Identification of novel tetracycline resistance gene tet(X14) and its co-occurrence with tet(X2) in a tigecycline-resistant and colistin-resistant Empedobacter stercoris

Tigecycline is one of the last-resort antibiotics to treat severe infections. Recently, tigecycline resistance has sporadically emerged with an increasing trend, and Tet(X) family represents a new resistance mechanism of tigecycline. In this study, a novel chromosome-encoded tigecycline resistance g...

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Main Authors: Yingying Cheng, Yong Chen, Yang Liu, Yuqi Guo, Yanzi Zhou, Tingting Xiao, Shuntian Zhang, Hao Xu, Yunbo Chen, Tongling Shan, Yonghong Xiao, Kai Zhou
Format: Article
Language:English
Published: Taylor & Francis Group 2020-01-01
Series:Emerging Microbes and Infections
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Online Access:https://www.tandfonline.com/doi/10.1080/22221751.2020.1803769
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author Yingying Cheng
Yong Chen
Yang Liu
Yuqi Guo
Yanzi Zhou
Tingting Xiao
Shuntian Zhang
Hao Xu
Yunbo Chen
Tongling Shan
Yonghong Xiao
Kai Zhou
author_facet Yingying Cheng
Yong Chen
Yang Liu
Yuqi Guo
Yanzi Zhou
Tingting Xiao
Shuntian Zhang
Hao Xu
Yunbo Chen
Tongling Shan
Yonghong Xiao
Kai Zhou
author_sort Yingying Cheng
collection DOAJ
description Tigecycline is one of the last-resort antibiotics to treat severe infections. Recently, tigecycline resistance has sporadically emerged with an increasing trend, and Tet(X) family represents a new resistance mechanism of tigecycline. In this study, a novel chromosome-encoded tigecycline resistance gene, tet(X14), was identified in a tigecycline-resistant and colistin-resistant Empedobacter stercoris strain ES183 recovered from a pig fecal sample in China. Tet(X14) shows 67.14-96.39% sequence identity to the other variants [Tet(X) to Tet(X13)]. Overexpression of Tet(X14) in Escherichia coli confers 16-fold increase in tigecycline MIC (from 0.125 to 2 mg/L), which is lower than that of Tet(X3), Tet(X4) and Tet(X6). Structural modelling predicted that Tet(X14) shared a high homology with the other 12 variants with RMSD value from 0.003 to 0.055, and Tet(X14) can interact with tetracyclines by a similar pattern as the other Tet(X)s. tet(X14) and two copies of tet(X2) were identified on a genome island with abnormal GC content carried by the chromosome of ES183, and no mobile genetic elements were found surrounding, suggesting that tet(X14) might be heterologously obtained by ES183 via recombination. Blasting in Genbank revealed that Tet(X14) was exclusively detected on the chromosome of Riemerella anatipestifer, mainly encoded on antimicrobial resistance islands. E. stercoris and R. anatipestifer belong to the family Flavobacteriaceae, suggesting that the members of Flavobacteriaceae maybe the major reservoir of tet(X14). Our study reports a novel chromosome-encoded tigecycline resistance gene tet(X14). The expanded members of Tet(X) family warrants the potential large-scale dissemination and the necessity of continuous surveillance for tet(X)-mediated tigecycline resistance.
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spelling doaj-art-3de62847bc8c454a8efc8895552c2ce92025-08-20T02:15:52ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512020-01-01911843185210.1080/22221751.2020.1803769Identification of novel tetracycline resistance gene tet(X14) and its co-occurrence with tet(X2) in a tigecycline-resistant and colistin-resistant Empedobacter stercorisYingying Cheng0Yong Chen1Yang Liu2Yuqi Guo3Yanzi Zhou4Tingting Xiao5Shuntian Zhang6Hao Xu7Yunbo Chen8Tongling Shan9Yonghong Xiao10Kai Zhou11Shenzhen Institute of Respiratory Diseases, Second Clinical Medical College (Shenzhen People’s Hospital), Jinan University, Shenzhen, People’s Republic of ChinaShenzhen Institute of Respiratory Diseases, Second Clinical Medical College (Shenzhen People’s Hospital), Jinan University, Shenzhen, People’s Republic of ChinaShenzhen Institute of Respiratory Diseases, Second Clinical Medical College (Shenzhen People’s Hospital), Jinan University, Shenzhen, People’s Republic of ChinaShenzhen Institute of Respiratory Diseases, Second Clinical Medical College (Shenzhen People’s Hospital), Jinan University, Shenzhen, People’s Republic of ChinaCollaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, People’s Republic of ChinaCollaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, People’s Republic of ChinaCollaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, People’s Republic of ChinaCollaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, People’s Republic of ChinaCollaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, People’s Republic of ChinaShanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai, People’s Republic of ChinaCollaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, People’s Republic of ChinaShenzhen Institute of Respiratory Diseases, Second Clinical Medical College (Shenzhen People’s Hospital), Jinan University, Shenzhen, People’s Republic of ChinaTigecycline is one of the last-resort antibiotics to treat severe infections. Recently, tigecycline resistance has sporadically emerged with an increasing trend, and Tet(X) family represents a new resistance mechanism of tigecycline. In this study, a novel chromosome-encoded tigecycline resistance gene, tet(X14), was identified in a tigecycline-resistant and colistin-resistant Empedobacter stercoris strain ES183 recovered from a pig fecal sample in China. Tet(X14) shows 67.14-96.39% sequence identity to the other variants [Tet(X) to Tet(X13)]. Overexpression of Tet(X14) in Escherichia coli confers 16-fold increase in tigecycline MIC (from 0.125 to 2 mg/L), which is lower than that of Tet(X3), Tet(X4) and Tet(X6). Structural modelling predicted that Tet(X14) shared a high homology with the other 12 variants with RMSD value from 0.003 to 0.055, and Tet(X14) can interact with tetracyclines by a similar pattern as the other Tet(X)s. tet(X14) and two copies of tet(X2) were identified on a genome island with abnormal GC content carried by the chromosome of ES183, and no mobile genetic elements were found surrounding, suggesting that tet(X14) might be heterologously obtained by ES183 via recombination. Blasting in Genbank revealed that Tet(X14) was exclusively detected on the chromosome of Riemerella anatipestifer, mainly encoded on antimicrobial resistance islands. E. stercoris and R. anatipestifer belong to the family Flavobacteriaceae, suggesting that the members of Flavobacteriaceae maybe the major reservoir of tet(X14). Our study reports a novel chromosome-encoded tigecycline resistance gene tet(X14). The expanded members of Tet(X) family warrants the potential large-scale dissemination and the necessity of continuous surveillance for tet(X)-mediated tigecycline resistance.https://www.tandfonline.com/doi/10.1080/22221751.2020.1803769Tigecycline resistancetetracycline resistancetet(X14)tet(X2)Empedobacter stercoris
spellingShingle Yingying Cheng
Yong Chen
Yang Liu
Yuqi Guo
Yanzi Zhou
Tingting Xiao
Shuntian Zhang
Hao Xu
Yunbo Chen
Tongling Shan
Yonghong Xiao
Kai Zhou
Identification of novel tetracycline resistance gene tet(X14) and its co-occurrence with tet(X2) in a tigecycline-resistant and colistin-resistant Empedobacter stercoris
Emerging Microbes and Infections
Tigecycline resistance
tetracycline resistance
tet(X14)
tet(X2)
Empedobacter stercoris
title Identification of novel tetracycline resistance gene tet(X14) and its co-occurrence with tet(X2) in a tigecycline-resistant and colistin-resistant Empedobacter stercoris
title_full Identification of novel tetracycline resistance gene tet(X14) and its co-occurrence with tet(X2) in a tigecycline-resistant and colistin-resistant Empedobacter stercoris
title_fullStr Identification of novel tetracycline resistance gene tet(X14) and its co-occurrence with tet(X2) in a tigecycline-resistant and colistin-resistant Empedobacter stercoris
title_full_unstemmed Identification of novel tetracycline resistance gene tet(X14) and its co-occurrence with tet(X2) in a tigecycline-resistant and colistin-resistant Empedobacter stercoris
title_short Identification of novel tetracycline resistance gene tet(X14) and its co-occurrence with tet(X2) in a tigecycline-resistant and colistin-resistant Empedobacter stercoris
title_sort identification of novel tetracycline resistance gene tet x14 and its co occurrence with tet x2 in a tigecycline resistant and colistin resistant empedobacter stercoris
topic Tigecycline resistance
tetracycline resistance
tet(X14)
tet(X2)
Empedobacter stercoris
url https://www.tandfonline.com/doi/10.1080/22221751.2020.1803769
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