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High Prevalence of Colistin-Resistant Escherichia coli with Chromosomally Carried mcr-1 in Healthy Residents in Vietnam

The wide distribution of colistin-resistant bacteria in developing countries has become a common phenomenon. To understand the mechanisms underlying their distribution, we studied the mcr genetic background of colistin-resistant Escherichia coli isolates from the fecal microbiota of healthy human re...

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Autores principales: Yamaguchi, Takahiro, Kawahara, Ryuji, Hamamoto, Kouta, Hirai, Itaru, Khong, Diep Thi, Nguyen, Thang Nam, Tran, Hoa Thi, Motooka, Daisuke, Nakamura, Shota, Yamamoto, Yoshimasa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7056805/
https://www.ncbi.nlm.nih.gov/pubmed/32132160
http://dx.doi.org/10.1128/mSphere.00117-20
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author Yamaguchi, Takahiro
Kawahara, Ryuji
Hamamoto, Kouta
Hirai, Itaru
Khong, Diep Thi
Nguyen, Thang Nam
Tran, Hoa Thi
Motooka, Daisuke
Nakamura, Shota
Yamamoto, Yoshimasa
author_facet Yamaguchi, Takahiro
Kawahara, Ryuji
Hamamoto, Kouta
Hirai, Itaru
Khong, Diep Thi
Nguyen, Thang Nam
Tran, Hoa Thi
Motooka, Daisuke
Nakamura, Shota
Yamamoto, Yoshimasa
author_sort Yamaguchi, Takahiro
collection PubMed
description The wide distribution of colistin-resistant bacteria in developing countries has become a common phenomenon. To understand the mechanisms underlying their distribution, we studied the mcr genetic background of colistin-resistant Escherichia coli isolates from the fecal microbiota of healthy human residents from a community in Vietnam with a high prevalence of colistin-resistant E. coli with mcr. Fifty-seven colistin-resistant isolates were obtained from 98 residents; one isolate was collected from each individual and analyzed for mcr. We found that 36.8% of the isolates carried chromosomal mcr-1. Further, 63.2% and 1.8% of the isolates carried mcr-1 on the plasmid and the plasmid/chromosome, respectively. Whole-genome sequencing of genetically unrelated isolates showed that the majority (6 of 7) of the isolates had the chromosomal mcr-1 in a complete ancestral mcr-1 transposon Tn6330, ISApl1-mcr-1-PAP2-ISApl1, which was inserted at various positions on the chromosomes. In addition, the majority (87.5%) of Tn6330 of mcr-1-carrying plasmids (n = 8) lacked both upstream and downstream ISApl1 transposons. The results obtained in this study indicate that plasmid-to-chromosomal transfer of mcr-1 may have occurred recently in the fecal microbiota of the residents. Additionally, Tn6330 on the chromosome may lose ISApl1 from the transposon during multiplication to gain a more stable mcr-1 state on the chromosome. Stabilization of resistance by the chromosomal incorporation of mcr-1 would be an additional challenge in combating the dissemination of resistant bacteria. IMPORTANCE Elucidation of the mechanism of the wide dissemination of colistin-resistant bacteria in communities of developing countries is an urgent public health issue. In this study, we investigated the genetic background of the colistin resistance gene mcr in E. coli isolates from the fecal microbiota of healthy human residents living in a community in Vietnam with a high prevalence of colistin-resistant E. coli. Our study revealed for the first time, a surprisingly high percentage (36.8%) of colistin-resistant E. coli carrying chromosomal mcr-1, the emergence of which may have occurred recently, in the fecal microbiota of the community residents. The mcr-1 transposon on the chromosome may develop into a more stable genotype by the loss of insertion sequences (ISs). Our results are valuable in understanding the mechanism underlying the increasing prevalence of colistin-resistant bacteria within a community.
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spelling pubmed-70568052020-03-06 High Prevalence of Colistin-Resistant Escherichia coli with Chromosomally Carried mcr-1 in Healthy Residents in Vietnam Yamaguchi, Takahiro Kawahara, Ryuji Hamamoto, Kouta Hirai, Itaru Khong, Diep Thi Nguyen, Thang Nam Tran, Hoa Thi Motooka, Daisuke Nakamura, Shota Yamamoto, Yoshimasa mSphere Research Article The wide distribution of colistin-resistant bacteria in developing countries has become a common phenomenon. To understand the mechanisms underlying their distribution, we studied the mcr genetic background of colistin-resistant Escherichia coli isolates from the fecal microbiota of healthy human residents from a community in Vietnam with a high prevalence of colistin-resistant E. coli with mcr. Fifty-seven colistin-resistant isolates were obtained from 98 residents; one isolate was collected from each individual and analyzed for mcr. We found that 36.8% of the isolates carried chromosomal mcr-1. Further, 63.2% and 1.8% of the isolates carried mcr-1 on the plasmid and the plasmid/chromosome, respectively. Whole-genome sequencing of genetically unrelated isolates showed that the majority (6 of 7) of the isolates had the chromosomal mcr-1 in a complete ancestral mcr-1 transposon Tn6330, ISApl1-mcr-1-PAP2-ISApl1, which was inserted at various positions on the chromosomes. In addition, the majority (87.5%) of Tn6330 of mcr-1-carrying plasmids (n = 8) lacked both upstream and downstream ISApl1 transposons. The results obtained in this study indicate that plasmid-to-chromosomal transfer of mcr-1 may have occurred recently in the fecal microbiota of the residents. Additionally, Tn6330 on the chromosome may lose ISApl1 from the transposon during multiplication to gain a more stable mcr-1 state on the chromosome. Stabilization of resistance by the chromosomal incorporation of mcr-1 would be an additional challenge in combating the dissemination of resistant bacteria. IMPORTANCE Elucidation of the mechanism of the wide dissemination of colistin-resistant bacteria in communities of developing countries is an urgent public health issue. In this study, we investigated the genetic background of the colistin resistance gene mcr in E. coli isolates from the fecal microbiota of healthy human residents living in a community in Vietnam with a high prevalence of colistin-resistant E. coli. Our study revealed for the first time, a surprisingly high percentage (36.8%) of colistin-resistant E. coli carrying chromosomal mcr-1, the emergence of which may have occurred recently, in the fecal microbiota of the community residents. The mcr-1 transposon on the chromosome may develop into a more stable genotype by the loss of insertion sequences (ISs). Our results are valuable in understanding the mechanism underlying the increasing prevalence of colistin-resistant bacteria within a community. American Society for Microbiology 2020-03-04 /pmc/articles/PMC7056805/ /pubmed/32132160 http://dx.doi.org/10.1128/mSphere.00117-20 Text en Copyright © 2020 Yamaguchi et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Yamaguchi, Takahiro
Kawahara, Ryuji
Hamamoto, Kouta
Hirai, Itaru
Khong, Diep Thi
Nguyen, Thang Nam
Tran, Hoa Thi
Motooka, Daisuke
Nakamura, Shota
Yamamoto, Yoshimasa
High Prevalence of Colistin-Resistant Escherichia coli with Chromosomally Carried mcr-1 in Healthy Residents in Vietnam
title High Prevalence of Colistin-Resistant Escherichia coli with Chromosomally Carried mcr-1 in Healthy Residents in Vietnam
title_full High Prevalence of Colistin-Resistant Escherichia coli with Chromosomally Carried mcr-1 in Healthy Residents in Vietnam
title_fullStr High Prevalence of Colistin-Resistant Escherichia coli with Chromosomally Carried mcr-1 in Healthy Residents in Vietnam
title_full_unstemmed High Prevalence of Colistin-Resistant Escherichia coli with Chromosomally Carried mcr-1 in Healthy Residents in Vietnam
title_short High Prevalence of Colistin-Resistant Escherichia coli with Chromosomally Carried mcr-1 in Healthy Residents in Vietnam
title_sort high prevalence of colistin-resistant escherichia coli with chromosomally carried mcr-1 in healthy residents in vietnam
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7056805/
https://www.ncbi.nlm.nih.gov/pubmed/32132160
http://dx.doi.org/10.1128/mSphere.00117-20
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