Plastid genome-based phylogeny pinpointed the origin of the green-colored plastid in the dinoflagellate Lepidodinium chlorophorum

Abstract

Unlike many other photosynthetic dinoflagellates, whose plastids contain a characteristic carotenoid peridinin, members of the genus Lepidodinium are the only known dinoflagellate species possessing green alga-derived plastids. However, the precise origin of Lepidodinium plastids has hitherto remained uncertain. In this study, we completely sequenced the plastid genome of Lepidodinium chlorophorum NIES-1868. Our phylogenetic analyses of 52 plastid-encoded proteins unite L. chlorophorum exclusively with a pedinophyte, Pedinomonas minor, indicating that the green-colored plastids in Lepidodinium spp. were derived from an endosymbiotic pedinophyte or a green alga closely related to pedinophytes. Our genome comparison incorporating the origin of the Lepidodinium plastids strongly suggests that the endosymbiont plastid genome acquired by the ancestral Lepidodinium species has lost genes encoding proteins involved in metabolism and biosynthesis, protein/metabolite transport, and plastid division during the endosymbiosis. We further discuss the commonalities and idiosyncrasies in genome evolution between the L. chlorophorum plastid and other plastids acquired through endosymbiosis of eukaryotic photoautotrophs.

Keywords: Lepidodinium; Pedinophyceae; genome reduction; plastid replacement; secondary plastids.

Fig. 1.—

Complete plastid genome of Lepidodinium chlorophorum and ML phylogeny inferred from an alignment comprising 52 plastid proteins. (A) Physical map of the L. chlorophorum plastid genome. Protein-coding and rRNA-coding regions are shown by gray and closed boxes, respectively; tRNAs and pseudogenes are shown by lines. Tandemly duplicated regions were highlighted in light blue and dark blue. Two ORFs generated by gene fusion are colored in pink (see supplementary fig. S1, Supplementary Material online, for the details). Red arrowheads indicate physically overlapping coding regions (see supplementary fig. S2, Supplementary Material online, for the details). Group II introns are depicted as yellowish green boxes (see supplementary fig. S3, Supplementary Material online, for the details). A single UAA and two UAG codons found within the rpoC1 coding region are shown by an open circle and open diamonds, respectively (see supplementary fig. S4, Supplementary Material online, for the details). (B) Phylogenetic analysis exploring the origin of the L. chlorophorum plastid. The alignment comprises 52 plastid proteins (8,917 amino acid positions in total) sampled from 26 genomes of 23 green algae and 3 green alga-derived plastids. Phylogenetic analyses were performed by both ML and Bayesian frameworks. As both methods reconstructed very similar trees, only the ML tree is shown here. BPPs and ML bootstrap values (MLBPs) are shown above and below the corresponding nodes. MLBPs less than 80% and BPPs less than 0.95 are omitted from the figure. Dots correspond to MLBPs of 100% and BPPs of 1.00. The MLBP from the analysis excluding rapidly evolving Bigelowiella natans and Euglena gracilis is shown in parentheses.

Fig. 2.—

Venn diagram of the gene contents in the plastid genomes of Lepidodinium chlorophorum and Pedinomonas minor. This diagram illuminates that the protein-coding gene set in L. chlorophorum is the subset of that of P. minor. rpoC1 is highlighted by an asterisk, as this ORF is disrupted by multiple stop codons. Genes encoding proteins involved in metabolism, plastid division, translation, transcription, transport, and photosynthesis are shown in red, magenta, purple, yellow, brown, and white, respectively.