Characterization of extended-spectrum cephalosporins and fluoroquinolone resistance of a Salmonella enterica serovar Thompson isolate from ready-to-eat pork product in China

Lili Li; Rikke Heidemann Olsen; Jian Xiao; Meidan Liang; Hecheng Meng; Shifu Peng

doi:10.3389/fmicb.2022.964009

Characterization of extended-spectrum cephalosporins and fluoroquinolone resistance of a Salmonella enterica serovar Thompson isolate from ready-to-eat pork product in China

Front Microbiol. 2022 Sep 15:13:964009. doi: 10.3389/fmicb.2022.964009. eCollection 2022.

Authors

Lili Li^{1

2}, Rikke Heidemann Olsen³, Jian Xiao⁴, Meidan Liang⁴, Hecheng Meng², Shifu Peng⁵

Affiliations

¹ Institute of Food Safety and Nutrition, Jinan University, Guangzhou, China.
² School of Food Science and Engineering, South China University of Technology, Guangzhou, China.
³ Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg C, Denmark.
⁴ Guangzhou Food Inspection Institute, Guangzhou, China.
⁵ Department of Environment and Health, Jiangsu Center for Disease Control and Prevention, Nanjing, China.

Abstract

Salmonella is a leading cause of foodborne illness worldwide and is a common concern in food safety. Salmonella enterica displaying resistance to extended-spectrum cephalosporins (ESCs) and fluoroquinolone (FQs) has been deemed a high-priority pathogen by the World Health Organization. Co-resistance to ESCs and FQs has been reported in S. enterica serovar Thompson (S. Thompson). However, the genetic context of ESCs and FQs resistance genes in S. Thompson lacks sufficient characterization. In this study, we characterized a multi-drug resistant (MDR) S. Thompson isolate recovered from a retail ready-to-eat (RTE) pork product in China. Short- and long-read sequencing (HiSeq and MinION) of the genome identified the presence of bla _CMY-2, qnrS1, and qepA8, along with 11 additional acquired antimicrobial resistance genes, residing on a 152,940 bp IncA/C plasmid. Specifically, the bla _CMY-2, qnrS1, and qepA8 genes were located in insertion sequences (ISs) and integron mediated mobile genetic structure, sugE-blc-bla _CMY-2-ISEc9, IS26-orf6-qnrS1-orf5-ISKpn19, and intl1-qepA8-orf10-IS91-orf1-dfrA12-orf11-aadA2-qacEΔ1-sul1, respectively. Each gene was identified in various bacteria species, indicating their high transfer ability. The plasmid was found to be transferable to Escherichia coli J53 by conjugation and resulted in the acquiring of multiple resistances in the transconjugants. The plasmid is closely related to plasmids from two human S. Thompson strains isolated in different regions and years in China. Moreover, core-genome Multi Locus Sequence Typing (cgMLST) and phylogenetic analysis based on global 1,868 S. Saintpaul isolates showed that the S. Thompson isolate was highly epidemiologically linked to a human isolate in China. Our findings suggest that Chinese RTE pork products are a possible source of human pathogenic ESCs and FQs co-resistant S. Thompson. Furthermore, the results underline the important role of conjugative plasmids in acquiring and transmission of ESCs and FQs resistance in S. Thompson isolates, which need continuous investigation.

Keywords: Salmonella Thompson; blaCMY−2; qepA8; qnrS1; ready-to-eat pork product.