Genomic and phenotypic characterization of multidrug-resistant salmonella enterica serovar reading isolates involved in a turkey-associated foodborne outbreak

Authors: SIVASANKARAN, SATHESH - Oak Ridge Institute For Science And Education (ORISE); Bearson, Bradley - Brad; Trachsel, Julian; NIELSEN, DANIEL - Oak Ridge Institute For Science And Education (ORISE); Looft, Torey; Bearson, Shawn

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/20/2023
Publication Date: 1/18/2024
Citation: Sivasankaran, S.K., Bearson, B.L., Trachsel, J.M., Nielsen, D.W., Looft, T.P., Bearson, S.M. 2024. Genomic and phenotypic characterization of multidrug-resistant salmonella enterica serovar reading isolates involved in a turkey-associated foodborne outbreak. Frontiers in Microbiology. https://doi.org/10.3389/fmicb.2023.1304029.
DOI: https://doi.org/10.3389/fmicb.2023.1304029

Interpretive Summary: Salmonella is a major human foodborne pathogen that can live in food producing animals without causing signs of disease or carriage, which can result in contamination of animal food products. Over the last 15 years, the Centers for Disease Control and Prevention (CDC) has documented 1,712 foodborne outbreaks involving Salmonella in the United States, and 47 of the outbreaks were associated with turkey products. An outbreak linked to turkey products in 2017-2019 was caused by a specific Salmonella (S. Reading) that did not usually cause human illness. In this study, we compared S. Reading isolates collected prior to the outbreak (pre-outbreak) to S. Reading isolated during the outbreak period to identify differences between the two outbreak groups but common within a group. Variation between the pre-outbreak and outbreak isolates was similarly identified in S. Reading isolated from turkeys/turkey products and human clinical infections. The variations involved missing or mutated genes detected in the outbreak isolates that could alter the fitness of Salmonella in a turkey or human host, thereby potentially enhancing its ability to colonize turkeys or cause human illness. The study illustrates the usefulness of genomic analysis in outbreak investigations as a surveillance mechanism of emerging Salmonella isolates involving food animal production.

Technical Abstract: Salmonella is a global bacterial foodborne pathogen associated with a variety of contaminated food products. Poultry products are a common source of Salmonella-associated foodborne illness, and an estimated 7% of human illnesses in the United States are attributed to turkey products. From November 2017 to March 2019, the Centers for Disease Control and Prevention reported a turkey-associated outbreak of multidrug-resistant (MDR; resistant to >3 antimicrobial classes) Salmonella enterica serovar Reading (S. Reading) linked to 358 human infections in 42 U.S. states and Canada. Because S. Reading was seldom linked to human illness prior to this outbreak, the current study compared genomic sequences of S. Reading isolates prior to the outbreak (pre-outbreak) to isolates identified during the outbreak period, focusing on genes that were different between the two groups but common within a group. Following whole genome sequence analysis of five pre-outbreak and five outbreak-associated turkey isolates of S. Reading, 37 genes located within two distinct chromosomal regions were identified only in the pre-outbreak isolates: 1) an ~5 kb region containing 4 protein-coding genes including uidA which encodes beta-glucuronidase, pgdA encoding peptidoglycan deacetylase, and two hypothetical proteins as well as 2) an ~28 kb region comprised of 32 phage-like genes and the xerC gene which encodes tyrosine recombinase (frequently associated with phage genes). The five outbreak isolates also had a deletional event within the cirA gene introducing a translational frame shift and premature stop codon. The cirA gene encodes a protein with dual receptor functions: a siderophore receptor for transport of dihydroxybenzoylserine as well as a colicin Ia/b receptor. Significant differences for the identified genetic variations were also detected in 75 S. Reading human isolates. Of the 41 S. Reading isolates collected before/in 2017, 81% and 90% of the isolates contained the uidA and pgdA genes, respectively, but only 24% of the isolates collected after 2017 harbored the uidA and pgdA genes. The truncation event within the cirA gene was also significantly higher in isolates collected after 2017 (74%) compared to before/in 2017 (5%). Phenotypic analysis of the S. Reading isolates for colicin and cefiderocol sensitivities (CirA) and ß-methyl-D-glucuronic acid utilization (UidA and accessory proteins) supported the genomic data. Overall, a similar genome reduction pattern was generally observed in both the turkey and human isolates of S. Reading during the outbreak period, and the genetic differences were present in genes that could potentially promote pathogen dissemination due to variation in Salmonella colonization, fitness and/or virulence.