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

Behzad Imanian,Jean-François Pombert,Patrick J Keeling,Anita Brandstaetter

doi:10.1371/journal.pone.0010711

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.

Highlights

The path of plastid evolution has been neither simple nor linear, but rather full of twists and turns
In tertiary endosymbiosis an alga with a secondary plastid is taken up by another eukaryote, and to date the only lineage known to take up tertiary plastids is dinoflagellates, where tertiary plastids derived from three different lineages are known: Karenia and Karlodinium species with plastids derived from a haptophyte [7,10]; Dinophysis species with cryptophyte derived-plastids [11,12,13]; and a small but growing group of dinoflagellates harboring a diatom endosymbiont [14,15,16,17,18], which we refer to as dinotoms
The D. baltica and K. foliaceum plastid genomes (Figure 1) map as circular molecules divided into large single-copy (LSC) and small single-copy (SSC) regions by the two inverted repeats (IRs), a quadripartite structure that is common to many other algal plastid genomes including the pennate and centric diatoms P. tricornutum and Thalassiosira pseudonana, respectively [41]

Summary

Introduction

The path of plastid evolution has been neither simple nor linear, but rather full of twists and turns. After the divergence of glaucophytes, red and green algae following primary endosymbiosis, plastids spread by the secondary and tertiary uptake of these eukaryotic algae by new eukaryotic hosts [1,2,3,4]. The products of many of these genes would be targeted to the plastid, which necessitated the development of a new protein targeting system to direct the protein products back to their correct location [8,9] These processes have been most thoroughly studied in primary and secondary plastids, but tertiary endosymbioses add another layer of complexity to the process. The evolution of these endosymbionts has attracted considerable interest, the plastid genome has not been examined in detail, and no tertiary plastid genome has yet been sequenced

Methods

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Conclusion