Genomic characterization of endemic and ecdemic non-typhoidal Salmonella enterica lineages circulating among animals and animal products in South Africa

Abstract

Non-typhoidal Salmonella enterica imposes a significant burden on human and animal health in South Africa. However, very little is known about lineages circulating among animals and animal products in the country on a genomic scale. Here, we used whole-genome sequencing (WGS) to characterize 63 Salmonella enterica strains (n = 18, 8, 13, and 24 strains assigned to serotypes Dublin, Hadar, Enteritidis, and Typhimurium, respectively) isolated from livestock, companion animals, wildlife, and animal products in South Africa over a 60-year period. Within-serotype phylogenies were constructed using genomes sequenced in this study, as well as publicly available genomes representative of each respective serotypes (i) global (n = 2,802 and 1,569 S. Dublin and Hadar genomes, respectively) and (ii) African (n = 716 and 343 S. Enteritidis and Typhimurium genomes, respectively) population. For S. Dublin, the approaches used here identified a largely antimicrobial-susceptible, endemic lineage circulating among humans, animals, and food in South Africa, as well as a lineage that was likely recently introduced from the United States. For S. Hadar, multiple South African lineages harboring streptomycin and tetracycline resistance-conferring genes were identified. African S. Enteritidis could be primarily partitioned into one largely antimicrobial-susceptible and one largely multidrug-resistant (MDR) clade, with South African isolates confined to the largely antimicrobial-susceptible clade. S. Typhimurium strains sequenced here were distributed across the African S. Typhimurium phylogeny, representing a diverse range of lineages, including numerous MDR lineages. Overall, this study provides insight into the evolution, population structure, and antimicrobial resistome composition of Salmonella enterica in Africa. IMPORTANCEGlobally, Salmonella enterica is estimated to be responsible for more than 93 million illnesses and 150,000 deaths annually. In Africa, the burden of salmonellosis is disproportionally high; however, WGS efforts are overwhelmingly concentrated in world regions with lower salmonellosis burdens. While WGS is being increasingly employed in South Africa to characterize Salmonella enterica, the bulk of these efforts have centered on characterizing human clinical strains. WGS data derived from non-typhoidal Salmonella enterica serotypes isolated from non-human sources in South Africa is extremely limited. To our knowledge, the genomes sequenced here represent the largest collection of non-typhoidal Salmonella enterica isolate genomes from non-human sources in South Africa to date. Furthermore, this study provides critical insights into endemic and ecdemic non-typhoidal Salmonella enterica lineages circulating among animals, foods, and humans in South Africa and showcases the utility of WGS in characterizing animal-associated strains from a world region with a high salmonellosis burden.