Genomic and phenotypic characterization of Salmonella enterica serovar Kentucky

Abstract

Non-typhoidal Salmonella are extremely diverse and different serovars can exhibit varied phenotypes, including host adaptation and the ability to cause clinical illness in animals and humans. In the USA, Salmonella enterica serovar Kentucky is infrequently found to cause human illness, despite being the top serovar isolated from broiler chickens. Conversely, in Europe, this serovar falls in the top 10 serovars linked to human salmonellosis. Serovar Kentucky is polyphyletic and has two lineages, Kentucky-I and Kentucky-II; isolates belonging to Kentucky-I are frequently isolated from poultry in the USA, while Kentucky-II isolates tend to be associated with human illness. In this study, we analysed whole-genome sequences and associated metadata deposited in public databases between 2017 and 2021 by federal agencies to determine serovar Kentucky incidence across different animal and human sources. Of 5151 genomes, 90.3 % were from isolates that came from broilers, while 5.9 % were from humans and 3.0 % were from cattle. Kentucky-I isolates were associated with broilers, while isolates belonging to Kentucky-II and a new lineage, Kentucky-III, were more commonly associated with cattle and humans. Very few serovar Kentucky isolates were associated with turkey and swine sources. Phylogenetic analyses showed that Kentucky-III genomes were more closely related to Kentucky-I, and this was confirmed by CRISPR-typing and multilocus sequence typing (MLST). In a macrophage assay, serovar Kentucky-II isolates were able to replicate over eight times better than Kentucky-I isolates. Analysis of virulence factors showed unique patterns across these three groups, and these differences may be linked to their association with different hosts.

Risk assessment predicts most of the salmonellosis risk in raw chicken parts is concentrated in those few products with high-levels of high-virulent serotypes ofSalmonella

“…Importantly, while our study used Salmonella as a proxy to define Salmonella subgroups that differ in virulence, it is becoming increasingly clear that there is substantial diversity and heterogeneity within many Salmonella serotypes. This is particularly apparent and important for Salmonella Kentucky, which represents at least two distinct clades, one that is virulence attenuated and common in chickens in the US (representing predominantly ST 152) and one that appears highly virulent and often is resistant to multiple antibiotics (ST 198) (Tate et al, 2022), and potentially other clades when using different nomenclature (Richards, Kue, et al, 2023). In our study here, Salmonella Kentucky thus represents a proxy for Salmonella Kentucky ST 152.…”

“…In contrast, to these high-virulent serotypes, there is evidence that Kentucky may represent a low-virulence serotype. Salmonella Kentucky was the most frequently recovered serotype from the carcass surveillance program from USDA-FSIS, but they are less likely to cause human illnesses in the U.S. than other serotypes (Cosby et al, 2015;Richards, Kue, et al, 2023).…”