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ORIGINAL RESEARCH article

Front. Microbiol.

Sec. Infectious Agents and Disease

Volume 16 - 2025 | doi: 10.3389/fmicb.2025.1602985

This article is part of the Research TopicInfectious disease control in the microbial functional genomics eraView all 9 articles

Methicillin-resistant Staphylococcus aureus in Saudi Arabia: genomic evidence of recent clonal expansion and plasmid-driven resistance dissemination

Provisionally accepted
Ahmed  Yousef AlhejailiAhmed Yousef Alhejaili1Ge  ZhouGe Zhou2Heba  HalawaHeba Halawa1Jiayi  HuangJiayi Huang2Omniya  FallatahOmniya Fallatah2Raneem  HiraybanRaneem Hirayban2Sara  IftikharSara Iftikhar2Abrar  AlasmariAbrar Alasmari1Mathew  MilnerMathew Milner2Manuel  BanzhafManuel Banzhaf3Albandari  A AlzaidiAlbandari A Alzaidi1Ahmad  A RajehAhmad A Rajeh1Maram  Al-OtaibyMaram Al-Otaiby1Sarah  S AlabbadSarah S Alabbad1Doua  BukhariDoua Bukhari1Abdullah  N AljurayyanAbdullah N Aljurayyan1Alanoud  T AljashamAlanoud T Aljasham4Zeyad  A AlzeyadiZeyad A Alzeyadi5Sulaiman  M AlajelSulaiman M Alajel6Rawan  Hamdan AlanaziRawan Hamdan Alanazi7Majed  F. AlghoribiMajed F. Alghoribi1Mashal  M AlmutairiMashal M Almutairi4Arnab  PainArnab Pain2Abiola  SenokAbiola Senok8*Danesh  MoradigaravandDanesh Moradigaravand2*Waleed  Al SalemWaleed Al Salem1*
  • 1Ministry of Health (Saudi Arabia), Riyadh, Riyadh, Saudi Arabia
  • 2King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
  • 3Newcastle University, Newcastle upon Tyne, North East England, United Kingdom
  • 4King Saud University, Riyadh, Riyadh, Saudi Arabia
  • 5Shaqra University, Shaqraa, Riyadh, Saudi Arabia
  • 6Saudi Food and Drug Authority (SFDA), Riyadh, Saudi Arabia
  • 7Ministry of Environment, Water and Agriculture (Saudi Arabia), Riyadh, Saudi Arabia
  • 8Mohammed Bin Rashid University of Medicine and Health Sciences, Dubai, United Arab Emirates

The final, formatted version of the article will be published soon.

Staphylococcus aureus is a leading cause of hospital-acquired infections worldwide. Over recent decades, methicillin-resistant Staphylococcus aureus (MRSA), which is resistant to multiple antimicrobials, has emerged as a significant pathogenic strain in both hospital and community settings. The rapid emergence and dissemination of MRSA clones are driven by a dynamic and evolving population, spreading swiftly across regions on epidemiological time scales. Despite the vast geographical expanse and diverse demographics of the Kingdom of Saudi Arabia and the broader West Asia region, the population diversity of MRSA in hospitals in these areas remains underexplored.We conducted a large-scale genomic analysis of a systematic Staphylococcus aureus collection obtained from 34 hospitals across all provinces of KSA, from diverse body sites between 2022 and 2024. The dataset comprised 581 MRSA and 31 methicillin-susceptible Staphylococcus aureus (MSSA) isolates, all subjected to whole-genome sequencing. A combination of phylogenetic and population genomics approaches was utilized to analyze the genomic data. Hybrid sequencing approach was employed to retrieve the complete plasmid content.The population displayed remarkable diversity, comprising 35 distinct sequence types (STs), with the majority harboring community-associated SCCmec loci (types IVa, V/VII, and VI). Virulence factors associated with community-acquired MRSA (CA-MRSA), including Panton-Valentine Leukocidin (PVL) genes, were identified in 12 distinct STs. Dominant clones, including ST8-t008 (USA300), ST88-t690, ST672-t3841, ST6-t304, and ST5-t311, were associated with infections at various body sites and were widely disseminated across the country. Linezolid and vancomycin resistance were mediated by cfr-carrying plasmids and mutations in the vraR gene (involved in cell-wall stress response) and the murF gene (peptidoglycan biosynthesis) in five isolates, respectively. Phylodynamic analysis revealed rapid expansion of the dominant clones, with their emergence estimated to have occurred 10-20 years ago. Plasmidome analysis uncovered a diverse repertoire of blaZ-containing plasmids and the sharing of erm(C)-encoding plasmids among major clades. The acquisition of plasmids coincided with clonal expansion.Our results highlight the recent concurrent expansion and geographical dissemination of CA-MRSA clones across hospitals. These findings also underscore the interplay between clonal spread and horizontal gene transfer in shaping the resistance landscape of MRSA.

Keywords: MRSA, MSSA, Bloodstream infection, St, Precision epidemiology, Kingdom of Saudi Arabia

Received: 02 Apr 2025; Accepted: 21 May 2025.

Copyright: © 2025 Alhejaili, Zhou, Halawa, Huang, Fallatah, Hirayban, Iftikhar, Alasmari, Milner, Banzhaf, Alzaidi, Rajeh, Al-Otaiby, Alabbad, Bukhari, Aljurayyan, Aljasham, Alzeyadi, Alajel, Alanazi, Alghoribi, Almutairi, Pain, Senok, Moradigaravand and Al Salem. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence:
Abiola Senok, Mohammed Bin Rashid University of Medicine and Health Sciences, Dubai, United Arab Emirates
Danesh Moradigaravand, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
Waleed Al Salem, Ministry of Health (Saudi Arabia), Riyadh, 11176, Riyadh, Saudi Arabia

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