Abstract
BACKGROUND: Salmonella enterica subspecies enterica serovar Kumasi (S. Kumasi) is an exceptionally rare non-typhoidal Salmonella (NTS) serovar that has been historically linked to plant- or environment-associated sources and only sporadically isolated from humans. Its genomic characteristics, ecological niche, and pathogenic potential remain poorly defined. METHODS: The clinical isolate (XXB410) underwent antimicrobial susceptibility testing and whole-genome sequencing. Comparative phylogenomic, resistome, virulence, and pan-genome analyses were performed against all 20 publicly available S. Kumasi genomes. RESULTS: We report the first human infection due to S. Kumasi in Asia, isolated from a 4-year-old child in China presenting with self-limiting diarrhea. XXB410 was identified as sequence type ST2302 and clustered within a lineage dominated by plant/botanical and non-human sources. The genome was plasmid-free and pansusceptible, carrying only the intrinsic aac (6')-Iaa and parC (T57S) polymorphism, with no acquired antimicrobial resistance (AMR) genes. Genomic profiling confirmed the conservation of canonical invasion islands (SPI1/2) and determinants critical for environmental persistence and plant attachment (e.g., csg operon), yet revealed an atypical toxin architecture restricted to a divergent cdtB homolog without pltA/B subunits. Pairwise core-genome SNP distances between XXB410 and other ST2302 isolates fell well outside outbreak-level relatedness, supporting sporadic spillover from plant-associated reservoirs rather than sustained human transmission. CONCLUSION: These findings expand the clinical and geographic range of S. Kumasi and support a model of a plant-adapted lineage characterized by a scarcity of mobile genetic elements (MGEs), an incomplete toxin architecture, and limited clinical expansion. The benign, self-limiting clinical course aligns with the genomic profile. Collectively, we propose S. Kumasi as a genomic sentinel to monitor hygiene vulnerabilities in plant-based food supply chains.