Staphylococcus in the One Health era: genomic insights and ecological roles reshaping food safety from farm to fork

Staphylococci are ubiquitous multi-host bacteria, encompassing Staphylococcus aureus alongside non- aureus staphylococci, and mammaliicocci (NASM), with profound implications for human and animal health and food safety. Staphylococcus aureus lineages exhibit repeated host jumps between humans and livestock, followed by niche-specific adaptation through core genome remodeling and acquisition or loss of mobile genetic elements encoding virulence and antimicrobial resistance. Host-specialist S. aureus clones dominate ecological niches, whereas host-generalist lineages carrying versatile resistance cassettes present the highest risk of zoonotic and foodborne emergence. NASM act as active participants in microbial ecology rather than passive reservoirs. Extensive horizontal gene transfer among NASM shapes the accessory gene pool, spreading antimicrobial resistance and metabolic traits across species, while selected NASM strains antagonize critical foodborne pathogens, modulate biofilms, and influence microbial community dynamics in host and food matrices. These contrasting roles underscore the need to distinguish high-risk NASM lineages from potentially beneficial ones. Hence, genome-informed surveillance integrating host-adaptive traits, metabolic adaptations, mobile resistance elements, and defense systems can predict emerging spillovers. Furthermore, coupling genomic data with antimicrobial usage, ecological context, and food-production practices will allow early detection of emergent clones and inform interventions to mitigate cross-host transmission and antimicrobial resistance dissemination. More strategically, using NASM as microbial ecological competitor could enhance food safety. Thus, advancing our understanding of staphylococcal host specialization, pangenome openness, and horizontal gene transfer is critical for predicting high-risk staphylococcal lineages and guiding proactive One Health interventions across the farm-to-fork continuum.