Global genomic surveillance of Salmonella in the environment: assessing virulence and antimicrobial resistance at scale

Salmonella is a globally distributed zoonotic pathogen with widespread environmental persistence; however, genomic characterization of environmental isolates from underrepresented regions remains limited. Current global data sets are predominantly populated with genomes from high-income countries, restricting our ability to resolve evolutionary trajectories, ecological adaptations, and emerging antimicrobial resistance (AMR). We performed a comparative genomic analysis of 1,399 high-quality Salmonella genomes, integrating 54 newly sequenced isolates from India (representing surface water and soil samples) with global data sets. Phenotypic analysis showed that 55.6% of the Indian isolates were multidrug-resistant, and 72.2% displayed strong biofilm-forming capacity. Integration of global genomes revealed extensive phylogenetic interspersion, reflecting widely distributed lineages shaped by shared ancestry or environmentally mixed Salmonella populations. The pangenome comprised 20,915 genes, with a 3,394 core, and a large accessory genome (>16,001 cloud genes). Serogroups B and C2-C3 dominated globally and carried the broadest AMR repertoires. While efflux-associated and regulatory resistance genes were conserved across subspecies, acquired determinants such as aminoglycoside-modifying enzymes, tet(A/B) , sul genes, and rare extended-spectrum β-lactamases (ESBLs) varied by serogroup. Detection of mcr-1 , mcr-5 , and mcr-9 highlights early circulation of colistin resistance in environmental reservoirs. Core virulence loci (SPI-1/SPI-2) remained uniformly conserved, whereas accessory modules, including spv and pef operons, siderophore systems ( iro , iuc/iut ), and stress-response genes, showed serogroup-specific enrichment. Plasmidome analysis revealed marked diversity, dominated by IncF and colicinogenic plasmids, with serogroup-specific patterns, suggesting niche adaptation and horizontal gene transfer. Overall, environmental Salmonella constitute a globally connected and genetically dynamic reservoir where conserved virulence backbones coexist with rapidly evolving resistance and plasmid repertoires. These findings position environmental surveillance as a cornerstone of One Health preparedness for tackling high-risk, pathogenic lineages of Salmonella .