High-resolution genomic comparisons within Salmonella enterica serotypes derived from beef feedlot cattle: Parsing the roles of cattle source, pen, animal, sample type and production period

Authors: LEVENT, GIZEM - Texas A&M University; SCHLOCHTERMEIER, ASHLYNN - West Texas A & M University; IVES, SAMUEL - West Texas A & M University; NORMAN, KERI - Texas A&M University; LAWHON, SARA - Texas A&M University; LONERAGAN, GUY - Texas Tech University; Anderson, Robin; VINASCO, JAVIER - Texas A&M University; DEN BAKKER, HENK - University Of Georgia; SCOTT, HARVEY - Texas A&M University

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/6/2021
Publication Date: 5/26/2021
Citation: Levent, G., Schlochtermeier, A., Ives, S.E., Norman, K.N., Lawhon, S.D., Loneragan, G.H., Anderson, R.C., Vinasco, J., Den Bakker, H., Scott, H.M. 2021. High-resolution genomic comparisons within Salmonella enterica serotypes derived from beef feedlot cattle: Parsing the roles of cattle source, pen, animal, sample type and production period. Applied and Environmental Microbiology. 18(12). Article e00485-21. https://doi.org/10.1128/AEM.00485-21.
DOI: https://doi.org/10.1128/AEM.00485-21

Interpretive Summary: The foodborne bacterial pathogen named Salmonella can be a major contaminant in beef products and has been identified as the primary source of many recent Salmonella-related outbreaks. There are many different strains of Salmonella that have been isolated from cattle and their pathogenic activity and antibiotic resistance can be strongly associated by the relatedness of these different strains. Consequently, it important to understand how these different strains of Salmonella are distributed within different cattle production systems. For instance, sampling methods used, the time of year of sampling, the farms the cattle had previously been at, and even their location within different pens on the farm they were sampled at have all been identified as important factors influencing which type of Salmonella may be recovered from a specific animal. In this study, we used state of the art gene sequencing techniques to compare the relatedness of many different Salmonella strains. We found that the relatedness of the many different Salmonella strains recovered from the sampled cattle was mainly influenced by their location at their current farm as well as by where the cattle had initially come from. Further research is needed concerning the role of the feedlot pen environment prior to cattle placement to better understand carry-over contributions of existing strains of Salmonella. These results help provide livestock producers information and tools to prevent the spread of Salmonella-infected cattle between and within herds, thereby reducing the chance of sending infected cattle to the market. Ultimately, these results will help producers continue to produce wholesome beef products at less cost for the American consumer.

Technical Abstract: Salmonella enterica is a major foodborne pathogen, and contaminated beef products have been identified as the primary source of Salmonella-related outbreaks. Pathogenicity and antibiotic resistance of Salmonella are highly serotype- and subpopulation-specific, which makes it essential to understand high-resolution Salmonella population dynamics in cattle. Time of year, source of cattle, pen and sampling site (i.e., feces, hide, or lymph nodes) have previously been identified as important factors influencing the serotype of Salmonella (e.g., Anatum, Lubbock, Cerro, Montevideo, Kentucky, Newport, and Norwich) that were isolated from a longitudinal sampling design in a research feedlot. In this study, we performed high-resolution genomic comparisons of Salmonella isolates within each serotype using both single-nucleotide polymorphism (SNP)-based maximum likelihood phylogeny and hierarchical clustering of core-genome multi-locus sequence typing. The importance of the aforementioned features on clonal Salmonella expansion was further explored using a supervised machine learning algorithm. In addition, we identified and compared the resistance genes, plasmids, and pathogenicity island profiles of the isolates within each sub-population. Our findings indicate that clonal expansion of Salmonella strains in cattle was mainly influenced by the randomization block and pen, as well as the origin/source of the cattle; that is, regardless of sampling time and sample type (i.e., feces, lymph node, or hide). Further research is needed concerning the role of the feedlot pen environment prior to cattle placement to better understand carry-over contributions of existing strains of Salmonella and their bacteriophages.