Methicillin-resistant Staphylococcus aureus in Saudi Arabia: genomic evidence of recent clonal expansion and plasmid-driven resistance dissemination
ObjectivesStaphylococcus 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...
Saved in:
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2025-06-01
|
| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1602985/full |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850135310756741120 |
|---|---|
| author | Ahmed Yousef Alhejaili Ahmed Yousef Alhejaili Ge Zhou Heba Halawa Jiayi Huang Omniya Fallatah Raneem Hirayban Sara Iftikhar Abrar AlAsmari Mathew Milner Manuel Banzhaf Albandari A. Alzaidi Ahmad A. Rajeh Maram Abdulmohsen Al-Otaiby Sarah S. Alabbad Doua Bukhari Abdullah N. Aljurayyan Alanoud T. Aljasham Zeyad A. Alzeyadi Sulaiman M. Alajel Rawan Hamdan Alanazi Majed Alghoribi Mashal M. Almutairi Arnab Pain Arnab Pain Abiola Senok Abiola Senok Danesh Moradigaravand Waleed Al Salem |
| author_facet | Ahmed Yousef Alhejaili Ahmed Yousef Alhejaili Ge Zhou Heba Halawa Jiayi Huang Omniya Fallatah Raneem Hirayban Sara Iftikhar Abrar AlAsmari Mathew Milner Manuel Banzhaf Albandari A. Alzaidi Ahmad A. Rajeh Maram Abdulmohsen Al-Otaiby Sarah S. Alabbad Doua Bukhari Abdullah N. Aljurayyan Alanoud T. Aljasham Zeyad A. Alzeyadi Sulaiman M. Alajel Rawan Hamdan Alanazi Majed Alghoribi Mashal M. Almutairi Arnab Pain Arnab Pain Abiola Senok Abiola Senok Danesh Moradigaravand Waleed Al Salem |
| author_sort | Ahmed Yousef Alhejaili |
| collection | DOAJ |
| description | ObjectivesStaphylococcus 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.MethodsWe 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.ResultsThe population displayed remarkable diversity, comprising 48 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 (involved in 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.ConclusionsOur 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. |
| format | Article |
| id | doaj-art-5aac8ce36245434db8e0aa4f9fa5e4da |
| institution | OA Journals |
| issn | 1664-302X |
| language | English |
| publishDate | 2025-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj-art-5aac8ce36245434db8e0aa4f9fa5e4da2025-08-20T02:31:27ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-06-011610.3389/fmicb.2025.16029851602985Methicillin-resistant Staphylococcus aureus in Saudi Arabia: genomic evidence of recent clonal expansion and plasmid-driven resistance disseminationAhmed Yousef Alhejaili0Ahmed Yousef Alhejaili1Ge Zhou2Heba Halawa3Jiayi Huang4Omniya Fallatah5Raneem Hirayban6Sara Iftikhar7Abrar AlAsmari8Mathew Milner9Manuel Banzhaf10Albandari A. Alzaidi11Ahmad A. Rajeh12Maram Abdulmohsen Al-Otaiby13Sarah S. Alabbad14Doua Bukhari15Abdullah N. Aljurayyan16Alanoud T. Aljasham17Zeyad A. Alzeyadi18Sulaiman M. Alajel19Rawan Hamdan Alanazi20Majed Alghoribi21Mashal M. Almutairi22Arnab Pain23Arnab Pain24Abiola Senok25Abiola Senok26Danesh Moradigaravand27Waleed Al Salem28Ministry of Health, Riyadh, Saudi ArabiaNewcastle University Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Newcastle upon Tyne, United KingdomLaboratory of Infectious Disease Epidemiology, KAUST Center of Excellence for Smart Health and Biological and Environmental Science and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaLaboratory of Infectious Disease Epidemiology, KAUST Center of Excellence for Smart Health and Biological and Environmental Science and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaLaboratory of Infectious Disease Epidemiology, KAUST Center of Excellence for Smart Health and Biological and Environmental Science and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaLaboratory of Infectious Disease Epidemiology, KAUST Center of Excellence for Smart Health and Biological and Environmental Science and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaLaboratory of Infectious Disease Epidemiology, KAUST Center of Excellence for Smart Health and Biological and Environmental Science and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaLaboratory of Infectious Disease Epidemiology, KAUST Center of Excellence for Smart Health and Biological and Environmental Science and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaMinistry of Health, Riyadh, Saudi ArabiaLaboratory of Infectious Disease Epidemiology, KAUST Center of Excellence for Smart Health and Biological and Environmental Science and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaFaculty of Medical Sciences, Biosciences Institute, Newcastle University, Newcastle upon Tyne, United KingdomMinistry of Health, Riyadh, Saudi ArabiaMinistry of Health, Riyadh, Saudi ArabiaMinistry of Health, Riyadh, Saudi ArabiaMinistry of Health, Riyadh, Saudi ArabiaMinistry of Health, Riyadh, Saudi ArabiaMinistry of Health, Riyadh, Saudi ArabiaDepartment of Clinical Laboratory Sciences, College of Applied Medical Sciences, King Saud University, Riyadh, Saudi ArabiaDepartment of Clinical Laboratory Sciences, College of Applied Medical Sciences, Shaqra University, Shaqra, Saudi ArabiaExecutive Department of Reference Laboratories, Research and Laboratories Sector, Saudi Food and Drug Authority, Riyadh, Saudi ArabiaMinistry of Environment Water and Agriculture, Riyadh, Saudi ArabiaMinistry of Health, Riyadh, Saudi ArabiaDepartment of Pharmacology and Toxicology, College of Pharmacy, King Saud University, Riyadh, Saudi Arabia0Pathogen Genomics Laboratory, KAUST Center of Excellence for Smart Health and Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia1International Institute for Zoonosis Control, Hokkaido University, Sapporo, Japan2College of Medicine, Mohammed Bin Rashid University of Medicine and Health Sciences, Dubai, United Arab Emirates3School of Dentistry, Cardiff University, Cardiff, United KingdomLaboratory of Infectious Disease Epidemiology, KAUST Center of Excellence for Smart Health and Biological and Environmental Science and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaMinistry of Health, Riyadh, Saudi ArabiaObjectivesStaphylococcus 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.MethodsWe 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.ResultsThe population displayed remarkable diversity, comprising 48 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 (involved in 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.ConclusionsOur 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.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1602985/fullMRSAMSSAbloodstream infectionSTprecision epidemiologyKingdom of Saudi Arabia |
| spellingShingle | Ahmed Yousef Alhejaili Ahmed Yousef Alhejaili Ge Zhou Heba Halawa Jiayi Huang Omniya Fallatah Raneem Hirayban Sara Iftikhar Abrar AlAsmari Mathew Milner Manuel Banzhaf Albandari A. Alzaidi Ahmad A. Rajeh Maram Abdulmohsen Al-Otaiby Sarah S. Alabbad Doua Bukhari Abdullah N. Aljurayyan Alanoud T. Aljasham Zeyad A. Alzeyadi Sulaiman M. Alajel Rawan Hamdan Alanazi Majed Alghoribi Mashal M. Almutairi Arnab Pain Arnab Pain Abiola Senok Abiola Senok Danesh Moradigaravand Waleed Al Salem Methicillin-resistant Staphylococcus aureus in Saudi Arabia: genomic evidence of recent clonal expansion and plasmid-driven resistance dissemination Frontiers in Microbiology MRSA MSSA bloodstream infection ST precision epidemiology Kingdom of Saudi Arabia |
| title | Methicillin-resistant Staphylococcus aureus in Saudi Arabia: genomic evidence of recent clonal expansion and plasmid-driven resistance dissemination |
| title_full | Methicillin-resistant Staphylococcus aureus in Saudi Arabia: genomic evidence of recent clonal expansion and plasmid-driven resistance dissemination |
| title_fullStr | Methicillin-resistant Staphylococcus aureus in Saudi Arabia: genomic evidence of recent clonal expansion and plasmid-driven resistance dissemination |
| title_full_unstemmed | Methicillin-resistant Staphylococcus aureus in Saudi Arabia: genomic evidence of recent clonal expansion and plasmid-driven resistance dissemination |
| title_short | Methicillin-resistant Staphylococcus aureus in Saudi Arabia: genomic evidence of recent clonal expansion and plasmid-driven resistance dissemination |
| title_sort | methicillin resistant staphylococcus aureus in saudi arabia genomic evidence of recent clonal expansion and plasmid driven resistance dissemination |
| topic | MRSA MSSA bloodstream infection ST precision epidemiology Kingdom of Saudi Arabia |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1602985/full |
| work_keys_str_mv | AT ahmedyousefalhejaili methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT ahmedyousefalhejaili methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT gezhou methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT hebahalawa methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT jiayihuang methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT omniyafallatah methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT raneemhirayban methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT saraiftikhar methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT abraralasmari methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT mathewmilner methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT manuelbanzhaf methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT albandariaalzaidi methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT ahmadarajeh methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT maramabdulmohsenalotaiby methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT sarahsalabbad methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT douabukhari methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT abdullahnaljurayyan methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT alanoudtaljasham methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT zeyadaalzeyadi methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT sulaimanmalajel methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT rawanhamdanalanazi methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT majedalghoribi methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT mashalmalmutairi methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT arnabpain methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT arnabpain methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT abiolasenok methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT abiolasenok methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT daneshmoradigaravand methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination AT waleedalsalem methicillinresistantstaphylococcusaureusinsaudiarabiagenomicevidenceofrecentclonalexpansionandplasmiddrivenresistancedissemination |