Phylogenomics of “ Candidatus Rickettsia mendelii” reveals a distinct early-diverging lineage with small genomes within the genus Rickettsia

ABSTRACT The genus Rickettsia comprises obligate intracellular bacteria belonging to the class Alphaproteobacteria. Although Rickettsia species have traditionally been classified into several phylogenetic groups, recent genome-based studies have revealed greater diversity within the genus and related Rickettsiaceae lineages than previously recognized. Here, we isolated six rickettsial strains from Ixodes turdus ticks collected at various locations across Japan and performed whole-genome sequencing. A closed-genome sequence was obtained for one of the isolates. The six isolates shared highly similar genomic features and were identified as “ Candidatus Rickettsia mendelii” on the basis of conserved rickettsial marker gene sequences. The genomes of “ Ca . R. mendelii” were smaller (1.05–1.06 Mb) and had lower GC content (29.2–29.3%) than most analyzed rickettsial genomes and were comparable in these respects to those of Typhus Group rickettsiae. Family-wide phylogenomic analysis using a quality-filtered Rickettsiaceae genome data set placed “ Ca . R. mendelii” in a distinct early-diverging lineage within the genus Rickettsia . Chromosome-level comparisons with many other Rickettsia species revealed stretches of conserved synteny distributed across the chromosome of “ Ca . R. mendelii.” Genes encoding major secretion-related and host interaction-associated components were detected, whereas no hits meeting the detection criteria were obtained for the F-type IV secretion system (F-T4SS) proteins encoded by Rickettsiales-amplified genetic elements (RAGEs). These results provide the first genome sequences from cultured “ Ca . R. mendelii” isolates and expand our understanding of genome diversity and evolution within the genus Rickettsia . IMPORTANCE Genome-based studies have expanded the known diversity of the genus Rickettsia and related Rickettsiaceae lineages, but genome information from cultured isolates remains unavailable for some poorly characterized taxa. Here, we report the first whole-genome sequences from six cultured isolates of “ Ca . R. mendelii” and show that this taxon represents a distinct early-diverging lineage within the genus Rickettsia . The genomes of “ Ca . R. mendelii” were smaller and had lower GC content than most analyzed rickettsial genomes and were comparable in these respects to those of Typhus Group rickettsiae, despite the distinct phylogenetic placement. This indicates that similar genome characteristics can occur in phylogenetically distant rickettsial lineages. The low genomic diversity among geographically separated “ Ca . R. mendelii” isolates suggests broad dispersal of closely related strains, which may be facilitated by infected ticks carried by migratory birds. These findings improve our understanding of the genome characteristics and geographic distribution of “ Ca . R. mendelii.”