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Genomic and proteomic analysis of Salmonella Enteritidis isolated from a patient with foodborne diarrhea

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Abstract

Salmonella is a major cause of foodborne diseases and clinical infections worldwide. This study aimed to investigate the drug resistance, genomic characteristics, and protein expression of foodborne Salmonella in Shanxi Province. We isolated a strain of Salmonella Enteritidis from patient feces and designated it 31A. The drug resistance of 31A against 14 antibiotics was determined using an antimicrobial susceptibility test. Whole-genome sequencing and quantitative proteomic analysis were performed on the 31A strain. Functional annotation of drug resistance genes/proteins and virulence genes/proteins was conducted using various databases, such as VFDB, ARDB, CAZY, COG, KOG, CARD, GO, and KEGG. The focus of this study was understanding the mechanisms related to food poisoning, and the genetic evolution of 31A was analyzed through comparative genomics. The 31A strain belonged to ST11 Salmonella Enteritidis and showed resistance to β-lactam and quinolone antibiotics. The genome of 31A had 70 drug resistance genes, 321 virulence genes, 12 SPIs, and 3 plasmid replicons. Functional annotation of these drug resistance and virulence genes revealed that drug resistance genes were mainly involved in defense mechanisms to confer resistance to antibiotics, while virulence genes were mainly associated with cellular motility. There were extensive interactions among the virulence genes, which included SPI-1, SPI-2, flagella, fimbriae, capsules and so on. The 31A strain had a close relationship with ASM2413794v1 and ASM130523v1, which were also ST11 Salmonella Enteritidis strains from Asia and originated from clinical patients, animals, and food. These results suggested minimal genomic differences among strains from different sources and the potential for interhost transmission. Differential analysis of the virulence and drug resistance-related proteins revealed their involvement in pathways related to human diseases, indicating that these proteins mediated bacterial invasion and infection. The integration of genomic and proteomic information led to the discovery that Salmonella can survive in a strong acid environment through various acid resistance mechanisms after entering the intestine with food and then invade intestinal epithelial cells to exert its effects. In this study, we comprehensively analyzed the drug resistance and virulence characteristics of Salmonella Enteritidis 31A using a combination of genomic and proteomic approaches, focusing on the pathogenic mechanism of Salmonella Enteritidis in food poisoning. We found significant fluctuations in various virulence factors during the survival, invasion, and infection of Salmonella Enteritidis, which collectively contributed to its pathogenicity. These results provide important information for the source tracing, prevention, and treatment of clinical infections caused by Salmonella Enteritidis.

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Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

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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).

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XBJ and LL designed the study and performed the experiments. HZR and XBJ drafted the manuscript. XBJ, HZR and LL revised the manuscript. HZR, XBJ, LL and WJH performed the literature search and analyzed the data. All authors have read and approved the final manuscript.

Corresponding authors

Correspondence to Benjin Xu or Zhuru Hou.

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The authors have no conflict of interest to declare.

Ethical approval

The study was approved by the Ethics Committee at Fenyang College of Shanxi Medical University. All research subjects signed an informed consent. All methods were performed in accordance with relevant guidelines and regulations. All investigators adhered to the principles expressed in the Declaration of Helsinki.

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Accession number

The nucleotide sequence of the chromosome and plasmids of S. Enteritidis isolate 31A have been deposited in GenBank under Accession Numbers CP121003-CP1210005.

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Supplementary file1 (DOCX 26 KB)

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Mass spectrometry identification of strain 31A. Supplementary file10 (JPG 230 KB)

11274_2023_3857_MOESM11_ESM.jpg

Basic information of quantified proteins. A: number of unique peptides in protein; B: the coverage of proteins; C: the molecular weight distribution of protein; D: the principal component analysis of 31A strain and reference strain. CG, the reference strain.Supplementary file11 (JPG 557 KB)

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Xu, B., Hou, Z., Liu, L. et al. Genomic and proteomic analysis of Salmonella Enteritidis isolated from a patient with foodborne diarrhea. World J Microbiol Biotechnol 40, 48 (2024). https://doi.org/10.1007/s11274-023-03857-0

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