Marked Genome Reduction Driven by a Parasitic Lifestyle: Two Complete Genomes of Endosymbiotic Bacteria Possibly Hosted by a Dinoflagellate.

Abstract

Bacteria with endosymbiotic lifestyles often show marked genome reduction. While the shrinkage of genomes in intracellular symbionts of animals, including parasitic bacteria, has been extensively exami-ned, less is known about symbiotic bacteria associated with single-celled eukaryotes. We herein report the genomes of two novel gammaproteobacterial lineages, RS3 and XS4, identified as putative parasitic endosymbionts of the dinoflagellate Citharistes regius. Phylogenetic ana-lyses suggest that RS3 and XS4 belong to the family Fastidiosibacteraceae within the order Beggiatoales, forming independent lineages therein. The genomes of RS3 and XS4 are 529 and 436‍ ‍kbp in size, respectively, revealing marked reductions from related bacterial genomes. XS4, which has a very reduced genome with a low GC content, uses a different genetic code, in which UGA assigned tryptophan. The small genomes of RS3 and XS4 encode a limited number of proteins, retaining only approximately 20% of the predicted ancestral proteome. Metabolic reconstruction suggests that RS3 and XS4 are parasitic symbionts that are heavily dependent on their host for essential metabolites. Furthermore, we found that the ancestor of both genomes likely acquired an ADP:ATP antiporter gene via horizontal gene transfer, an event that may have enabled their evolution as energy parasites by facilitating the acquisition of ATP from their host. These results on novel bacteria with highly reduced genomes expand our understanding of the phylogenetic and genomic diversities of endosymbiotic bacteria in protists.