The Resistance and Virulence Characteristics of Salmonella Enteritidis Strain Isolated from Patients with Food Poisoning Based on the Whole-Genome Sequencing and Quantitative Proteomic Analysis

Benjin Xu; Zhuru Hou; Ling Liu; Rongrong Yan; Jinjing Zhang; Jianhong Wei; Miao Du; Yan Xuan; Lei Fan; Zhuoxi Li

doi:10.2147/IDR.S411125

The Resistance and Virulence Characteristics of Salmonella Enteritidis Strain Isolated from Patients with Food Poisoning Based on the Whole-Genome Sequencing and Quantitative Proteomic Analysis

Infect Drug Resist. 2023 Oct 6:16:6567-6586. doi: 10.2147/IDR.S411125. eCollection 2023.

Authors

Benjin Xu^#^{1

2

3}, Zhuru Hou^#^{2

4}, Ling Liu^#^{1

2

3}, Rongrong Yan³, Jinjing Zhang³, Jianhong Wei⁴, Miao Du^{1

2}, Yan Xuan^{1

2}, Lei Fan^{2

4}, Zhuoxi Li^{2

4}

Affiliations

¹ Department of Medical Laboratory Science, Fenyang College of Shanxi Medical University, Fenyang, People's Republic of China.
² Key Laboratory of Lvliang for Clinical Molecular Diagnostics, Fenyang, People's Republic of China.
³ Department of Clinical Laboratory, Fenyang Hospital of Shanxi Province, Fenyang, People's Republic of China.
⁴ Department of Basic Medicine, Fenyang College of Shanxi Medical University, Fenyang, People's Republic of China.

^# Contributed equally.

Abstract

Objective: This paper explores the drug resistance, genome and proteome expression characteristics of Salmonella from a food poisoning event.

Methods: A multidrug-resistant Salmonella Enteritidis strain, labeled as 27A, was isolated and identified from a food poisoning patient. Antimicrobial susceptibility testing determined the resistance of 27A strain to 14 antibiotics. Then, WGS analysis and comparative genomics analysis were performed on 27A, and the functional annotation of resistance genes, virulence genes were performed based on VFDB, ARDB, COG, CARD, GO, KEGG, and CAZY databases. Meanwhile, based on iTRAQ technology, quantitative proteomic analysis was conducted on 27A to analyze the functions and interactions of differentially expressed proteins related to bacterial resistance and pathogenicity.

Results: Strain 27A belonged to ST11 S. Enteritidis and was resistant to levofloxacin, ciprofloxacin, ampicillin, piperacillin, and ampicillin/sulbactam. There were 33 drug resistance genes, 384 virulence genes and 2 plasmid replicon, IncFIB(S) and IncFII(S), annotated by WGS. Proteomic analysis revealed significant changes in virulence and drug proteins, which were mainly involved in bacterial pathogenicity and metabolic processes. PPI prediction showed the relationship between virulence proteins and T3SS proteins, and PagN cooperated with proteins related to T3SS to jointly mediate the invasion of 27A strain on the human body. Phylogenetic analysis indicated that S. Enteritidis has potential transmission in humans, food, and animals.

Conclusion: This study comprehensively analyzed the drug resistance and virulence phenotypes of S. Enteritidis 27A using genomic and proteomic approaches. These helps reveal the drug resistance and virulence mechanisms of S. Enteritidis, and provides important information for the source tracing and the prevention of related diseases, which lays a foundation for research on food safety, public health monitoring, and the drug resistance and pathogenicity of S. Enteritidis.

Keywords: Salmonella; WGS; evolution; quantitative proteomics; resistance; virulence.

Grants and funding

This study was supported by Fundamental Research Program of Shanxi Province (Grant no. 20210302123397; 202203021212351), Key R&D Projects of Introducing High-Level Scientific and Technological Talents in Lvliang City (Grant no. 2021RC-1-4), the Project of Lvliang City Science and Technology Program (Grant no. 2020SHFZ29), Science and Technology Innovation Project of Colleges and Universities in Shanxi Province (Grant no. 2020L0749), the National College Students’ Innovation and Entrepreneurship Training Program (Grant no. 20221569), Projects of Innovation and Entrepreneurship Training Program for College Students of Fenyang College of Shanxi Medical University (Grant no. FDC202209; FDC202214; FDC202215), and Special Fund for Key Disciplines of Fenyang College of Shanxi Medical University (Grant no. 2022B14).