A Large Spatial Survey of Colistin-Resistant Gene <i>mcr-1</i>-Carrying <i>E. coli</i> in Rivers across Taiwan

Background: Colistin is one of the last-line antimicrobial agents against life-threatening infections. The distribution of the colistin resistance gene <i>mcr-1</i> has been reported worldwide. However, most studies have focused on the distribution of <i>mcr-1</i>-positive ba...

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Main Authors: Ching-Hao Teng, Pin-Chieh Wu, Sen-Lin Tang, Yi-Chen Chen, Ming-Fang Cheng, Ping-Chih Huang, Wen-Chien Ko, Jiun-Ling Wang
Format: Article
Language:English
Published: MDPI AG 2021-03-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/9/4/722
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author Ching-Hao Teng
Pin-Chieh Wu
Sen-Lin Tang
Yi-Chen Chen
Ming-Fang Cheng
Ping-Chih Huang
Wen-Chien Ko
Jiun-Ling Wang
author_facet Ching-Hao Teng
Pin-Chieh Wu
Sen-Lin Tang
Yi-Chen Chen
Ming-Fang Cheng
Ping-Chih Huang
Wen-Chien Ko
Jiun-Ling Wang
author_sort Ching-Hao Teng
collection DOAJ
description Background: Colistin is one of the last-line antimicrobial agents against life-threatening infections. The distribution of the colistin resistance gene <i>mcr-1</i> has been reported worldwide. However, most studies have focused on the distribution of <i>mcr-1</i>-positive bacteria in humans, animals, food, and sewage; few have focused on their distribution in natural environments. Method: We conducted a large spatial survey of <i>mcr-1</i>-positive <i>Escherichia coli</i> at 119 sites in 48 rivers, covering the entire island of Taiwan. We investigated the relationship between the livestock or poultry density in the surveyed riverine area and the number of <i>mcr-1</i>-positive <i>E. coli</i> in the river water. We then sequenced and characterized the isolated <i>mcr-1</i>-positive plasmids. Results: Seven <i>mcr-1</i> positive <i>E. coli</i> were isolated from 5.9% of the sampling sites. The <i>mcr-1</i>-positive sites correlated with high chicken and pig stocking densities but not human population density or other river parameters. Four of the <i>mcr-1</i>-positive <i>E. coli</i> strains harbored epidemic IncX4 plasmids, and three of them exhibited identical sequences with a size of 33,309 bp. One of the plasmids contained identical 33,309 bp sequences but carried an additional 5711-bp transposon (Tn3 family). To our knowledge, this is the first demonstration that <i>mcr-1</i>-carrying IncX4 plasmids can contain an insertion of such transposons. All <i>mcr-1</i>-positive isolates belonged to phylogenetic group A and harbored few known virulence genes. Conclusion: This study showed a positive relationship between the number of <i>mcr-1</i>-positive sites and high livestock and poultry density. The sequencing analyses indicated that the epidemic plasmid in the <i>mcr-1</i> isolates circulates not only in humans, animals, and food but also in the associated environments or natural habitats in Taiwan, suggesting that the surveillance of antibiotics-resistance genes for livestock or poultry farm quality control should include their associated environments.
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spelling doaj.art-0423320d9b204950acbb326200c571692023-11-21T13:33:46ZengMDPI AGMicroorganisms2076-26072021-03-019472210.3390/microorganisms9040722A Large Spatial Survey of Colistin-Resistant Gene <i>mcr-1</i>-Carrying <i>E. coli</i> in Rivers across TaiwanChing-Hao Teng0Pin-Chieh Wu1Sen-Lin Tang2Yi-Chen Chen3Ming-Fang Cheng4Ping-Chih Huang5Wen-Chien Ko6Jiun-Ling Wang7Institute of Molecular Medicine, College of Medicine, National Cheng Kung University, Tainan 704, TaiwanDepartment of Physical Examination Center, Kaohsiung Veterans General Hospital, Kaohsiung 813, TaiwanBiodiversity Research Center, Academia Sinica, Taipei 115, TaiwanInstitute of Molecular Medicine, College of Medicine, National Cheng Kung University, Tainan 704, TaiwanDepartment of Pediatrics, Kaohsiung Veterans General Hospital, Kaohsiung 813, TaiwanDepartment of Cosmetics and Fashion Styling, Cheng-Shiu University, Kaohsiung 833, TaiwanDepartment of Internal Medicine, National Cheng Kung University Hospital, Tainan 704, TaiwanDepartment of Internal Medicine, National Cheng Kung University Hospital, Tainan 704, TaiwanBackground: Colistin is one of the last-line antimicrobial agents against life-threatening infections. The distribution of the colistin resistance gene <i>mcr-1</i> has been reported worldwide. However, most studies have focused on the distribution of <i>mcr-1</i>-positive bacteria in humans, animals, food, and sewage; few have focused on their distribution in natural environments. Method: We conducted a large spatial survey of <i>mcr-1</i>-positive <i>Escherichia coli</i> at 119 sites in 48 rivers, covering the entire island of Taiwan. We investigated the relationship between the livestock or poultry density in the surveyed riverine area and the number of <i>mcr-1</i>-positive <i>E. coli</i> in the river water. We then sequenced and characterized the isolated <i>mcr-1</i>-positive plasmids. Results: Seven <i>mcr-1</i> positive <i>E. coli</i> were isolated from 5.9% of the sampling sites. The <i>mcr-1</i>-positive sites correlated with high chicken and pig stocking densities but not human population density or other river parameters. Four of the <i>mcr-1</i>-positive <i>E. coli</i> strains harbored epidemic IncX4 plasmids, and three of them exhibited identical sequences with a size of 33,309 bp. One of the plasmids contained identical 33,309 bp sequences but carried an additional 5711-bp transposon (Tn3 family). To our knowledge, this is the first demonstration that <i>mcr-1</i>-carrying IncX4 plasmids can contain an insertion of such transposons. All <i>mcr-1</i>-positive isolates belonged to phylogenetic group A and harbored few known virulence genes. Conclusion: This study showed a positive relationship between the number of <i>mcr-1</i>-positive sites and high livestock and poultry density. The sequencing analyses indicated that the epidemic plasmid in the <i>mcr-1</i> isolates circulates not only in humans, animals, and food but also in the associated environments or natural habitats in Taiwan, suggesting that the surveillance of antibiotics-resistance genes for livestock or poultry farm quality control should include their associated environments.https://www.mdpi.com/2076-2607/9/4/722riverplasmid<i>mcr-1</i>chickenpigstransconjugants
spellingShingle Ching-Hao Teng
Pin-Chieh Wu
Sen-Lin Tang
Yi-Chen Chen
Ming-Fang Cheng
Ping-Chih Huang
Wen-Chien Ko
Jiun-Ling Wang
A Large Spatial Survey of Colistin-Resistant Gene <i>mcr-1</i>-Carrying <i>E. coli</i> in Rivers across Taiwan
Microorganisms
river
plasmid
<i>mcr-1</i>
chicken
pigs
transconjugants
title A Large Spatial Survey of Colistin-Resistant Gene <i>mcr-1</i>-Carrying <i>E. coli</i> in Rivers across Taiwan
title_full A Large Spatial Survey of Colistin-Resistant Gene <i>mcr-1</i>-Carrying <i>E. coli</i> in Rivers across Taiwan
title_fullStr A Large Spatial Survey of Colistin-Resistant Gene <i>mcr-1</i>-Carrying <i>E. coli</i> in Rivers across Taiwan
title_full_unstemmed A Large Spatial Survey of Colistin-Resistant Gene <i>mcr-1</i>-Carrying <i>E. coli</i> in Rivers across Taiwan
title_short A Large Spatial Survey of Colistin-Resistant Gene <i>mcr-1</i>-Carrying <i>E. coli</i> in Rivers across Taiwan
title_sort large spatial survey of colistin resistant gene i mcr 1 i carrying i e coli i in rivers across taiwan
topic river
plasmid
<i>mcr-1</i>
chicken
pigs
transconjugants
url https://www.mdpi.com/2076-2607/9/4/722
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