Genetic characteristics, antimicrobial susceptibility, and virulence genes distribution of Campylobacter isolated from local dual-purpose chickens in central China

Jia Xiao; Yiluo Cheng; Wenting Zhang; Qin Lu; Yunqing Guo; Qiao Hu; Guoyuan Wen; Huabin Shao; Qingping Luo; Tengfei Zhang

doi:10.3389/fcimb.2023.1236777

Genetic characteristics, antimicrobial susceptibility, and virulence genes distribution of Campylobacter isolated from local dual-purpose chickens in central China

Front Cell Infect Microbiol. 2023 Sep 7:13:1236777. doi: 10.3389/fcimb.2023.1236777. eCollection 2023.

Authors

Jia Xiao¹, Yiluo Cheng¹, Wenting Zhang^{1

2}, Qin Lu^{1

2}, Yunqing Guo^{1

2}, Qiao Hu^{1

2}, Guoyuan Wen^{1

2}, Huabin Shao^{1

2}, Qingping Luo^{1

2

3}, Tengfei Zhang^{1

2}

Affiliations

¹ Key Laboratory of Prevention and Control Agents for Animal Bacteriosis (Ministry of Agriculture and Rural Affairs), Institute of Animal Husbandry and Veterinary, Hubei Academy of Agricultural Sciences, Wuhan, China.
² Hubei Provincial Key Laboratory of Animal Pathogenic Microbiology, Institute of Animal Husbandry and Veterinary, Hubei Academy of Agricultural Sciences, Wuhan, China.
³ Institute of Animal Husbandry and Veterinary, Hubei Academy of Agricultural Sciences, Hubei Hongshan Laboratory, Wuhan, China.

Abstract

Food-borne antibiotic-resistant Campylobacter poses a serious threat to public health. To understand the prevalence and genetic characteristics of Campylobacter in Chinese local dual-purpose (meat and eggs) chickens, the genomes of 30 Campylobacter isolates, including 13 C. jejuni and 17 C. coli from Jianghan-chickens in central China, were sequenced and tested for antibiotic susceptibility. The results showed that CC-354 and CC-828 were the dominant clonal complexes of C. jejuni and C. coli, respectively, and a phylogenetic analysis showed that three unclassified multilocus sequence types of C. coli were more closely genetically related to C. jejuni than to other C. coli in this study. Of the six antibiotics tested, the highest resistance rates were to ciprofloxacin and tetracycline (100%), followed by lincomycin (63.3%), erythromycin (30.0%), amikacin (26.7%), and cefotaxime (20.0%). The antibiotic resistance rate of C. coli was higher than that of C. jejuni. The GyrA T86I mutation and 15 acquired resistance genes were detected with whole-genome sequencing (WGS). Among those, the GyrA T86I mutation and tet(O) were most prevalent (both 96.7%), followed by the blaOXA-type gene (90.0%), ant(6)-Ia (26.7%), aac(6')-aph(3'') (23.3%), erm(B) (13.3%), and other genes (3.3%). The ciprofloxacin and tetracycline resistance phenotypes correlated strongly with the GyrA T86I mutation and tet(O)/tet(L), respectively, but for other antibiotics, the correlation between genes and resistance phenotypes were weak, indicating that there may be resistance mechanisms other than the resistance genes detected in this study. Virulence gene analysis showed that several genes related to adhesion, colonization, and invasion (including cadF, porA, ciaB, and jlpA) and cytolethal distending toxin (cdtABC) were only present in C. jejuni. Overall, this study extends our knowledge of the epidemiology and antibiotic resistance of Campylobacter in local Chinese dual-purpose chickens.

Keywords: Campylobacter; antibiotic resistance; antibiotic-resistance gene; virulence factor; whole-genome sequencing.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Anti-Bacterial Agents / pharmacology
Campylobacter*
Chickens*
China / epidemiology
Ciprofloxacin / pharmacology
Phylogeny
Virulence / genetics

Substances

Anti-Bacterial Agents
Ciprofloxacin

Grants and funding

This work was supported by grants from the National Key Research and Development Plan of China (2022YFD1800400), the China Agriculture Research System (CARS-41), the Key Projects of Hubei Natural Science Foundation (2021CFA019), and the Key Research and Development Program of Hubei Province (2022BBA0055).