Another layer: The Karenia brevis plastid transcriptome expands the complex story of dinoflagellate RNA processing and tertiary endosymbiosis.

Abstract

Dinoflagellates are a diverse group of protists, which possess the ability to modify their genomic information at a rapid rate compared to other eukaryotes. When adding plastid organelles via endosymbiosis, the genome of the endosymbiont can also be modified by means such as fragmentation into circular chromosomes (minicircles), reorganization of protein structure, and transference of more of their photosynthesis genes to the nucleus than any other eukaryote. Due to being "suited" for endosymbiotic acquisition of organelles, the dinoflagellate family exhibits three distinct plastid types, two of which use chlorophyll a along with peridinin and fucoxanthin, respectively. The third plastid type is found in Lepidodinium, and appears to be derived from a chlorophyte inclusion, as it uses chlorophylls a and b. At this time, the peridinin dinoflagellates have been better studied than the fucoxanthin lineages such as Karenia brevis and Karlodinium veneficum. Although comparative studies have found phylogenetic evidence of similarities between the peridinin and fucoxanthin dinoflagellates, conflicting results and a significant body of empirical evidence suggests substantial differences between them in the areas of genome and membrane structure. In this study, we have used Illumina RNA sequencing to produce the most complete plastid transcriptome of Karenia brevis to date. We have analyzed the transcript structure and noted a number of dinoflagellate hallmarks, such as polyuridylation of the 3' end of mRNAs, and loss of consensus start codons. We have also identified evidence of polyadenylation of the 5' end of protein coding transcripts, which has not been reported so far. Six of the protein sequences produced were used to conduct a comparative phylogenetic analysis, which has identified both previously known, and unreported similarities, between the peridinin and fucoxanthin dinoflagellates, including shared instances of consensus loss when compared to broad group of reference taxa. We have also found discrete instances of invariant site substitution preferences, which are shared between these groups. These findings do not support previous studies that have suggested a common lineage for these groups, but further elucidate a complex pattern of endosymbiont genome modifications associated with the dinoflagellate host cell.