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.
Highlights
Salmonella is a major foodborne pathogen, annually resulting in 1.4 million cases in the United States [1] and over 90 million on a global scale [2]
The goals of this study were to (1) sequence and compare two clinical isolates and ground beef source strains; (2) conduct a detailed genomic comparison of S. typhimurium clinical and bovine-associated DT104 and non-DT104 strains; (3) compare the ground beef outbreak strains against a global DT104 population; (4) compare these bovine-associated DT104 strains to other bovineassociated S. typhimurium from North America, which will provide a detailed genomic characterization of DT104 strains associated with cattle and beef products
S. typhimurium strains are highly clonal, and many traditional subtyping methods such as pulsed field gel electrophoresis (PFGE) have trouble resolving strains during an outbreak [6]. This was true with DT104 strains, as prior to the advent of whole genome sequencing (WGS) only MLVA was shown to have some resolution to differentiate DT104 strains [21,31]
Summary
Salmonella is a major foodborne pathogen, annually resulting in 1.4 million cases in the United States [1] and over 90 million on a global scale [2]. Enterica serovar Typhimurium (Salmonella typhimurium) was the most common serovar fifteen years ago, and it is currently the third most common serovar in the United States [3] with many different types of food products, including beef products, associated with outbreaks. Since 1973, there have been 16 S. typhimurium outbreaks associated with beef products in the U.S, with ground beef accounting for 37.5% of those outbreaks [4]. While beef consumption in the U.S is four times higher than the world average [5], this does suggest surveillance of beef products for S. typhimurium is critically important to the safety of consumers on a global scale
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