Abstract: The bacterial accessory genome, comprised of plasmids, phages, and other mobile elements, underpins the adaptability of bacterial populations. Pangenome (core and accessory) analysis of pathogens can reveal epidemiological relatedness missed by using core-genome methods alone. Employing a k-mer-based Jaccard Index approach to compute pangenome relatedness, we explore the population structure and epidemiology of Salmonella enterica serotype Hadar (Hadar), an emerging zoonotic pathogen in the United States (U.S.) linked to both commercial and backyard poultry. A total of 3384 U.S. Hadar genomes collected between 1990 and 2023 are analyzed here. Hadar populations underwent substantial shifts between 2019 and 2020 in the U.S., driven by the expansion of a lineage carrying a previously uncommon prophage-like element. Phylogenetic and pangenomic relatedness, coupled with epidemiological data, suggest this lineage emerged from extant populations circulating in commercial poultry, with subsequent dissemination into backyard poultry environments. We demonstrate the utility of pangenomic approaches for mapping vertical and horizontal diversity and informing complex dynamics of zoonotic bacterial pathogens.

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