The complete plastid genomes of the two 'dinotoms' Durinskia baltica and Kryptoperidinium foliaceum

Abstract

Background: In one small group of dinoflagellates, photosynthesis is carried out by a tertiary endosymbiont derived from a diatom, giving rise to a complex cell that we collectively refer to as a 'dinotom'. The endosymbiont is separated from its host by a single membrane and retains plastids, mitochondria, a large nucleus, and many other eukaryotic organelles and structures, a level of complexity suggesting an early stage of integration. Although the evolution of these endosymbionts has attracted considerable interest, the plastid genome has not been examined in detail, and indeed no tertiary plastid genome has yet been sequenced.

Methodology/principal findings: Here we describe the complete plastid genomes of two closely related dinotoms, Durinskia baltica and Kryptoperidinium foliaceum. The D. baltica (116470 bp) and K. foliaceum (140426 bp) plastid genomes map as circular molecules featuring two large inverted repeats that separate distinct single copy regions. The organization and gene content of the D. baltica plastid closely resemble those of the pennate diatom Phaeodactylum tricornutum. The K. foliaceum plastid genome is much larger, has undergone more reorganization, and encodes a putative tyrosine recombinase (tyrC) also found in the plastid genome of the heterokont Heterosigma akashiwo, and two putative serine recombinases (serC1 and serC2) homologous to recombinases encoded by plasmids pCf1 and pCf2 in another pennate diatom, Cylindrotheca fusiformis. The K. foliaceum plastid genome also contains an additional copy of serC1, two degenerate copies of another plasmid-encoded ORF, and two non-coding regions whose sequences closely resemble portions of the pCf1 and pCf2 plasmids.

Conclusions/significance: These results suggest that while the plastid genomes of two dinotoms share very similar gene content and genome organization with that of the free-living pennate diatom P. tricornutum, the K. folicaeum plastid genome has absorbed two exogenous plasmids. Whether this took place before or after the tertiary endosymbiosis is not clear.

Figure 1. The plastid genome maps of Durinskia baltica and Kryptoperidinium foliaceum.

Functionally related genes are indicated by color and transcriptional direction is indicated by boxes outside the ring (clockwise) or inside the ring (counterclockwise). Genes for tRNAs are indicated by their single letter code. The large single copy (LSC), small single copy (SSC), and inverted repeats (IRa and IRb) are shown on the inner circle. Roman numerals (I-IX) mark the locations of 9 distinct regions in the plastid genome of K. foliaceum.

Figure 2. Conserved ordered gene blocks among three plastid genomes.

All possible two-way comparisons between plastid genomes of K. foliaceum, D. baltica, and P. tricornutum. Conserved blocks of genes are indicated by color, inversions are marked by a black triangle, inversions/translocations by a hexagon, translocations by a rectangle, missing genes by a black circle and insertions by Roman numerals I-IX.