High-resolution comparative genomics of Salmonella Kentucky aids source tracing and detection of ST198 and ST152 lineage-specific mutations

Authors: SOLTYS, RACHEL - Washington State University; SAKOMOTO, CARSON - Wake Forest University; OLTEAN, HANNA - State Of Washington; Guard, Jean; Haley, Bradd; SHAH, DEVENDRA - Washington State University

Submitted to: Frontiers in Sustainable Food Systems
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/10/2021
Publication Date: 7/30/2021
Citation: Soltys, R.C., Sakomoto, C., Oltean, H.N., Guard, J.Y., Haley, B.J., Shah, D.H. 2021. High-resolution comparative genomics of Salmonella Kentucky aids source tracing and detection of ST198 and ST152 lineage-specific mutations. Frontiers in Sustainable Food Systems. 5:6953368.

Interpretive Summary: Based on comparative phenotypic, genotypic and epidemiologic analysis, this study demonstrates that human strains of Salmonella enterica serotype Kentucky (S. Kentucky) resistant to fluoroquinolone (FluR) and genotyped as ST198 isolated in Washington state during 2004-2014 were likely linked to international travel. In contrast, S. Kentucky ST198 human strains sensitive to fluoroquinolone (FluS) isolated in Washington state during the same period appeared to be linked to domestic cattle sources. Similarly, human FluS S. Kentucky genotyped as ST152 infections in Washington state were likely linked to domestic poultry sources. Increasing incidence of FluR S. Kentucky ST198 in the US and globally raises intriguing questions about whether this lineage is undergoing metabolic or virulence adaptation in a specific niche. A small number of lineage-specific SNPs identified in ST198 and ST152 were predicted to result in high-impact protein effects, and may provide good targets for further investigations on variation in virulence, metabolic adaptation to different environments, and potential for development of intervention strategies to improve the safety of food.

Technical Abstract: Nontyphoidal Salmonella (NTS) is a major cause of foodborne illness globally. Salmonella Kentucky is a polyphyletic NTS serovar comprised of two predominant sequence types (STs): ST152 and ST198. Epidemiological studies have revealed that ST152 is most prevalent in US poultry whereas ST198 is more prevalent internationally. Interestingly, ST152 is sporadically associated with human illness, whereas ST198 is more commonly associated with human disease. In this study, we compared the antimicrobial resistance phenotypes and genetic relationship using sub-genomic fingerprinting of 26 clinical strains of S. Kentucky isolated in Washington State between 2004 and 2014, and 140 poultry-associated strains of S. Kentucky mostly recovered from the northwestern US between 2004 and 2014. We sequenced whole genomes of 2 fluoroquinolone-susceptible (FluS) and 4 fluoroquinolone resistant (FluR) ST198 human clinical isolates along with 4 ST152 strains each isolated from humans and poultry from the northwestern US, respectively. Genome sequences of these isolates were compared with a global database of S. Kentucky genomes representing 400 ST198 and 50 ST152 strains. The results of the phenotypic, genotypic, and case report data on food consumption and travel show the human infection caused by FluR S. Kentucky ST198 in WA State originated from outside of North America. In contrast, FluS S. Kentucky ST198 and S. Kentucky ST152 infection have a likely domestic origin, with domestic cattle and poultry being the potential sources. We also identified lineage-specific single nucleotide polymorphisms that distinguish ST198 and ST152. Further studies are warranted to determine their role in differential virulence, metabolic, or host-adaptation of these lineages.