Non-typhoidal Salmonella (NTS) remains a leading cause of food-borne diarrheal disease worldwide. A landmark global burden analysis estimated approximately 93.8 million episodes of gastroenteritis and 155,000 deaths annually, with the greatest impact in low- and middle-income countries and among children under 5 years of age (Majowicz et al., 2010). Crucially, the globalization of food supply chains has introduced new complexities to pathogen dissemination. A recent global atlas spanning 1900–2023 further quantitatively mapped the evolutionary trajectories of Salmonella populations, identifying international food trade and livestock intensification as the primary accelerators of antimicrobial resistance (AMR) dissemination and lineage expansion globally (Wang et al., 2025).

Salmonella enterica is highly diverse, comprising more than 2,600 recognized serovars (Grimont and Weill, 2007). While surveillance consistently shows that a limited number of animal-associated serovars, principally S. Enteritidis and S. Typhimurium (including monophasic 4,5,12:i:-), accounts for most human NTS infections globally (Centers for Disease Control and Prevention [CDC], 2025; European Food Safety Authority [EFSA], and European Centre for Disease Prevention and Control [ECDC], 2024; Ferrari et al., 2019; Gal-Mor et al., 2014). This animal-centric focus often obscures a critical blind spot: the rising incidence of outbreaks links to non-animal reservoirs. Epidemiological investigations in North America and Europe have increasingly implicated fresh produce (e.g., leafy greens, onions) and low-moisture foods (e.g., spices and seasonings) as vehicles for widespread salmonellosis (Aiyedun et al., 2021; Centers for Disease Control and Prevention [CDC], 2010; U.S. Food and Drug Administration [FDA], 2025). Notable historical events, such as the multistate S. Montevideo outbreak traced to imported red and black pepper (Centers for Disease Control and Prevention [CDC], 2010), underscore the ability of Salmonella to persist in desiccated environmental niches and contaminate global food supply chains. Despite this shifting landscape, the specific environmental lineages driving these plant-associated spillovers remain under-surveilled.

To address such surveillance gaps and capture this overlooked diversity, large-scale genomic surveillance efforts have been initiated in China. Through coordinated sequencing and curation of nearly 8,000 isolates, our team established a comprehensive genomic database that integrates human, food, animal, and environmental Salmonella data (Wang et al., 2023a; Wang et al., 2023b). This unified resource enables the rapid identification and contextualization of emerging or rare serovars, thereby supporting timely clinical and public-health responses and underscoring the value of sustained genomic monitoring—particularly for environmentally adapted lineages that may act as reservoirs for future spillover, as exemplified by recent findings of diverse antimicrobial resistance genes and plasmids in hospital effluent pathogens (Chen et al., 2025). It was through this systematic surveillance network that the rare isolate described in this study was identified.

The specific lineage identified is Salmonella enterica subspecies enterica serovar Kumasi (S. Kumasi). First described in 1961, this serovar belongs to O-group 30 (formerly Group N), characterized by the antigenic formula 30:z₁₀:e,n,z₁₅ (Guinée and Kampelmacher, 1961). Unlike broad-host-range serovars, S. Kumasi shares ecological traits with other Group N serovars (e.g., S. Urbana), historically associated with cold-blooded animals and environmental reservoirs (Kocianová et al., 2010; Rimhanen-Finne et al., 2010). Its environmental niche is strongly substantiated by global surveillance data. Our analysis of the NCBI Pathogen Detection database revealed that majority of S. Kumasi genomes were recovered during the 2018 US FDA investigation into contaminated kratom (Mitragyna speciosa) products (Schwensohn et al., 2022; U.S. Food and Drug Administration [FDA], 2018). This specific association with a dried botanical commodity strongly supports the hypothesis that S. Kumasi occupies a plant-associated ecological niche. In contrast, human clinical isolates are exceptionally rare. Consequently, the isolate (XXB410) reported in this study represents the fourth human infection worldwide and the first clinical report from Asia.

Despite its potential relevance to food safety in plant-based supply chains, S. Kumasi remains poorly characterized. The determinants underlying its restricted virulence and sporadic occurrence remain unknown. Here, we describe the genomic features, virulence potential, and ecological context of S. Kumasi ST2302. By integrating microbiological identification with whole-genome sequencing (WGS) and comparative analyses, we elucidate the determinants underlying its restricted virulence and propose its utility as a genomic sentinel for plant-associated food safety risks.

This study broadens the clinical and geographic footprint of S. Kumasi by characterizing the first human case reported in Asia. By integrating the clinical genome with global public datasets, we propose that S. Kumasi represents a specialized plant-adapted lineage rather than a typical broad-host-range serovar. This ecological positioning is strongly substantiated by the origin of the global dataset: a significant proportion of the available genomes were isolated during the 2018 US FDA investigation into contaminated kratom products (Schwensohn et al., 2022; U.S. Food and Drug Administration [FDA], 2018). The recovery of S. Kumasi from these dried botanical supplements not only clarifies the epidemiological background of these archival strains but also, given its rarity in extensive global livestock surveillance, strongly points toward a predominantly plant-associated or environmental ecological niche. To persist in such desiccated, nutrient-limited environments, Salmonella requires specific genomic mechanisms, which are reflected in the S. Kumasi genome.

The genomic machinery of S. Kumasi strongly corroborates its environmental adaptability. Our analysis revealed the universal conservation of the csg operon (curli fimbriae) and the fim operon (Type 1 fimbriae) across all genomes. Functionally, the FimH adhesin specifically binds mannose residues on plant cell walls, while the csg operon encodes curli fimbriae—the primary structural component of the “rdar” (red, dry, and rough) biofilm morphotype (Barak et al., 2005; Berger et al., 2010; White et al., 2006; Zogaj et al., 2001). This phenotype is critical for protecting Salmonella against desiccation stress and UV radiation (White et al., 2006). Furthermore, the detection of the C63PI island suggests an enhanced capacity to sequester iron via the sit system in the metal depleted phyllosphere (Brandl, 2006). Collectively, this specific genomic toolkit aligns with the archetypal features of plant-associated Salmonella, supporting the classification of S. Kumasi as a lineage specialized for survival in the phyllosphere and dried botanical commodities.

The distinct environmental niche also provides a plausible explanation for the lineage’s genomic stability and lack of antimicrobial resistance and plasmids. Unlike high-burden serovars that evolve under constant clinical antibiotic pressure, S. Kumasi displays a pansusceptible phenotype and a scarcity of plasmids. While genomic screening identified an intrinsic aac (6’)-Iaa gene and a parC (T57S) polymorphism, crucially, neither of these features conferred phenotypic resistance. The parC (T57S) substitution is widely recognized as a natural phylogenetic marker rather than a resistance-conferring mutation (Chang et al., 2021; Vázquez et al., 2022), and the aac (6’)-Iaa gene is typically silent in Salmonella unless upregulated by specific mutations (Magnet et al., 1999; Tang et al., 2022). This profile reflects an evolutionary history in “low-pressure” non-clinical environments. However, despite this adaptation, S. Kumasi appears to retain a “cross-kingdom lifestyle” capacity characteristic of the genus (Schikora et al., 2012). The conservation of intact SPI-1and SPI-2 invasion systems indicates that the lineage retains the genomic potential to colonize mammalian hosts upon ingestion (Sia et al., 2025), providing a biological basis for the diarrheal symptoms observed in our case.

Regarding pathogenicity, the isolate presents an “atypical” virulence profile. While canonical invasion determinants (SPI-1 and SPI-2) are retained, the typhoid toxin locus is incomplete. Crucially, sequence analysis reveals that while the divergent CdtB homolog retains conserved catalytic residues essential for DNase activity, the absence of the delivery complex likely compromises the toxin’s entry into host cells (Song et al., 2013). This pattern of gene loss resembles host-adaptation trajectories described in other lineages and aligns with the self-limiting nature of the infection (Langridge et al., 2015; Zhou et al., 2023). Clinically, although incidental detection via foodborne transport is a theoretical possibility, the definitive exclusion of other common viral and bacterial pathogens establishes S. Kumasi as the sole recovered agent, strongly supporting its role as the primary cause.

We acknowledge certain limitations in this study. First, our conclusions regarding the “atypical” virulence potential and environmental adaptation are based on high-resolution genomic data. Future functional characterization using in vitro or in vivo models is required to definitively confirm the biological activity of the divergent cdtB and the biofilm-forming capacity. Second, establishing definitive causality in a single case report presents inherent challenges. While we rigorously excluded common viral and bacterial co-pathogens, the theoretical possibility of incidental detection cannot be entirely eliminated without broader epidemiological data.

From a public health perspective, we propose that S. Kumasi serves as a valuable “genomic sentinel”. While the serovar itself may pose a lower immediate clinical risk than high-burden serovars, its detection signals hygiene vulnerabilities in non-animal supply chains, particularly fresh produce and herbal supplements, which are increasingly recognized as vehicles for transboundary salmonellosis (Aiyedun et al., 2021; Schwensohn et al., 2022). Monitoring such sentinel lineages allows for the early detection of contamination routes that might be missed by traditional meat-focused surveillance. Finally, we emphasize the critical importance of international collaboration. By contributing this first Asian clinical genome to public repositories, we underscore the necessity of global data transparency and an One Health approach to track the cross-border movement of environmental pathogens in our interconnected food systems.

S. Kumasi appears to be a plant-associated lineage with an incomplete typhoid-toxin architecture and limited clinical expansion. These features argue for targeted genomic surveillance of plant-linked supply chains to detect and prevent sporadic spillover.