The Complete Plastid Genomes of the Two ‘Dinotoms’ Durinskia baltica and Kryptoperidinium foliaceum

Abstract

BackgroundIn 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 FindingsHere 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/SignificanceThese 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.

Endosymbiotic Gene Transfer in Tertiary Plastid-Containing Dinoflagellates

“…On the other hand, the low level of EGT observed in dinotoms puts their endosymbiont on the periphery of the organelle definition, since it is fully integrated within the cell in many ways but not deeply integrated on a genetic level. Thus, in addition to challenging our view of how we define endosymbionts and organelles, this also reinforces the idea that dinotoms may represent an unusual intermediate in the continuum of symbiotic interactions observed in nature (51,105,106). …”

“…Exponentially growing cells were collected and ground as described previously (50). Cells lysis, RNA extractions, precipitations and purifications were performed for both species as described earlier (51). Total RNA for reverse transcription-PCR (RT-PCR) was obtained as described earlier (50).…”

What makes a chloroplast? Reconstructing the establishment of photosynthetic symbioses

“…The unusual genomes of redalgal-derived chloroplasts within many dinoflagellates probably have no more than 20 genes, so might have lost over 200 (Howe et al, 2008b). The haptophyte-derived chloroplasts of the dinoflagellate Karlodinium veneficum have lost over forty genes following endosymbiosis (Gabrielsen et al, 2011), whereas the diatom-derived chloroplasts of the dinoflagellates Kryptoperidinium foliaceum and Durinskia baltica have only lost three (Imanian et al, 2010). With a very few known exceptions, the nuclei and/or mitochondria of eukaryotic symbionts are not retained along with the secondary and tertiary chloroplasts (Archibald and Lane, 2009;Imanian et al, 2010;Johnson et al, 2007).…”

“…In most cases, the host lineage is believed to have originally been non-photosynthetic, but some examples are known in which a previously photosynthetic eukaryote acquired a new chloroplast lineage by serial replacement of the original chloroplast. Such serial endosymbioses gave rise to green algal-, haptophyte-and diatomderived chloroplasts in dinoflagellates, which ancestrally contained a red-algal-derived chloroplast (Gabrielsen et al, 2011;Imanian et al, 2010;Kim and Archibald, 2009;Minge et al, 2010).…”

Pigment compositions are linked to the habitat types in dinoflagellates

“…We treated 34 species (35 strains) of peridinin-type species and six species (ten strains) of dinoflagellates having diatom-derived chloroplasts; the latter dinoflagellates are collectively called 'dinotoms' (Imanian et al 2010). Dinotoms are known to possess chlorophylls c 1 and c 2 with fucoxanthin as the major xanthophyll (Mandelli 1968, Jeffery et al 1975, Withers et al 1977, Tamura et al 2005.…”