Abstract
Toxic dinoflagellates belonging to the genus Dinophysis acquire plastids indirectly from cryptophytes through the consumption of the ciliate Mesodinium rubrum. Dinophysis acuminata harbours three genes encoding plastid-related proteins, which are thought to have originated from fucoxanthin dinoflagellates, haptophytes and cryptophytes via lateral gene transfer (LGT). Here, we investigate the origin of these plastid proteins via RNA sequencing of species related to D. fortii. We identified 58 gene products involved in porphyrin, chlorophyll, isoprenoid and carotenoid biosyntheses as well as in photosynthesis. Phylogenetic analysis revealed that the genes associated with chlorophyll and carotenoid biosyntheses and photosynthesis originated from fucoxanthin dinoflagellates, haptophytes, chlorarachniophytes, cyanobacteria and cryptophytes. Furthermore, nine genes were laterally transferred from fucoxanthin dinoflagellates, whose plastids were derived from haptophytes. Notably, transcription levels of different plastid protein isoforms varied significantly. Based on these findings, we put forth a novel hypothesis regarding the evolution of Dinophysis plastids that ancestral Dinophysis species acquired plastids from haptophytes or fucoxanthin dinoflagellates, whereas LGT from cryptophytes occurred more recently. Therefore, the evolutionary convergence of genes following LGT may be unlikely in most cases.
Highlights
Plastids in photosynthetic dinoflagellates are classified into five types according to their origin[1]
Sequencing of Complementary DNA (cDNA) libraries of the cryptophyte alga Teleaulax amphioxeia, the ciliate M. rubrum and the dinoflagellate D. fortii using NextSeq 500 (Illumina Inc., San Diego, CA, USA) yielded a total of 44–110 million reads per species, which were deposited in the DNA Data Bank of Japan (DDBJ) Sequence Read Archive under accession numbers DRX131336–DRX131339, DRX131340– DRX131341 and DRX131342–DRX131343, respectively
3,365 gene ontology (GO) numbers were assigned to 39,850 amino acid sequences (10.7%), and 711 enzyme commission (EC) numbers were assigned to 10,328 amino acid sequences (2.8%) (Supplementary Table 1)
Summary
Plastids in photosynthetic dinoflagellates are classified into five types according to their origin[1]. Some photosynthetic dinoflagellates possess plastids originated from other eukaryotic alga. Plastids in some dinoflagellates (e.g. Dinophysis spp. and Nusuttodinium spp.) are derived from their photosynthetic prey through kleptoplasty[9,10,11], which is believed to have been the driving force behind the evolutionary transition towards the establishment of a permanent plastid. Dinophysis spp. acquire plastids of cryptophyte origin (kleptoplastids). Expression of genes related to cryptophyte plastid function and maintenance is lower in D. acuminata than in www.nature.com/scientificreports/. We sequenced D. fortii transcripts and identified proteins that are generally considered to functions in plastids. The origins of both newly identified and known D. acuminata proteins were analysed through phylogenetic studies. The findings of this study shed light on the evolutionary transition towards plastid retention in Dinophysis
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