Comparative pangenomic and phylogenetic analysis of Staphylococcus aureus for identifying ecological associations of adhesion genes and the role of fibronectin-binding proteins across the food supply chain

Sammanfattning

Staphylococcus aureus is a common opportunistic pathogen and a major cause of foodborne intoxication worldwide with high ecological plasticity and adaptability to diverse ecological niches. Its accessory genome, contains extensive virulence determinants that contribute to strong metabolic and physiological flexibility, enables it to persist under complex and adverse conditions encountered throughout the food supply chain including during food production and preservation. The aim of this study was to investigate the distribution of adhesion-associated genes with a particular focus on the fibronectin-binding protein genes (fnbA and fnbB), and their potential role in the ecological adaptation of Staphylococcus aureus across the food supply chain. Comparative genomic analyses were performed using publicly available isolate genomes and metagenome-assembled genomes. A total of 4,503 genomes were analysed and annotated using comparative pangenomics, core-genome phylogenetics and phylogeny-aware genome-wide association analyses to identify niche associated genomic patterns among 15 adhesion-associated virulence determinants with a focus on fibronectin-binding proteins. The samples were unevenly distributed among ecological niches and the dataset was biased towards milk-associated samples. Nevertheless, the pangenome contained approximately 80% accessory genes with a Heap’s law α value of 0.87, supporting an accessory-rich open pangenome. Significant associations were identified between different ecological niches and several adhesion-associated genes, including sdrC, sdrD, sdrE, icaA, icaD, icaR, ebpS, clfA clfB, fnbA and fnbB. These results provide evidence for possible candidate niche-associated genomic patterns. However, the broad distribution of fnbA and fnbB suggests that these genes are biologically important but cannot be considered simple niche-specific markers or direct markers of transmission routes. Overall, the findings suggest that adhesion association genes may contribute to the ecological flexibility of S. aureus across the food supply chain, although they do not confirm direct transmission, functional adaptation or causality. Further studies are required to validate these associations and to evaluate the potential role of fibronectin-binding proteins in the persistence and adaptation of S. aureus in food-associated environments.