Genomic diversity and resistome profiles of Salmonella enterica subsp. enterica serovar Kentucky isolated from food and animal sources in Ireland

Authors: SLOWEY, ROSEMARIE - Department Of Agriculture, Food, And The Marine; Kim, Seonwoo; PRENDERGAST, DEIRDRE - Department Of Agriculture, Food, And The Marine; MADIGAN, GILLIAN - Department Of Agriculture, Food, And The Marine; Van Kessel, Jo Ann; Haley, Bradd

Submitted to: Zoonoses and Public Health
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/20/2021
Publication Date: 10/30/2021
Citation: Slowey, R., Kim, S., Prendergast, D., Madigan, G., Van Kessel, J.S., Haley, B.J. 2021. Genomic diversity and resistome profiles of Salmonella enterica subsp. enterica serovar Kentucky isolated from food and animal sources in Ireland. Zoonoses and Public Health. (10):1011. https://doi.org/10.1111/zph.12884.
DOI: https://doi.org/10.1111/zph.12884

Interpretive Summary: Salmonella Kentucky is a globally-distributed subgroup of the human and animal pathogen Salmonella enterica. Salmonella Kentucky is considered an emerging pathogen and it frequently causes human illness in Europe, Africa, and Southeast Asia. Even though S. Kentucky is frequently harbored by food-producing animals in the United States, it rarely causes human disease in this country. This regional discrepancy is due to the differences in the virulence potential of the different Kentucky types found throughout the world. To better understand the Kentucky types isolated from agricultural sources in Ireland, we partnered with the Department of Agriculture, Food and the Marine Laboratories in Ireland to sequence the genomes of 61 isolates collected from food sources in this country. The genomes were analyzed for the presence of antibiotic resistance genes and they were compared with the genomes of isolates collected from animals and human clinical cases across the world. Results of this study demonstrated that most of the S. Kentucky from Ireland are similar to strains that rarely cause disease in humans and are rarely isolated from food animals in the United States. Additionally, most of the isolates were not antibiotic-resistant, but two strains that are similar to those known to cause considerable disease in humans were resistant to multiple antibiotics. The results of this study will help scientists to further understand the diversity amongst the Salmonella Kentucky found around the world and the potential human health risk of S. Kentucky strains in food and animal sources outside of the United States.

Technical Abstract: Salmonella enterica subsp. enterica serovar Kentucky is frequently isolated from poultry, dairy and beef cattle, the environment, and people with clinical salmonellosis globally. However, the sources of this serovar and the diversity and antimicrobial resistance capacities remain poorly-described in many regions. To further understand the genetic diversity and antimicrobial sensitivity patterns among S. Kentucky strains isolated from non-human sources in Ireland, we sequenced and analyzed the genomes of 61 isolates collected from avian, bovine, canine, ovine, piscine, porcine, environmental, and vegetation sources between 2000 and 2016. The majority of isolates (n = 53, ca. 86%) were sequence type (ST) 314, while only three isolates were ST198 and one was ST152. Several isolates were multidrug-resistant and 14 carried at least one acquired antimicrobial resistance gene. When compared to a database of publicly-available ST314, four distinct clades were identified (Clades I – IV) with the majority of isolates from Ireland clustering together in Clade I. Two of the three ST198 isolates were characteristic of those originating outside of the Americas (Clade ST198.2), while one was distantly clustered with isolates from South and North America (clade ST198.1). The genomes of the two clade ST198.2 isolates encoded Salmonella Genomic Island 1 (SGI1), were multidrug resistant, and encoded polymorphisms in the DNA gyrase (gyrA) and DNA topoisomerase (parC) known to confer resistance to fluoroquinolones. The single ST152 isolate was from raw beef, clustered with isolates from food and bovine sources in North America, and was pan-susceptible. Results of this study indicate that most S. Kentucky isolates from non-human sources in Ireland are closely related ST314, and only a few isolates are antimicrobial-resistant. This study also demonstrates the presence of multidrug-resistant ST198 in food sources in Ireland.