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.2020 Mar 10;117(10):5364-5375.
doi: 10.1073/pnas.1911884117. Epub 2020 Feb 24.

Dinoflagellates with relic endosymbiont nuclei as models for elucidating organellogenesis

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Dinoflagellates with relic endosymbiont nuclei as models for elucidating organellogenesis

Chihiro Sarai et al. Proc Natl Acad Sci U S A..

Abstract

Nucleomorphs are relic endosymbiont nuclei so far found only in two algal groups, cryptophytes and chlorarachniophytes, which have been studied to model the evolutionary process of integrating an endosymbiont alga into a host-governed plastid (organellogenesis). However, past studies suggest that DNA transfer from the endosymbiont to host nuclei had already ceased in both cryptophytes and chlorarachniophytes, implying that the organellogenesis at the genetic level has been completed in the two systems. Moreover, we have yet to pinpoint the closest free-living relative of the endosymbiotic alga engulfed by the ancestral chlorarachniophyte or cryptophyte, making it difficult to infer how organellogenesis altered the endosymbiont genome. To counter the above issues, we need novel nucleomorph-bearing algae, in which endosymbiont-to-host DNA transfer is on-going and for which endosymbiont/plastid origins can be inferred at a fine taxonomic scale. Here, we report two previously undescribed dinoflagellates, strains MGD and TGD, with green algal endosymbionts enclosing plastids as well as relic nuclei (nucleomorphs). We provide evidence for the presence of DNA in the two nucleomorphs and the transfer of endosymbiont genes to the host (dinoflagellate) genomes. Furthermore, DNA transfer between the host and endosymbiont nuclei was found to be in progress in both the MGD and TGD systems. Phylogenetic analyses successfully resolved the origins of the endosymbionts at the genus level. With the combined evidence, we conclude that the host-endosymbiont integration in MGD/TGD is less advanced than that in cryptophytes/chrorarachniophytes, and propose the two dinoflagellates as models for elucidating organellogenesis.

Keywords: Pedinophyceae; endosymbiotic gene transfer; nucleomorph; plastid; secondary endosymbiosis.

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Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.
Morphology of undescribed dinoflagellate strains MGD (A–D) and TGD (E–H). (A andE) Cross sections of the cell under TEM, showing the dinoflagellate nucleus (DN), nucleomorph (Nm), plastid (Pl), and PPC. (B andF) Whole-cell light micrographs. (C andG) Enlarged image of a cross section of the cell under TEM observation. (D andH) Fluorescent microscopy with SYBER green I-staining image.
Fig. 2.
Fig. 2.
Scatter plots showing the distribution of GC% (A andB) and box plots for putative N-terminal extension (C andD) of the transcripts found in TGD (Left) and MGD (Right). (A andB) Thex andy axes show the GC% of first and third codon positions, respectively. Plots in green and orange represent the transcripts encoding the putative green algal and alveolate proteins, respectively. In both plots, green algal transcripts were divided into two populations based on GC%, and the ones with higher GC% overlapped with the masses of alveolate transcripts, which were presumably expressed from the dinoflagellate nuclear genomes. (C andD) Box plots of N-terminal extension of green algal transcripts with low and high GC%. Thex axes show lengths of putative N-terminal extensions (seeMaterial and Methods).P values displayed in the plots were calculated based on the Wilcoxon rank-sum test.
Fig. 3.
Fig. 3.
ML trees for the green algal orthologous proteins with distinct GC%. The numbers above branches show nonparametric ML bootstrap values. Only ML bootstrap support values greater than 50% are shown on the corresponding branches.
Fig. 4.
Fig. 4.
ML tree inferred from eukaryotic small subunit ribosomal RNA (18S rRNA) sequences. All of the taxon names are omitted except MGD, TGD, and Pedinophyceae green algae. Taxon labels of red and green algae per Adl et al. (89). Only ML bootstrap support values greater than 80% are shown on the corresponding branches. The branches supported by BPPs greater than 0.95 are shown as thick lines. The clade comprising MGD, TGD, and Pedinophyceae green algae inferred from plastidal small subunit rRNA (16S rRNA) sequences is shown in the box. The 16S rRNA tree includingL. chlorophorum with full taxon names is provided asSI Appendix, Fig. S10.
Fig. 5.
Fig. 5.
ML tree inferred from a 75-protein alignment. The topology in question was emphasized. The 75-protein alignment contains 21,042 amino acid positions. The tree topology was generated by a ML analysis with the LG + Γ + F + C60 model. Nonparametric ML bootstrap support values (shown above the nodes) were calculated from 100 replicates with the LG + Γ + F + PMSF model. The nodes highlighted by closed dots were supported fully by nonparametric bootstrap analyses. Only bootstrap support values greater than 70% are shown.
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