Neutral genomic microevolution of a recently emerged pathogen, Salmonella enterica serovar Agona

Salmonella enterica serovar Agona has caused multiple foodborne outbreaks of gastroenteritis since it was first isolated in 1952. We analyzed the genomes of 73 isolates from global sources, comparing five distinct outbreaks with sporadic infections. Agona consists of three lineages with minimal mutational diversity: only 846 single nucleotide polymorphisms (SNPs) have accumulated in the non-repetitive, core genome since Agona evolved in 1932 and underwent a major population expansion in the 1960s. Homologous recombination with other serovars of S. enterica imported 42 recombinational tracts (360 kb) in 5/143 nodes within the genealogy, which resulted in 3,164 additional SNPs. In contrast to this paucity of genetic diversity, Agona is highly diverse according to pulsed field gel electrophoresis (PFGE), which is used to assign isolates to outbreaks. PFGE diversity reflects a highly dynamic accessory genome associated with the gain or loss (indels) of 51 bacteriophages, 10 plasmids, and 6 integrative conjugational systems (ICE/IMEs). Unlike the core genome, these indels occurred repeatedly in independent nodes (homoplasies), resulting in inaccurate PFGE genealogies. Most indels did not introduce cargo genes relevant to infection, other than antibiotic resistance, and plasmids and ICE/IMEs were not correlated with homologous recombination. Each outbreak was caused by an independent clade, without universal, outbreak-associated genomic features. Thus, most of the genetic diversity within this recently emerged pathogen reflects changes in the accessory genome, or is due to recombination, but these changes probably reflect neutral processes rather than Darwinian selection.