Genomic characterization of Salmonella typhimurium DT104 strains associated with cattle and beef products

Authors: Parker, Craig; Huynh, Steven; ALEXANDER, AARON - California State University; OLIVER, ANDREW - California State University; COOPER, KERRY - University Of Arizona

Submitted to: Pathogens
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/27/2021
Publication Date: 4/27/2021
Citation: Parker, C., Huynh, S., Alexander, A., Oliver, A.S., Cooper, K.K. 2021. Genomic characterization of Salmonella typhimurium DT104 strains associated with cattle and beef products. Pathogens. 10(5):529. https://doi.org/10.3390/pathogens10050529.
DOI: https://doi.org/10.3390/pathogens10050529

Interpretive Summary: Salmonella Typhimurium is a major foodborne pathogen and the most common serotype in many parts of the world, additionally the multidrug resistant phage type DT104 strains are the most frequent phage type in many countries. Understanding the genomics of these strains and improving the genomic epidemiology will allow for more rapid source-tracking during outbreaks. Improving source-tracking allows for a more rapid identification of contaminated food products, which can then be recalled quicker and eliminate additional cases. By determining the types of genomic analysis that are the most effective at rapidly and accurately identifying clusters of DT104 strains during an outbreak will provide public health officials with improved genomic epidemiology tools, which is vital to improving global food safety. In this study, we sequenced several S. Typhimurium DT104 strains associated with a 2009 outbreak caused by ground beef, including the outbreak source strain and several clinical strains. Comparing the 2009 outbreak DT104 strains to global DT104 strains demonstrated that whole genome multi-locus sequence typing (wgMLST) analysis provided the higher resolution needed to more accurately cluster strains based on country and source of isolation compared to core genome MLST (cgMLST).

Technical Abstract: Salmonella enterica subsp. Enterica serovar Typhimurium DT104, a multidrug-resistant phage type, has emerged globally as a major cause of foodborne outbreaks particularly associated with contaminated beef products. In this study, we sequenced three S. Typhimurium DT104 strains associated with a 2009 outbreak caused by ground beef, including the outbreak source strain and two clinical strains. The goal of the study was to gain a stronger understanding of the genomics and genomic epidemiology of highly clonal S. Typhimurium DT104 strains associated with bovine sources. Our study found no single nucleotide polymorphisms (SNPs) between the ground beef source strain and the clinical isolates from the 2009 outbreak. SNP analysis including twelve other S. Typhimurium strains from bovine and clinical sources, including both DT104 and non-DT104, determined DT104 strains averaged 55.0 SNPs between strains compared to 474.5 SNPs among non-DT104 strains. Phylogenetic analysis separated the DT104 strains from the non-DT104 strains, but strains did not cluster together based on source of isolation even within the DT104 phage type. Pangenome analysis of the strains confirmed previous studies showing that DT104 strains are missing the genes for the allantoin utilization pathway, but this study confirmed that the genes were part of a deletion event and not substituted or disrupted by the insertion of another genomic element. Additionally, cgMLST analysis revealed that DT104 strains with cattle as the source of isolation were quite diverse as a group and did not cluster together, even among strains from the same country. Expansion of the analysis to 775 S. Typhimurium ST19 strains associated with cattle from North America revealed diversity between strains, not limited to just among DT104 strains, which suggests that the cattle environment is favorable for a diverse group of S. Typhimurium strains and not just DT104 strains.