Comparative genomic analysis of antibiotic resistance and virulence genes in Staphylococcus aureus isolates from patients and retail meat

Dalal M Alkuraythi; Manal M Alkhulaifi; Abdulwahab Z Binjomah; Mohammed Alarwi; Mohammed I Mujallad; Saleh Ali Alharbi; Mohammad Alshomrani; Takashi Gojobori; Sulaiman M Alajel

doi:10.3389/fcimb.2023.1339339

Comparative genomic analysis of antibiotic resistance and virulence genes in Staphylococcus aureus isolates from patients and retail meat

Front Cell Infect Microbiol. 2024 Jan 12:13:1339339. doi: 10.3389/fcimb.2023.1339339. eCollection 2023.

Authors

Affiliations

¹ Department of Botany and Microbiology, College of Science, King Saud University, Riyadh, Saudi Arabia.
² Department of Biology, College of Science, University of Jeddah, Jeddah, Saudi Arabia.
³ Microbiology Department, Riyadh Regional Laboratory, Ministry of Health, Riyadh, Saudi Arabia.
⁴ College of Medicine, Al-Faisal University, Riyadh, Saudi Arabia.
⁵ Computational Bioscience Research Center, Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
⁶ Department of Microbiology, Food and Drug Authority, Jeddah, Saudi Arabia.
⁷ Reference Laboratory for Microbiology, Executive Department for Reference Laboratories, Research and Laboratories Sector, Food and Drug Authority, Riyadh, Saudi Arabia.

Abstract

Introduction: Staphylococcus aureus is a significant human pathogen that poses a threat to public health due to its association with foodborne contamination and a variety of infections. The factors contributing to the pathogenicity of S. aureus include virulence, drug resistance, and toxin production, making it essential to monitor their prevalence and genetic profiles. This study investigated and compared the genomic characteristics of S. aureus isolates from retail meat and patients in Saudi Arabia.

Methods: A total of 136 S. aureus isolates were obtained between October 2021 and June 2022:84 from patients and 53 from meat samples in Riyadh, Saudi Arabia. S. aureus isolates were identified using conventional methods and MALDI-TOF MS, and methicillin-resistant S. aureus (MRSA) was identified using VITEK2 and BD Phoenix systems. MRSA was confirmed phenotypically using chromogenic agar, and genotypically by detecting mecA. Genomic data were analyzed using BactopiaV2 pipeline, local BLAST, and MLST databases.

Results: Antibiotic resistance genes were prevalent in both meat and patient S. aureus isolates, with high prevalence of tet38, blaZ, and fosB. Notably, all S. aureus isolates from patients carried multidrug-resistant (MDR) genes, and a high percentage of S. aureus isolates from meat also harbored MDR genes. Phenotypically, 43% of the S. aureus isolates from meat and 100% of the patients' isolates were MDR. Enterotoxin genes, including selX, sem, and sei, exhibited high compatibility between meat and patient S. aureus isolates. Virulence genes such as cap, hly/hla, sbi, and isd were found in all S. aureus isolates from both sources.

Conclusion: Our study established a genetic connection between S. aureus isolates from meat and patients, showing shared antibiotic resistance and virulence genes. The presence of these genes in meat derived isolates underscores its role as a reservoir. Genomic relatedness also suggests potential transmission of resistance between different settings. These findings emphasize the necessity for a comprehensive approach to monitor and control S. aureus infections in both animals and humans.

Keywords: MRSA; Staphylococcal toxins; Staphylococcus aureus; antibiotic resistance genes; virulence factors.

Publication types

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

MeSH terms

Animals
Anti-Bacterial Agents / pharmacology
Drug Resistance, Microbial
Genomics
Humans
Meat
Methicillin-Resistant Staphylococcus aureus* / genetics
Microbial Sensitivity Tests
Multilocus Sequence Typing / methods
Staphylococcal Infections* / epidemiology
Staphylococcus aureus
Virulence / genetics

Substances

Anti-Bacterial Agents

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was partially funded by the Saudi Food and Drug Authority (SFDA), Riyadh, Saudi Arabia, and King Abdullah University of Science and Technology (KAUST), Thwal, Saudi Arabia.