Genomes of Rickettsiales are shaped by ongoing reductive evolution and are typically small (<1.5 Mb), rich in A+T nucleotides (<40% G+C), display a low coding density (<85%), lack metabolite biosynthesis genes and display a high degree of pseudogenization 6, 7. Well-known examples include Rickettsia prowazekii, the causative agent of epidemic typhus in humans 4, and Wolbachia, a genus of bacteria infecting over two-thirds of arthropods and nearly all filarial nematodes 5. Rickettsiales infect a wide variety of eukaryotic species, including protists, leeches, cnidarians, arthropods and mammals 1. The Rickettsiales represent a widespread and diverse order of obligate host-associated alphaproteobacteria that have been estimated to have originated >1.7 Ga, similar to a conservative estimated age of eukaryotes 2, 3. While the molecular and cellular underpinnings of host association have been described in considerable detail 1, their evolutionary origin remains generally poorly understood. Obligate host-associated bacteria include pathogens that represent a leading cause of human, livestock and crop disease, resulting in considerable economic loss worldwide. 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. Comparative analyses indicate that the gene complement of Mitibacteraceae and Athabascaceae is reminiscent of that of free-living and biofilm-associated bacteria. The third clade, Gamibacteraceae, branch sister to the recently identified ectosymbiotic ‘ Candidatus Deianiraea vastatrix’. Phylogenomic analyses reveal that two of these clades, Mitibacteraceae and Athabascaceae, branch sister to all previously sampled Rickettsiales. 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. Induced by their host-associated lifestyle, Rickettsiales genomes have undergone reductive evolution, leading to small, AT-rich genomes with limited metabolic capacities. 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. The evolution of obligate host-association of bacterial symbionts and pathogens remains poorly understood.
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