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

Background: Staphylococcus aureus 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. Objectives: To supplement existing information, this current study investigated the prevalence, clonal distribution, antimicrobial resistance, and virulence gene profiles of S. aureus isolates from fish, fish water, and occupationally exposed fish handlers in Anambra State, Southeast Nigeria. Methods: 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, spa typing, and SCCmec typing. Results: S. aureus was recovered from 16.5% (100/607) of the samples. Fourteen (14%) isolates were methicillin-resistant (MRSA), harboring mecA and SCCmec 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 spa types across 13 clonal complexes (CCs) were identified, with CC1, CC5, and CC8 predominating. The detection of shared spa types between fish and handlers indicates potential cross-contamination. Detected virulence genes included those for accessory gene regulators (agrI-IV), Pantone–Valentine leucocidin (lukFS-PV), toxic shock syndrome (tsst-1), hemolysins (hla, hlb, hld/hlIII, hlgA), biofilm formation (icaA, icaD), immune evasion (chp, scn, sak), enterotoxins (sea, seb, sec, sed, egc, and others), exfoliative toxins (etA, etB), epidermal cells differentiation (edinA, edinB), and capsular types (cap5, cap8). Conclusions: This study reveals that the aquaculture sector in Southeast Nigeria serves as a significant reservoir of genetically diverse, multidrug-resistant S. aureus 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.