Genetic Diversity and Epidemiological Overlap of Staphylococcus aureus at the Animal–Food–Environment–Human Interface Within a One Health Framework

Vollständiger Abstract

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ABSTRACT This study aimed to assess the genetic diversity and potential epidemiological overlap of Staphylococcus aureus using molecular (spa and SCCmec typing) and phenotypic characterization of 108 isolates obtained along the farm‐to‐fork continuum (dairy and meat chains) and 50 human clinical isolates. Forty‐four spa types, including 17 novel patterns, were identified, with t11284 and t127 predominating among animal‐related MRSA and clinical MRSA, respectively. Six SCCmec types (I–VI) were detected in the majority of isolates (85.2%), with SCCmec IVa prevalent in farm‐to‐fork isolates (67%) and SCCmec III dominant in clinical isolates (28%). Spa repeat‐based MST analysis revealed a heterogeneous distribution of isolates across clusters, with identical spa types detected in multiple source categories, indicating genetic relatedness rather than direct transmission events. Overall, 54.6% of isolates exhibited a multidrug‐resistant phenotype. Farm‐to‐fork isolates showed mainly β‐lactam resistance (≥ 85%), whereas clinical MRSA exhibited broader resistance profiles, including high fluoroquinolone resistance (≥ 92%). PVL was detected in 41 isolates (38%), predominantly in MRSA, and was associated with SCCmec IV/V and diverse spa types. Toxin genes ( tst −1, sea , seb , and sed ) were mainly confined to clinical MRSA, suggesting source‐associated distribution of virulence determinants. Biofilm formation was observed in 49 isolates (45.3%), more frequently among farm‐to‐fork isolates. Our study demonstrate marked genetic and phenotypic diversity of S. aureus across farm‐to‐fork and human clinical sources and suggest the presence of shared genetic lineages among isolates from different sources. The results support the importance of integrated One Health surveillance for monitoring antimicrobial‐resistant and virulent S. aureus populations across interconnected ecological compartments.