Neutral genomic microevolution of a recently emerged pathogen, Salmonella enterica serovar Agona. Salmonella enterica subsp. enterica serovar Agona str. 45.E.09 isolate:SF_R0037-09

Salmonella enterica serovar Agona has caused multiple food-borne outbreaks of gastroenteritis since it was first isolated in 1952. We compared the genomic contents of 73 isolates from global sources, including five distinct outbreaks and 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 3164 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 pan-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 of these indels did not affect 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 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.

肠炎沙门氏菌阿贡纳血清型（Salmonella enterica serovar Agona）自1952年首次被分离以来，已引发多起食源性胃肠炎暴发疫情。本研究对73株来自全球不同来源的分离株进行了基因组组成比较，这些分离株涵盖5起明确的暴发疫情以及散发性感染病例。阿贡纳血清型可分为三个进化谱系，其突变多样性极低：自1932年阿贡纳血清型演化形成并于20世纪60年代发生大规模种群扩张以来，其非重复核心基因组仅累积了846个单核苷酸多态性（single nucleotide polymorphisms, SNPs）。在该菌的进化系谱的143个节点中，有5个节点发生了与其他肠炎沙门氏菌血清型的同源重组，导入了42个重组片段（总长360kb），由此额外产生了3164个SNPs。与这种极低的遗传多样性形成鲜明对比的是，阿贡纳血清型在脉冲场凝胶电泳（pulsed field gel electrophoresis, PFGE，常用于为分离株划分暴发聚类）下呈现出高度多样性。PFGE多样性反映了其高度动态的泛基因组，该泛基因组与51个噬菌体、10个质粒以及6个整合接合元件（integrative conjugational systems, ICE/IMEs）的获得或缺失（插入缺失，insertions and deletions, indels）相关。与核心基因组不同，这些插入缺失事件在独立的进化节点中多次发生（即同塑性，homoplasies），由此导致PFGE系谱分析结果不准确。除了抗生素耐药性相关基因外，大多数此类插入缺失事件并未影响与感染相关的功能基因，且质粒与整合接合元件并未与同源重组存在相关性。每一起暴发疫情均由独立的进化枝引发，未携带与暴发相关的基因组特征。因此，这种新近出现的病原菌内部的绝大多数遗传多样性，要么体现为附属基因组的变化，要么源自同源重组，但这些变化更可能反映的是中性进化过程，而非达尔文自然选择。