
Fulei Li
Muhammad Ishfaq
Xiuying Zhang
spellingShingle Ping Cheng
Yuqi Yang
Sai Cao
Haibin Liu
Xiaoting Li
Jichao Sun
Fulei Li
Muhammad Ishfaq
Xiuying Zhang
Prevalence and Characteristic of Swine-Origin mcr-1-Positive Escherichia coli in Northeastern China
Frontiers in Microbiology
colistin resistance
mcr-1 gene
swine
Escherichia coli
prevalence
characteristics
author_facet Ping Cheng
Yuqi Yang
Sai Cao
Haibin Liu
Xiaoting Li
Jichao Sun
Fulei Li
Muhammad Ishfaq
Xiuying Zhang
author_sort Ping Cheng
title Prevalence and Characteristic of Swine-Origin mcr-1-Positive Escherichia coli in Northeastern China
title_short Prevalence and Characteristic of Swine-Origin mcr-1-Positive Escherichia coli in Northeastern China
title_full Prevalence and Characteristic of Swine-Origin mcr-1-Positive Escherichia coli in Northeastern China
title_fullStr Prevalence and Characteristic of Swine-Origin mcr-1-Positive Escherichia coli in Northeastern China
title_full_unstemmed Prevalence and Characteristic of Swine-Origin mcr-1-Positive Escherichia coli in Northeastern China
title_sort prevalence and characteristic of swine-origin mcr-1-positive escherichia coli in northeastern china
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2021-07-01
description The emergence of the plasmid-mediated colistin resistance gene mcr-1 is threatening the last-line role of colistin in human medicine. With mcr-1-positive Escherichia coli (E. coli) isolated from food animal being frequently reported in China, the prevalence of mcr-1 in food animal has attracted public attention. In the present study, a total of 105 colistin-resistant E. coli strains were isolated from 200 fecal samples collected from six swine farms in northeastern China. mcr-PCR revealed that the prevalence of mcr-1 in colistin-resistant E. coli was 53.33% (56/105). mcr-1-positive E. coli showed extensive antimicrobial resistance profiles with the presence of additional resistance genes, increased expression of multidrug efflux pump-associated genes, and increased biofilm formation ability. MLST differentiated all the mcr-1-positive E. coli into 25 sequence types (STs) and five unknown ST, and the most common ST was ST10 (n = 11). By phylogenetic group classification, the distribution of all mcr-1-positive E. coli belonging to groups A, B1, B2, and D was 46.43, 35.71, 5.36, and 5.36%, respectively. Conjugation experiment demonstrated that most of the mcr-1 were transferable at frequencies of 2.68 × 10–6–3.73 × 10–3 among 30 representative mcr-1-positive E. coli. The plasmid replicon types IncI2 (n = 9), IncX4 (n = 5), IncHI2 (n = 3), IncN (n = 3), and IncP (n = 1) were detected in the transconjugants. The results of growth assay, competition experiment, and plasmid stability testing showed that acquisition of mcr-1-harboring plasmids could reduce the fitness of bacterial hosts, but mcr-1 remained stable in the recipient strain. Due to the potential possibility of these mcr-1-positive E. coli being transmitted to humans through the food chain or through horizontal transmission, therefore, it is necessary to continuously monitor the prevalence and dissemination of mcr-1 in food animal, particularly in swine.
topic colistin resistance
mcr-1 gene
swine
Escherichia coli
prevalence
characteristics
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.712707/full
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spelling doaj-02fa5208e5834907a191c99f38b7925e2021-07-20T10:51:35ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-07-011210.3389/fmicb.2021.712707712707Prevalence and Characteristic of Swine-Origin mcr-1-Positive Escherichia coli in Northeastern ChinaPing Cheng0Yuqi Yang1Sai Cao2Haibin Liu3Xiaoting Li4Jichao Sun5Fulei Li6Muhammad Ishfaq7Xiuying Zhang8Heilongjiang Key Laboratory for Animal Disease Control and Pharmaceutical Development, Faculty of Basic Veterinary Science, College of Veterinary Medicine, Northeast Agricultural University, Harbin, ChinaPharmacology Teaching and Research Department, School of Basic Medicine, Guizhou University of Traditional Chinese Medicine, Guiyang, ChinaHeilongjiang Key Laboratory for Animal Disease Control and Pharmaceutical Development, Faculty of Basic Veterinary Science, College of Veterinary Medicine, Northeast Agricultural University, Harbin, ChinaHeilongjiang Key Laboratory for Animal Disease Control and Pharmaceutical Development, Faculty of Basic Veterinary Science, College of Veterinary Medicine, Northeast Agricultural University, Harbin, ChinaHeilongjiang Key Laboratory for Animal Disease Control and Pharmaceutical Development, Faculty of Basic Veterinary Science, College of Veterinary Medicine, Northeast Agricultural University, Harbin, ChinaHeilongjiang Key Laboratory for Animal Disease Control and Pharmaceutical Development, Faculty of Basic Veterinary Science, College of Veterinary Medicine, Northeast Agricultural University, Harbin, ChinaHeilongjiang Key Laboratory for Animal Disease Control and Pharmaceutical Development, Faculty of Basic Veterinary Science, College of Veterinary Medicine, Northeast Agricultural University, Harbin, ChinaHeilongjiang Key Laboratory for Animal Disease Control and Pharmaceutical Development, Faculty of Basic Veterinary Science, College of Veterinary Medicine, Northeast Agricultural University, Harbin, ChinaHeilongjiang Key Laboratory for Animal Disease Control and Pharmaceutical Development, Faculty of Basic Veterinary Science, College of Veterinary Medicine, Northeast Agricultural University, Harbin, ChinaThe emergence of the plasmid-mediated colistin resistance gene mcr-1 is threatening the last-line role of colistin in human medicine. With mcr-1-positive Escherichia coli (E. coli) isolated from food animal being frequently reported in China, the prevalence of mcr-1 in food animal has attracted public attention. In the present study, a total of 105 colistin-resistant E. coli strains were isolated from 200 fecal samples collected from six swine farms in northeastern China. mcr-PCR revealed that the prevalence of mcr-1 in colistin-resistant E. coli was 53.33% (56/105). mcr-1-positive E. coli showed extensive antimicrobial resistance profiles with the presence of additional resistance genes, increased expression of multidrug efflux pump-associated genes, and increased biofilm formation ability. MLST differentiated all the mcr-1-positive E. coli into 25 sequence types (STs) and five unknown ST, and the most common ST was ST10 (n = 11). By phylogenetic group classification, the distribution of all mcr-1-positive E. coli belonging to groups A, B1, B2, and D was 46.43, 35.71, 5.36, and 5.36%, respectively. Conjugation experiment demonstrated that most of the mcr-1 were transferable at frequencies of 2.68 × 10–6–3.73 × 10–3 among 30 representative mcr-1-positive E. coli. The plasmid replicon types IncI2 (n = 9), IncX4 (n = 5), IncHI2 (n = 3), IncN (n = 3), and IncP (n = 1) were detected in the transconjugants. The results of growth assay, competition experiment, and plasmid stability testing showed that acquisition of mcr-1-harboring plasmids could reduce the fitness of bacterial hosts, but mcr-1 remained stable in the recipient strain. Due to the potential possibility of these mcr-1-positive E. coli being transmitted to humans through the food chain or through horizontal transmission, therefore, it is necessary to continuously monitor the prevalence and dissemination of mcr-1 in food animal, particularly in swine.https://www.frontiersin.org/articles/10.3389/fmicb.2021.712707/fullcolistin resistancemcr-1 geneswineEscherichia coliprevalencecharacteristics