Abstract
Organelle acquisitions via endosymbioses with prokaryotes were milestones in the evolution of eukaryotes. Still, quite a few uncertainties have remained for the evolution in the early stage of organellogenesis. In this respect, rhopalodiacean diatoms and their obligate cyanobacterial endosymbionts, called spheroid bodies, are emerging as new models for the study of organellogenesis. The genome for the spheroid body of Epithemia turgida, a rhopalodiacean diatom, has unveiled its unique metabolic nature lacking the photosynthetic ability. Nevertheless, the genome sequence of a spheroid body from a single lineage may not be sufficient to depict the evolution of these cyanobacterium-derived intracellular structures as a whole. Here, we report on the complete genome for the spheroid body of Rhopalodia gibberula, a lineage distinct from E. turgida, of which genome has been fully determined. Overall, features in genome structure and metabolic capacity, including a lack of photosynthetic ability, were highly conserved between the two spheroid bodies. However, our comparative genomic analyses revealed that the genome of the R. gibberula spheroid body exhibits a lower non-synonymous substitution rate and a slower progression of pseudogenisation than those of E. turgida, suggesting that a certain degree of diversity exists amongst the genomes of obligate endosymbionts in unicellular eukaryotes.
Highlights
Photosynthesis and aerobic respiration were introduced to eukaryotes through the acquisition of plastids and mitochondria, respectively
The spheroid body genomes have been rearranged during the divergence of rhopalodiacean diatoms, as inversions and/or translocations were detected between the two spheroid body genomes (Fig. 1b). 1,671 and 1,720 open reading frames (ORFs) were predicted in the Rhopalodia gibberula spheroid body (RgSB) and Epithemia turgida spheroid body (EtSB) genomes (Tables S1 and S2), respectively, and 60.3 and 54.5% of the predicted ORFs (i.e. 1,007 and 937 ORFs) in the RgSB and EtSB genomes, respectively, were assigned into any of functional categories in the Kyoto Encyclopedia of Genes and Genomes (KEGG) orthology (KO)
We found that the majority of KO IDs from the RgSB and EtSB genomes were shared between the two genomes (844 out of 909 and 849, respectively; Fig. 1c)
Summary
Photosynthesis and aerobic respiration were introduced to eukaryotes through the acquisition of plastids and mitochondria, respectively. As both mitochondria and plastids have already been established as organelles, the systems for maintenance and functions of the two organelles in modern eukaryotes most likely retained little information regarding the early process of organellogenesis In this respect, unicellular eukaryotic cells hosting bacterial intracellular symbionts have been paid attention as new model systems to study organellogenesis[1,2]. The spheroid bodies are obligate endosymbionts, as these structures have never been cultivated outside of the host cells[8] and are passed to the daughter cells through binary cell division[10,11] Both host (diatom) and symbiont (cyanobacteria) phylogenies suggested that the endosymbiosis of a nitrogen-fixing cyanobacterium, which later gave rise to the spheroid body, was established in the common ancestor of species in genera Rhopalodia and Epithemia, and inherited throughout the host speciation[6]. The detailed comparison between the E. turgida and R. gibberula spheroid body genomes provided new insights into the genome evolution of the obligate cyanobacterial endosymbiont in rhopalodiacean diatoms
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