The evolution of obligate host-association of bacterial symbionts and pathogens remains poorly understood. The Rickettsiales are an alphaproteobacterial order of obligate endosymbionts and parasites that infect a wide variety of eukaryotic hosts, including humans, livestock, insects and protists. Induced by their host-associated lifestyle, Rickettsiales genomes have undergone reductive evolution, leading to small, AT-rich genomes with limited metabolic capacities. Here we uncover eleven deep-branching alphaproteobacterial metagenome assembled genomes from aquatic environments, including data from the Tara Oceans initiative and other publicly available datasets, distributed over three previously undescribed Rickettsiales-related clades. Phylogenomic analyses reveal that two of these clades, Mitibacteraceae and Athabascaceae, branch sister to all previously sampled Rickettsiales. The third clade, Gamibacteraceae, branch sister to the recently identified ectosymbiotic ‘Candidatus Deianiraea vastatrix’. Comparative analyses indicate that the gene complement of Mitibacteraceae and Athabascaceae is reminiscent of that of free-living and biofilm-associated bacteria. Ancestral genome content reconstruction across the Rickettsiales species tree further suggests that the evolution of host association in Rickettsiales was a gradual process that may have involved the repurposing of a type IV secretion system.

细菌共生体和病原体的专性宿主关联的进化仍然知之甚少。立克次体目是专性内共生菌和寄生虫的α变形菌目，可感染多种真核宿主，包括人类、牲畜、昆虫和原生生物。受宿主相关生活方式的影响，立克次氏体基因组经历了还原性进化，导致代谢能力有限的小型、富含 AT 的基因组。在这里，我们发现了来自水生环境的 11 个深分支 alphaproteobacterial 宏基因组组装的基因组，包括来自Tara的数据海洋倡议和其他公开可用的数据集，分布在三个先前未描述的与立克次氏体相关的进化枝上。系统基因组分析表明，这些进化枝中的两个，Mitibacteraceae 和 Athabascaceae，是所有先前采样的立克次氏体的分支姐妹。第三个进化枝，Gamibacteraceae，是最近发现的外共生菌' Candidatus Deianiraea mastatrix' 的分支姐妹。比较分析表明，Mitibacteraceae 和 Athabascaceae 的基因补体让人联想到自由生活和生物膜相关细菌。立克次体目物种树的祖先基因组内容重建进一步表明，立克次体目宿主关联的进化是一个渐进的过程，可能涉及重新利用 IV 型分泌系统。