Novel IS26-mediated hybrid plasmid harbouring tet(X4) in Escherichia coli

Pengcheng Du; Dejun Liu; Huangwei Song; Pei Zhang; Ruichao Li; Yulin Fu; Xiao Liu; Jinli Jia; Xiaodi Li; Séamus Fanning; Yang Wang; Li Bai; Hui Zeng

doi:10.1016/j.jgar.2020.03.018

Novel IS26-mediated hybrid plasmid harbouring tet(X4) in Escherichia coli

Pengcheng Du, Dejun Liu, Huangwei Song, Pei Zhang, Ruichao Li, Yulin Fu, Xiao Liu, Jinli Jia, Xiaodi Li, Séamus Fanning, Yang Wang, Li Bai^*, Hui Zeng

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

35 Citations (Scopus)

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Abstract

Objectives: As the spread of antimicrobial resistance genes becomes an increasing global threat, improved understanding of genetic structure and transferability of the resistant plasmids becomes more critical. The newly description of several plasmid-mediated tet(X) variant genes, tet(X3), tet(X4) and tet(X5), poses a considerable risk for public health. This study aimed to investigate the recombination event that occurred during the conjugation process of a tet(X4)-bearing plasmid.

Methods: A Tet(X4)-producing Escherichia coli isolate, 2019XSD11, was subjected to susceptibility testing, S1-PFGE and whole genome sequencing. The genetic features of plasmids and the recombination event were analyzed by sequence comparison and annotation. We performed electrotransformation assay to further test the transferability of the tet(X4)-bearing plasmid. Results: A novel type of fusion tet(X4)-bearing plasmid was discovered from the transconjugant, plasmid p2019XSD11-TC2-284 (∼280 kbp). The sequence of this plasmid consisted of a hybrid episome of two plasmids p2019XSD11-190 (∼190 kbp) harbouring tet(X4) and p2019XSD11-92 (∼92 kbp) harbouring bla_CTX-M-55 originated from 2019XSD11. The two plasmids were concatenated by IS26 elements. Analyses of the genetic constitution of the plasmids essential for transmission showed the plasmid p2019XSD11-190 lacked an intact type IV secretion system. Beyond this, the origin of transfer region and relaxase genes in plasmid p2019XSD11-190 had no sequence similarity with those in plasmid p2019XSD11-92.

Conclusions: The fusion of the two plasmids probably formed through IS26 homologous recombination. Such recombination events presumably play an important role in the dissemination of the tet(X4). Molecular surveillance of tet(X) variant genes and genetic structures warrants further investigation to evaluate the underlying public health risk.

Original language	English
Pages (from-to)	162-168
Number of pages	7
Journal	Journal of Global Antimicrobial Resistance
Volume	21
Early online date	12 May 2020
DOIs	https://doi.org/10.1016/j.jgar.2020.03.018
Publication status	Published - Jun 2020
Externally published	Yes

Bibliographical note

Funding Information:
This work was supported by the National Natural Science Foundation of China (grant numbers: 31871899 , 31930110 and 81702038 ) and Beijing Hospitals Authority Youth Programme (code: QML20181802 ).

Publisher Copyright:
© 2020 The Author(s)

Keywords

Co-integration plasmid
Intramolecular restructuring
tet(X4) gene
Tigecycline resistance

ASJC Scopus subject areas

Microbiology
Immunology and Allergy
Immunology
Microbiology (medical)

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.jgar.2020.03.018Licence: CC BY-NC-ND

Novel IS26-mediated hybrid plasmid harbouring tet(X4) in Escherichia coli
Copyright 2020 the authors. Published by Elsevier Ltd on behalf of International Society for Antimicrobial Chemotherapy. This is an open access article published under a Creative Commons Attribution-NonCommercial-NoDerivs License (https://creativecommons.org/licenses/by-nc-nd/4.0/), which permits distribution and reproduction for non-commercial purposes, provided the author and source are cited.
Final published version, 1.58 MBLicence: CC BY-NC-ND

Cite this

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title = "Novel IS26-mediated hybrid plasmid harbouring tet(X4) in Escherichia coli",

abstract = "Objectives: As the spread of antimicrobial resistance genes becomes an increasing global threat, improved understanding of genetic structure and transferability of the resistant plasmids becomes more critical. The newly description of several plasmid-mediated tet(X) variant genes, tet(X3), tet(X4) and tet(X5), poses a considerable risk for public health. This study aimed to investigate the recombination event that occurred during the conjugation process of a tet(X4)-bearing plasmid. Methods: A Tet(X4)-producing Escherichia coli isolate, 2019XSD11, was subjected to susceptibility testing, S1-PFGE and whole genome sequencing. The genetic features of plasmids and the recombination event were analyzed by sequence comparison and annotation. We performed electrotransformation assay to further test the transferability of the tet(X4)-bearing plasmid. Results: A novel type of fusion tet(X4)-bearing plasmid was discovered from the transconjugant, plasmid p2019XSD11-TC2-284 (∼280 kbp). The sequence of this plasmid consisted of a hybrid episome of two plasmids p2019XSD11-190 (∼190 kbp) harbouring tet(X4) and p2019XSD11-92 (∼92 kbp) harbouring blaCTX-M-55 originated from 2019XSD11. The two plasmids were concatenated by IS26 elements. Analyses of the genetic constitution of the plasmids essential for transmission showed the plasmid p2019XSD11-190 lacked an intact type IV secretion system. Beyond this, the origin of transfer region and relaxase genes in plasmid p2019XSD11-190 had no sequence similarity with those in plasmid p2019XSD11-92. Conclusions: The fusion of the two plasmids probably formed through IS26 homologous recombination. Such recombination events presumably play an important role in the dissemination of the tet(X4). Molecular surveillance of tet(X) variant genes and genetic structures warrants further investigation to evaluate the underlying public health risk.",

keywords = "Co-integration plasmid, Intramolecular restructuring, tet(X4) gene, Tigecycline resistance",

author = "Pengcheng Du and Dejun Liu and Huangwei Song and Pei Zhang and Ruichao Li and Yulin Fu and Xiao Liu and Jinli Jia and Xiaodi Li and S{\'e}amus Fanning and Yang Wang and Li Bai and Hui Zeng",

note = "Funding Information: This work was supported by the National Natural Science Foundation of China (grant numbers: 31871899 , 31930110 and 81702038 ) and Beijing Hospitals Authority Youth Programme (code: QML20181802 ). Publisher Copyright: {\textcopyright} 2020 The Author(s)",

year = "2020",

month = jun,

doi = "10.1016/j.jgar.2020.03.018",

language = "English",

volume = "21",

pages = "162--168",

journal = "Journal of Global Antimicrobial Resistance",

issn = "2213-7165",

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TY - JOUR

T1 - Novel IS26-mediated hybrid plasmid harbouring tet(X4) in Escherichia coli

AU - Du, Pengcheng

AU - Liu, Dejun

AU - Song, Huangwei

AU - Zhang, Pei

AU - Li, Ruichao

AU - Fu, Yulin

AU - Liu, Xiao

AU - Jia, Jinli

AU - Li, Xiaodi

AU - Fanning, Séamus

AU - Wang, Yang

AU - Bai, Li

AU - Zeng, Hui

N1 - Funding Information: This work was supported by the National Natural Science Foundation of China (grant numbers: 31871899 , 31930110 and 81702038 ) and Beijing Hospitals Authority Youth Programme (code: QML20181802 ). Publisher Copyright: © 2020 The Author(s)

PY - 2020/6

Y1 - 2020/6

N2 - Objectives: As the spread of antimicrobial resistance genes becomes an increasing global threat, improved understanding of genetic structure and transferability of the resistant plasmids becomes more critical. The newly description of several plasmid-mediated tet(X) variant genes, tet(X3), tet(X4) and tet(X5), poses a considerable risk for public health. This study aimed to investigate the recombination event that occurred during the conjugation process of a tet(X4)-bearing plasmid. Methods: A Tet(X4)-producing Escherichia coli isolate, 2019XSD11, was subjected to susceptibility testing, S1-PFGE and whole genome sequencing. The genetic features of plasmids and the recombination event were analyzed by sequence comparison and annotation. We performed electrotransformation assay to further test the transferability of the tet(X4)-bearing plasmid. Results: A novel type of fusion tet(X4)-bearing plasmid was discovered from the transconjugant, plasmid p2019XSD11-TC2-284 (∼280 kbp). The sequence of this plasmid consisted of a hybrid episome of two plasmids p2019XSD11-190 (∼190 kbp) harbouring tet(X4) and p2019XSD11-92 (∼92 kbp) harbouring blaCTX-M-55 originated from 2019XSD11. The two plasmids were concatenated by IS26 elements. Analyses of the genetic constitution of the plasmids essential for transmission showed the plasmid p2019XSD11-190 lacked an intact type IV secretion system. Beyond this, the origin of transfer region and relaxase genes in plasmid p2019XSD11-190 had no sequence similarity with those in plasmid p2019XSD11-92. Conclusions: The fusion of the two plasmids probably formed through IS26 homologous recombination. Such recombination events presumably play an important role in the dissemination of the tet(X4). Molecular surveillance of tet(X) variant genes and genetic structures warrants further investigation to evaluate the underlying public health risk.

AB - Objectives: As the spread of antimicrobial resistance genes becomes an increasing global threat, improved understanding of genetic structure and transferability of the resistant plasmids becomes more critical. The newly description of several plasmid-mediated tet(X) variant genes, tet(X3), tet(X4) and tet(X5), poses a considerable risk for public health. This study aimed to investigate the recombination event that occurred during the conjugation process of a tet(X4)-bearing plasmid. Methods: A Tet(X4)-producing Escherichia coli isolate, 2019XSD11, was subjected to susceptibility testing, S1-PFGE and whole genome sequencing. The genetic features of plasmids and the recombination event were analyzed by sequence comparison and annotation. We performed electrotransformation assay to further test the transferability of the tet(X4)-bearing plasmid. Results: A novel type of fusion tet(X4)-bearing plasmid was discovered from the transconjugant, plasmid p2019XSD11-TC2-284 (∼280 kbp). The sequence of this plasmid consisted of a hybrid episome of two plasmids p2019XSD11-190 (∼190 kbp) harbouring tet(X4) and p2019XSD11-92 (∼92 kbp) harbouring blaCTX-M-55 originated from 2019XSD11. The two plasmids were concatenated by IS26 elements. Analyses of the genetic constitution of the plasmids essential for transmission showed the plasmid p2019XSD11-190 lacked an intact type IV secretion system. Beyond this, the origin of transfer region and relaxase genes in plasmid p2019XSD11-190 had no sequence similarity with those in plasmid p2019XSD11-92. Conclusions: The fusion of the two plasmids probably formed through IS26 homologous recombination. Such recombination events presumably play an important role in the dissemination of the tet(X4). Molecular surveillance of tet(X) variant genes and genetic structures warrants further investigation to evaluate the underlying public health risk.

KW - Co-integration plasmid

KW - Intramolecular restructuring

KW - tet(X4) gene

KW - Tigecycline resistance

U2 - 10.1016/j.jgar.2020.03.018

DO - 10.1016/j.jgar.2020.03.018

M3 - Article

C2 - 32247809

AN - SCOPUS:85084370473

SN - 2213-7165

VL - 21

SP - 162

EP - 168

JO - Journal of Global Antimicrobial Resistance

JF - Journal of Global Antimicrobial Resistance

ER -

Novel IS26-mediated hybrid plasmid harbouring tet(X4) in Escherichia coli

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

UN SDGs

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