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. 2017 Oct 12;7(1):13075.
doi: 10.1038/s41598-017-13578-8.

Genomic divergence within non-photosynthetic cyanobacterial endosymbionts in rhopalodiacean diatoms

Takuro Nakayama  1   2 , Yuji Inagaki  3
Affiliations

Genomic divergence within non-photosynthetic cyanobacterial endosymbionts in rhopalodiacean diatoms

Takuro Nakayama et al. Sci Rep. .

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.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1
The spheroid body genome of Rhopalodia gibberula and comparison with the spheroid body genome of Epithemia turgida. (a) Map of the circular chromosome of the spheroid body of the diatom Rhopalodia gibberula (RgSB). Dark and light green bars in the outermost and second outermost circles show the positions of protein-coding genes on the plus and minus strands, respectively. The two circles also contain rRNA gene clusters shown by red bars. The bars on the second innermost circle indicate pseudogenes, and the innermost circle shows the GC content (window size: 5,000 bp). (b) Whole-genome comparison between the RgSB and Epithemia turgida spheroid body (EtSB). The RgSB genome sequence was aligned based on the EtSB genome sequence. Syntenic regions between the two genomes are colour-coded. The regions coloured in purple, dark green, light green and dark blue were found to be inverted in the RgSB genome relative to the EtSB genome. (c) Comparison of the unique KEGG orthology (KO) ID repertoire of the RgSB and EtSB genomes. The numbers in parentheses indicate the total number of unique KO IDs in each genome.
Figure 2
Figure 2
Chlorophyll a and vitamin B12 biosynthetic pathways in the spheroid bodies of Rhopalodia gibberula (RgSB) and Epithemia turgida (EtSB). (a) Pathways for chlorophyll a and vitamin B12 biosynthesis. Each arrow indicates a single reaction. Gene names corresponding to each reaction are displayed. The step indicated by a dashed grey arrow is catalysed by cobyrinic acid a,c-diamide reductase (encoded by cobR) in diverse photosynthetic organisms, but this gene was not detected in the genome of the RgSB, EtSB, or their close free-living relatives (i.e. Cyanothece spp.). (b) Status of genes for the chlorophyll a and vitamin B12 biosynthetic pathways in the RgSB and EtSB genomes. A filled box indicates the presence of an intact gene, whereas a box with a X mark and a blank box designate the presence of a pseudogene and the absence of a gene, respectively.
Figure 3
Figure 3
Overall difference in non-synonymous substitution rates between the Rhopalodia gibberula spheroid body (RgSB) and Epithemia turgida spheroid body (EtSB) genomes. For each orthologous pair of the EtSB and RgSB genes, non-synonymous substitution rates (dN values) were estimated, and then the difference between the two corresponding dN values (ΔdN) were calculated. To calculate ΔdN, the dN values of a EtSB gene was subtracted from the value of the corresponding gene in the RgSB genome. The mean of the total ΔdN values was -0.0101 (indicated by a solid line). Outliers were not included in this histogram.
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