Neutral genomic microevolution of a recently emerged pathogen, Salmonella enterica serovar Agona. Salmonella enterica subsp. enterica serovar Agona str. 16.H.08 isolate:DBS_20080506

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事件。本研究对73株来自全球不同地区的分离株开展了基因组组成比较分析，这些分离株涵盖5起独立暴发事件及散发病例。阿贡纳血清型可划分为三个谱系，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，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）。在其谱系树的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个重组区段（总长度360 kb），由此额外引入了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）分型中表现出高度多样性，而该方法正是用于将分离株归类至不同暴发事件的常规手段。PFGE分型展现的多样性，反映出该菌拥有高度动态的泛基因组（pan-genome），该泛基因组的变化与51个噬菌体、10种质粒以及6个整合接合元件（integrative conjugational systems, ICE/IMEs）的获得或缺失（插入缺失，indels）密切相关。与核心基因组不同，这些插入缺失事件在独立的谱系节点上反复出现（即同塑性事件，homoplasies），这导致PFGE构建的谱系树出现不准确的情况。除抗生素抗性相关基因外，大多数此类插入缺失事件并未影响与感染相关的载荷基因（cargo genes），且质粒与整合接合元件的携带情况与同源重组并无显著关联。每一起暴发事件均由独立的进化枝（clades）引发，未携带与暴发相关的特异性基因组特征。综上，这种新近出现的病原菌所具有的多数遗传多样性，要么源于附属基因组（accessory genome）的变化，要么由同源重组导致，但这些变化更可能是中性演化过程的结果，而非达尔文自然选择的产物。