Deciphering the Structural Diversity and Classification of the Mobile Tigecycline Resistance Gene <italic toggle="yes">tet</italic>(X)-Bearing Plasmidome among Bacteria

ABSTRACT The emergence of novel plasmid-mediated resistance genes constitutes a great public concern. Recently, mobile tet(X) variants were reported in diverse pathogens from different sources. However, the diversity of tet(X)-bearing plasmids remains largely unknown. In this study, the phenotypes a...

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Autores principales:	Ruichao Li, Xiaoyu Lu, Kai Peng, Ziyi Liu, Yan Li, Yuan Liu, Xia Xiao, Zhiqiang Wang
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	tigecycline resistance tet(X) variants tandem repeats resistance plasmidome Nanopore sequencing Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e1dd5837b4e641a1b79216356acd8d58
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spelling	oai:doaj.org-article:e1dd5837b4e641a1b79216356acd8d582021-12-02T19:46:20ZDeciphering the Structural Diversity and Classification of the Mobile Tigecycline Resistance Gene <italic toggle="yes">tet</italic>(X)-Bearing Plasmidome among Bacteria10.1128/mSystems.00134-202379-5077https://doaj.org/article/e1dd5837b4e641a1b79216356acd8d582020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00134-20https://doaj.org/toc/2379-5077ABSTRACT The emergence of novel plasmid-mediated resistance genes constitutes a great public concern. Recently, mobile tet(X) variants were reported in diverse pathogens from different sources. However, the diversity of tet(X)-bearing plasmids remains largely unknown. In this study, the phenotypes and genotypes of all the tet(X)-positive tigecycline-resistant strains isolated from a slaughterhouse in China were characterized by antimicrobial susceptibility testing, conjugation, pulsed-field gel electrophoresis with S1 nuclease (S1-PFGE), and PCR. The diversity and polymorphism of tet(X)-harboring strains and plasmidomes were investigated by whole-genome sequencing (WGS) and single-plasmid-molecule analysis. Seventy-four tet(X4)-harboring Escherichia coli strains and one tet(X6)-bearing Providencia rettgeri strain were identified. The tet(X4)-bearing elements in 27 strains could be transferred to the recipient strain via plasmids. All tet(X4)-bearing plasmids isolated in this study and 15 tet(X4)-bearing plasmids reported online were analyzed. tet(X4)-bearing plasmids ranged from 9 to 294 kb and were categorized as ColE2-like, IncQ, IncX1, IncA/C2, IncFII, IncFIB, and hybrid plasmids with different replicons. The core tet(X4)-bearing genetic contexts were divided into four major groups: ISCR2-tet(X4)-abh, △ISCR2-abh-tet(X4)-ISCR2, ISCR2-abh-tet(X4)-ISCR2-virD2-floR, and abh-tet(X4)-ISCR2-yheS-cat-zitR-ISCR2-virD2-floR. Tandem repeats of tet(X4) were universally mediated by ISCR2. Different tet(X)-bearing strains existed in the same microbiota. Reorganization of tet(X4)-bearing multidrug resistance plasmids was found to be mediated by IS26 and other homologous regions. Finally, single-plasmid-molecule analysis captured the heterogenous state of tet(X4)-bearing plasmids. These findings significantly expand our knowledge of the tet(X)-bearing plasmidome among microbiotas, which establishes a baseline for investigating the structure and diversity of human, animal, and environmental tigecycline resistomes. Characterization of tet(X) genes among different microbiotas should be performed systematically to understand the evolution and ecology. IMPORTANCE Tigecycline is an expanded-spectrum tetracycline used as a last-resort antimicrobial for treating infections caused by superbugs such as carbapenemase-producing or colistin-resistant pathogens. Emergence of the plasmid-mediated mobile tigecycline resistance gene tet(X4) created a great public health concern. However, the diversity of tet(X4)-bearing plasmids and bacteria remains largely uninvestigated. To cover this knowledge gap, we comprehensively identified and characterized the tet(X)-bearing plasmidome in different sources using advanced sequencing technologies for the first time. The huge diversity of tet(X4)-bearing mobile elements demonstrates the high level of transmissibility of the tet(X4) gene among bacteria. It is crucial to enhance stringent surveillance of tet(X) genes in animal and human pathogens globally.Ruichao LiXiaoyu LuKai PengZiyi LiuYan LiYuan LiuXia XiaoZhiqiang WangAmerican Society for Microbiologyarticletigecycline resistancetet(X) variantstandem repeatsresistance plasmidomeNanopore sequencingMicrobiologyQR1-502ENmSystems, Vol 5, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	tigecycline resistance tet(X) variants tandem repeats resistance plasmidome Nanopore sequencing Microbiology QR1-502
spellingShingle	tigecycline resistance tet(X) variants tandem repeats resistance plasmidome Nanopore sequencing Microbiology QR1-502 Ruichao Li Xiaoyu Lu Kai Peng Ziyi Liu Yan Li Yuan Liu Xia Xiao Zhiqiang Wang Deciphering the Structural Diversity and Classification of the Mobile Tigecycline Resistance Gene <italic toggle="yes">tet</italic>(X)-Bearing Plasmidome among Bacteria
description	ABSTRACT The emergence of novel plasmid-mediated resistance genes constitutes a great public concern. Recently, mobile tet(X) variants were reported in diverse pathogens from different sources. However, the diversity of tet(X)-bearing plasmids remains largely unknown. In this study, the phenotypes and genotypes of all the tet(X)-positive tigecycline-resistant strains isolated from a slaughterhouse in China were characterized by antimicrobial susceptibility testing, conjugation, pulsed-field gel electrophoresis with S1 nuclease (S1-PFGE), and PCR. The diversity and polymorphism of tet(X)-harboring strains and plasmidomes were investigated by whole-genome sequencing (WGS) and single-plasmid-molecule analysis. Seventy-four tet(X4)-harboring Escherichia coli strains and one tet(X6)-bearing Providencia rettgeri strain were identified. The tet(X4)-bearing elements in 27 strains could be transferred to the recipient strain via plasmids. All tet(X4)-bearing plasmids isolated in this study and 15 tet(X4)-bearing plasmids reported online were analyzed. tet(X4)-bearing plasmids ranged from 9 to 294 kb and were categorized as ColE2-like, IncQ, IncX1, IncA/C2, IncFII, IncFIB, and hybrid plasmids with different replicons. The core tet(X4)-bearing genetic contexts were divided into four major groups: ISCR2-tet(X4)-abh, △ISCR2-abh-tet(X4)-ISCR2, ISCR2-abh-tet(X4)-ISCR2-virD2-floR, and abh-tet(X4)-ISCR2-yheS-cat-zitR-ISCR2-virD2-floR. Tandem repeats of tet(X4) were universally mediated by ISCR2. Different tet(X)-bearing strains existed in the same microbiota. Reorganization of tet(X4)-bearing multidrug resistance plasmids was found to be mediated by IS26 and other homologous regions. Finally, single-plasmid-molecule analysis captured the heterogenous state of tet(X4)-bearing plasmids. These findings significantly expand our knowledge of the tet(X)-bearing plasmidome among microbiotas, which establishes a baseline for investigating the structure and diversity of human, animal, and environmental tigecycline resistomes. Characterization of tet(X) genes among different microbiotas should be performed systematically to understand the evolution and ecology. IMPORTANCE Tigecycline is an expanded-spectrum tetracycline used as a last-resort antimicrobial for treating infections caused by superbugs such as carbapenemase-producing or colistin-resistant pathogens. Emergence of the plasmid-mediated mobile tigecycline resistance gene tet(X4) created a great public health concern. However, the diversity of tet(X4)-bearing plasmids and bacteria remains largely uninvestigated. To cover this knowledge gap, we comprehensively identified and characterized the tet(X)-bearing plasmidome in different sources using advanced sequencing technologies for the first time. The huge diversity of tet(X4)-bearing mobile elements demonstrates the high level of transmissibility of the tet(X4) gene among bacteria. It is crucial to enhance stringent surveillance of tet(X) genes in animal and human pathogens globally.
format	article
author	Ruichao Li Xiaoyu Lu Kai Peng Ziyi Liu Yan Li Yuan Liu Xia Xiao Zhiqiang Wang
author_facet	Ruichao Li Xiaoyu Lu Kai Peng Ziyi Liu Yan Li Yuan Liu Xia Xiao Zhiqiang Wang
author_sort	Ruichao Li
title	Deciphering the Structural Diversity and Classification of the Mobile Tigecycline Resistance Gene <italic toggle="yes">tet</italic>(X)-Bearing Plasmidome among Bacteria
title_short	Deciphering the Structural Diversity and Classification of the Mobile Tigecycline Resistance Gene <italic toggle="yes">tet</italic>(X)-Bearing Plasmidome among Bacteria
title_full	Deciphering the Structural Diversity and Classification of the Mobile Tigecycline Resistance Gene <italic toggle="yes">tet</italic>(X)-Bearing Plasmidome among Bacteria
title_fullStr	Deciphering the Structural Diversity and Classification of the Mobile Tigecycline Resistance Gene <italic toggle="yes">tet</italic>(X)-Bearing Plasmidome among Bacteria
title_full_unstemmed	Deciphering the Structural Diversity and Classification of the Mobile Tigecycline Resistance Gene <italic toggle="yes">tet</italic>(X)-Bearing Plasmidome among Bacteria
title_sort	deciphering the structural diversity and classification of the mobile tigecycline resistance gene <italic toggle="yes">tet</italic>(x)-bearing plasmidome among bacteria
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/e1dd5837b4e641a1b79216356acd8d58
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Deciphering the Structural Diversity and Classification of the Mobile Tigecycline Resistance Gene <italic toggle="yes">tet</italic>(X)-Bearing Plasmidome among Bacteria

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