Molecular Epidemiology, Antimicrobial Resistance, and Virulence Profiles of Staphylococcus aureus from Fish, Aquatic Environments, and Fish Handlers in Southeast Nigeria

<b>Background:</b><i>Staphylococcus aureus</i> is a major zoonotic and foodborne pathogen with substantial One Health implications, yet its prevalence, resistance, and virulence potential within the aquaculture sector in Nigeria remains poorly characterized. <b>Objectives</b>: To supplement existing information, this current study investigated the prevalence, clonal distribution, antimicrobial resistance, and virulence gene profiles of <i>S. aureus</i> isolates from fish, fish water, and occupationally exposed fish handlers in Anambra State, Southeast Nigeria. <b>Methods</b>: A total of 607 samples-comprising 465 surface swabs from raw and processed fish, 36 fish water samples, and 106 nasal swabs from fish handlers-were processed using selective culture, biochemical tests, antimicrobial susceptibility testing, DNA microarray analysis, <i>spa</i> typing, and SCC<i>mec</i> typing. <b>Results</b>: <i>S. aureus</i> was recovered from 16.5% (100/607) of the samples. Fourteen (14%) isolates were methicillin-resistant (MRSA), harboring <i>mecA</i> and SCC<i>mec</i> types IV and V, with a combined MRSA prevalence of 2.3%. Multidrug resistance was observed in 52.2% of isolates (mean Multiple Antimicrobial Resistance index: 0.23), with 19 resistance genes spanning nine antimicrobial classes-including heavy metal and biocide resistance. Twenty-eight <i>spa</i> types across 13 clonal complexes (CCs) were identified, with CC1, CC5, and CC8 predominating. The detection of shared <i>spa</i> types between fish and handlers indicates potential cross-contamination. Detected virulence genes included those for accessory gene regulators (<i>agrI</i>-<i>IV</i>), Pantone-Valentine leucocidin (<i>lukFS-PV</i>), toxic shock syndrome (<i>tsst-1</i>), hemolysins (<i>hla</i>, <i>hlb</i>, <i>hld</i>/<i>hlIII</i>, <i>hlgA</i>), biofilm formation (<i>icaA</i>, <i>icaD</i>), immune evasion (<i>chp</i>, <i>scn</i>, <i>sak</i>), enterotoxins (<i>sea</i>, <i>seb</i>, <i>sec</i>, <i>sed</i>, <i>egc</i>, and others), exfoliative toxins (<i>etA</i>, <i>etB</i>), epidermal cells differentiation (<i>edinA</i>, <i>edinB</i>), and capsular types (<i>cap5</i>, <i>cap8</i>). <b>Conclusions</b>: This study reveals that the aquaculture sector in Southeast Nigeria serves as a significant reservoir of genetically diverse, multidrug-resistant <i>S. aureus</i> strains with robust virulence profiles. These findings highlight the necessity of integrated One Health surveillance and targeted interventions addressing antimicrobial use and hygiene practices within aquatic food systems.