The F204S mutation in adrenodoxin oxidoreductase drives salinomycin resistance in Eimeria tenella

Abstract Salinomycin is a polyether ionophore widely used for the treatment of coccidiosis in poultry. However, the emergence of coccidia strains resistant to salinomycin presents challenges for control efforts, and the mechanisms underlying this resistance in Eimeria remain inadequately understood....

Full description

Saved in:
Bibliographic Details
Main Authors: Pei Sun, Chaoyue Wang, Fujie Xie, Linlin Chen, Yuanyuan Zhang, Xinming Tang, Dandan Hu, Yang Gao, Ning Zhang, Zhenkai Hao, Yonglan Yu, Jingxia Suo, Xun Suo, Xianyong Liu
Format: Article
Language:English
Published: BMC 2024-12-01
Series:Veterinary Research
Subjects:
Online Access:https://doi.org/10.1186/s13567-024-01431-6
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850102797447462912
author Pei Sun
Chaoyue Wang
Fujie Xie
Linlin Chen
Yuanyuan Zhang
Xinming Tang
Dandan Hu
Yang Gao
Ning Zhang
Zhenkai Hao
Yonglan Yu
Jingxia Suo
Xun Suo
Xianyong Liu
author_facet Pei Sun
Chaoyue Wang
Fujie Xie
Linlin Chen
Yuanyuan Zhang
Xinming Tang
Dandan Hu
Yang Gao
Ning Zhang
Zhenkai Hao
Yonglan Yu
Jingxia Suo
Xun Suo
Xianyong Liu
author_sort Pei Sun
collection DOAJ
description Abstract Salinomycin is a polyether ionophore widely used for the treatment of coccidiosis in poultry. However, the emergence of coccidia strains resistant to salinomycin presents challenges for control efforts, and the mechanisms underlying this resistance in Eimeria remain inadequately understood. In this study, 78 stable salinomycin-resistant strains were generated through experimental evolution approaches. Whole-genome sequencing of salinomycin-resistant Eimeria tenella isolates revealed single nucleotide polymorphisms (SNPs), with 12 candidate genes harboring nonsynonymous mutations identified. To confirm the candidate gene responsible for conferring salinomycin resistance, we leveraged reverse genetic strategies and identified a key amino acid substitution (F204S) in adrenodoxin oxidoreductase (EtADR), which markedly reduced susceptibility to salinomycin. Our results elucidate the complex interactions among salinomycin resistance, parasite fitness, point mutations, and the structure of EtADR, laying the foundation for future studies on drug resistance in Eimeria and contributing to the development of targeted control strategies.
format Article
id doaj-art-1978fc31a5054ebfa2e9f148ff058607
institution DOAJ
issn 1297-9716
language English
publishDate 2024-12-01
publisher BMC
record_format Article
series Veterinary Research
spelling doaj-art-1978fc31a5054ebfa2e9f148ff0586072025-08-20T02:39:41ZengBMCVeterinary Research1297-97162024-12-0155111410.1186/s13567-024-01431-6The F204S mutation in adrenodoxin oxidoreductase drives salinomycin resistance in Eimeria tenellaPei Sun0Chaoyue Wang1Fujie Xie2Linlin Chen3Yuanyuan Zhang4Xinming Tang5Dandan Hu6Yang Gao7Ning Zhang8Zhenkai Hao9Yonglan Yu10Jingxia Suo11Xun Suo12Xianyong Liu13National Key Laboratory of Veterinary Public Health and Safety; Key Laboratory of Animal Epidemiology and Zoonosis of Ministry of Agriculture, National Animal Protozoa Laboratory & College of Veterinary Medicine, China Agricultural UniversityDepartment of Pathogen Biology, Guangdong Provincial Key Laboratory of Tropical Disease Research, School of Public Health, Southern Medical UniversityNational Key Laboratory of Veterinary Public Health and Safety; Key Laboratory of Animal Epidemiology and Zoonosis of Ministry of Agriculture, National Animal Protozoa Laboratory & College of Veterinary Medicine, China Agricultural UniversityNational Key Laboratory of Veterinary Public Health and Safety; Key Laboratory of Animal Epidemiology and Zoonosis of Ministry of Agriculture, National Animal Protozoa Laboratory & College of Veterinary Medicine, China Agricultural UniversityKey Laboratory of Animal Genetics, Breeding and Reproduction of the Ministry of Agriculture & Beijing Key Laboratory of Animal Genetic Improvement, China Agricultural UniversityKey Laboratory of Animal Biosafety Risk Prevention and Control (North) of MARA, Institute of Animal Sciences, Chinese Academy of Agricultural SciencesCollege of Animal Science and Technology, Guangxi UniversityNational Key Laboratory of Veterinary Public Health and Safety; Key Laboratory of Animal Epidemiology and Zoonosis of Ministry of Agriculture, National Animal Protozoa Laboratory & College of Veterinary Medicine, China Agricultural UniversityNational Key Laboratory of Veterinary Public Health and Safety; Key Laboratory of Animal Epidemiology and Zoonosis of Ministry of Agriculture, National Animal Protozoa Laboratory & College of Veterinary Medicine, China Agricultural UniversityNational Key Laboratory of Veterinary Public Health and Safety; Key Laboratory of Animal Epidemiology and Zoonosis of Ministry of Agriculture, National Animal Protozoa Laboratory & College of Veterinary Medicine, China Agricultural UniversityDepartment of Clinic Veterinary Medicine, College of Veterinary Medicine, China Agricultural UniversityNational Key Laboratory of Veterinary Public Health and Safety; Key Laboratory of Animal Epidemiology and Zoonosis of Ministry of Agriculture, National Animal Protozoa Laboratory & College of Veterinary Medicine, China Agricultural UniversityNational Key Laboratory of Veterinary Public Health and Safety; Key Laboratory of Animal Epidemiology and Zoonosis of Ministry of Agriculture, National Animal Protozoa Laboratory & College of Veterinary Medicine, China Agricultural UniversityNational Key Laboratory of Veterinary Public Health and Safety; Key Laboratory of Animal Epidemiology and Zoonosis of Ministry of Agriculture, National Animal Protozoa Laboratory & College of Veterinary Medicine, China Agricultural UniversityAbstract Salinomycin is a polyether ionophore widely used for the treatment of coccidiosis in poultry. However, the emergence of coccidia strains resistant to salinomycin presents challenges for control efforts, and the mechanisms underlying this resistance in Eimeria remain inadequately understood. In this study, 78 stable salinomycin-resistant strains were generated through experimental evolution approaches. Whole-genome sequencing of salinomycin-resistant Eimeria tenella isolates revealed single nucleotide polymorphisms (SNPs), with 12 candidate genes harboring nonsynonymous mutations identified. To confirm the candidate gene responsible for conferring salinomycin resistance, we leveraged reverse genetic strategies and identified a key amino acid substitution (F204S) in adrenodoxin oxidoreductase (EtADR), which markedly reduced susceptibility to salinomycin. Our results elucidate the complex interactions among salinomycin resistance, parasite fitness, point mutations, and the structure of EtADR, laying the foundation for future studies on drug resistance in Eimeria and contributing to the development of targeted control strategies.https://doi.org/10.1186/s13567-024-01431-6Eimeria tenellasalinomycindrug resistancepoint mutation
spellingShingle Pei Sun
Chaoyue Wang
Fujie Xie
Linlin Chen
Yuanyuan Zhang
Xinming Tang
Dandan Hu
Yang Gao
Ning Zhang
Zhenkai Hao
Yonglan Yu
Jingxia Suo
Xun Suo
Xianyong Liu
The F204S mutation in adrenodoxin oxidoreductase drives salinomycin resistance in Eimeria tenella
Veterinary Research
Eimeria tenella
salinomycin
drug resistance
point mutation
title The F204S mutation in adrenodoxin oxidoreductase drives salinomycin resistance in Eimeria tenella
title_full The F204S mutation in adrenodoxin oxidoreductase drives salinomycin resistance in Eimeria tenella
title_fullStr The F204S mutation in adrenodoxin oxidoreductase drives salinomycin resistance in Eimeria tenella
title_full_unstemmed The F204S mutation in adrenodoxin oxidoreductase drives salinomycin resistance in Eimeria tenella
title_short The F204S mutation in adrenodoxin oxidoreductase drives salinomycin resistance in Eimeria tenella
title_sort f204s mutation in adrenodoxin oxidoreductase drives salinomycin resistance in eimeria tenella
topic Eimeria tenella
salinomycin
drug resistance
point mutation
url https://doi.org/10.1186/s13567-024-01431-6
work_keys_str_mv AT peisun thef204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT chaoyuewang thef204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT fujiexie thef204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT linlinchen thef204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT yuanyuanzhang thef204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT xinmingtang thef204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT dandanhu thef204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT yanggao thef204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT ningzhang thef204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT zhenkaihao thef204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT yonglanyu thef204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT jingxiasuo thef204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT xunsuo thef204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT xianyongliu thef204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT peisun f204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT chaoyuewang f204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT fujiexie f204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT linlinchen f204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT yuanyuanzhang f204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT xinmingtang f204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT dandanhu f204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT yanggao f204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT ningzhang f204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT zhenkaihao f204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT yonglanyu f204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT jingxiasuo f204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT xunsuo f204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella
AT xianyongliu f204smutationinadrenodoxinoxidoreductasedrivessalinomycinresistanceineimeriatenella