Decoding the enigma: unveiling the molecular transmission of avian-associated tet(X4)-positive E. coli in Sichuan Province, China

Shaqiu Zhang; Jinfeng Wen; Yuwei Wang; Zhijun Zhong; Mingshu Wang; Renyong Jia; Shun Chen; Mafeng Liu; Dekang Zhu; Xinxin Zhao; Ying Wu; Qiao Yang; Juan Huang; Xumin Ou; Sai Mao; Qun Gao; Di Sun; Bin Tian; Anchun Cheng

Poultry Science (Dec 2023)

Decoding the enigma: unveiling the molecular transmission of avian-associated tet(X4)-positive E. coli in Sichuan Province, China

Shaqiu Zhang,
Jinfeng Wen,
Yuwei Wang,
Zhijun Zhong,
Mingshu Wang,
Renyong Jia,
Shun Chen,
Mafeng Liu,
Dekang Zhu,
Xinxin Zhao,
Ying Wu,
Qiao Yang,
Juan Huang,
Xumin Ou,
Sai Mao,
Qun Gao,
Di Sun,
Bin Tian,
Anchun Cheng

Affiliations

Shaqiu Zhang: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the PR China, Chengdu 611130, PR China
Jinfeng Wen: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China
Yuwei Wang: Mianyang Academy of Agricultural Sciences, Mianyang 621023, PR China
Zhijun Zhong: Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the PR China, Chengdu 611130, PR China
Mingshu Wang: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the PR China, Chengdu 611130, PR China
Renyong Jia: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the PR China, Chengdu 611130, PR China
Shun Chen: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the PR China, Chengdu 611130, PR China
Mafeng Liu: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the PR China, Chengdu 611130, PR China
Dekang Zhu: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the PR China, Chengdu 611130, PR China
Xinxin Zhao: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the PR China, Chengdu 611130, PR China
Ying Wu: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the PR China, Chengdu 611130, PR China
Qiao Yang: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the PR China, Chengdu 611130, PR China
Juan Huang: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the PR China, Chengdu 611130, PR China
Xumin Ou: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the PR China, Chengdu 611130, PR China
Sai Mao: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the PR China, Chengdu 611130, PR China
Qun Gao: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the PR China, Chengdu 611130, PR China
Di Sun: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the PR China, Chengdu 611130, PR China
Bin Tian: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the PR China, Chengdu 611130, PR China
Anchun Cheng: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the PR China, Chengdu 611130, PR China; Corresponding author:

Journal volume & issue: Vol. 102, no. 12
p. 103142

Abstract

Read online

ABSTRACT: Tigecycline is considered one of the “last resort antibiotics” for treating complex infections caused by multidrug-resistant (MDR) bacteria, especially for combating clinical resistant strains that produce carbapenemases. However, the tet(X4) gene, which carried by different plasmids can mediate high levels of bacterial resistance to tigecycline, was first reported in 2019. Here, we report the emergence of the plasmid-mediated tet(X4) in avian environment of Sichuan Province. A total of 21 tet(X4)-positive Escherichia coli (E. coli) strains were isolated and identified from avian samples in selected regions, with an isolation rate of 1.6% (21/1,286), and all of them were MDR strains. Multilocus Sequence Typing (MLST) method was used to classify the 21 tet(X4)-positive E. coli into the ST206, ST761, ST155, ST1638, ST542, and ST767 types, which also belong to the 3 phylogenetic subgroups A, B1, and C. Tet(X4) is located on mobile plasmids that can be efficiently and stably propagated. The results of fitness cost experiments showed that tet(X4)-positive plasmids may incur some fitness cost to host bacteria, but different tet(X4)-positive plasmids bring about differential fitness costs. Whole-genome sequencing further confirmed the tet(X4) gene can be located on IncX1-type plasmids and the core genetic structures are ISVsa3-rdmc-tet(X4) or rdmc-tet(X4)-ISVsa3, the former is a 7 copies tandem repeat structure. In this study, we isolated and identified tet(X4)-positive E. coli from the avian origin in Sichuan, analyzed the mobility of the tet(X4) by conjugational transfer and S1-PFGE, and evaluated the biological characteristics of the tet(X4)-positive plasmid using the results of conjugational frequency, plasmid stability, and fitness costs. Finally, combined with the third-generation whole-genome sequencing analysis, the molecular transmission characteristics of the tet(X4) were preliminarily clarified, providing a scientific basis for guiding veterinary clinical use in this area, as well as risk assessment and prevention of the transfer and spread of tigecycline resistant strains or genes.

Published in Poultry Science

ISSN: 0032-5791 (Print); 1525-3171 (Online)
Publisher: Elsevier
Country of publisher: United States
LCC subjects: Agriculture: Animal culture
Website: https://www.journals.elsevier.com/poultry-science

About the journal

Abstract

Keywords