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TitleMajor transitions in dinoflagellate evolution unveiled by phylotranscriptomics
AuthorJanouskovek, J; Gavelis, G S; Burki, F; Dinh, D; Bachvaroff, T R; Gornik, S G; Bright, K J; Imanian, B; Strom, S L; Delwiche, C F; Waller, R F; Fensome, R A; Leander, B S; Rohwer, F L; Saldarriaga, J F
SourceProceedings of the National Academy of Sciences of the United States of America vol. 114, no. 2, 2016 p. E171-E180,
Alt SeriesEarth Sciences Sector, Contribution Series 20160099
Mediapaper; on-line; digital
File formatpdf
Subjectsmarine geology; environmental geology; phylogeny; taxonomy; biogeochemistry; fossils; microfossils; Dinoflagellates
Illustrationscharts; paleontological drawings; graphs; tables
ProgramBaffin Petroleum Systems, GEM2: Geo-mapping for Energy and Minerals
AbstractDinoflagellates are key species in marine environments, but they remain poorly understood in part because of their large, complex genomes, unique molecular biology, and unresolved in-group relationships. We created a taxonomically representative dataset of dinoflagellate transcriptomes and used this to infer a strongly supported phylogeny to map major morphological and molecular transitions in dinoflagellate evolution. Our results show an early-branching position of Noctiluca, monophyly of thecate (plate-bearing) dinoflagellates, and paraphyly of athecate ones. This represents unambiguous phylogenetic evidence for a single origin of the group’s cellulosic theca, which we show coincided with a radiation of cellulases implicated in cell division. By integrating dinoflagellate molecular, fossil, and biogeochemical evidence, we propose a revised model for the evolution of thecal tabulations and suggest that the late acquisition of dinosterol in the group is inconsistent with dinoflagellates being the source of this biomarker in pre-Mesozoic strata. Three distantly related, fundamentally nonphotosynthetic dinoflagellates, Noctiluca, Oxyrrhis, and Dinophysis, contain cryptic plastidial metabolisms and lack alternative cytosolic pathways, suggesting that all free-living dinoflagellates are metabolically dependent on plastids. This finding led us to propose general mechanisms of dependency on plastid organelles in eukaryotes that have lost photosynthesis; it also suggests that the evolutionary origin of bioluminescence in nonphotosynthetic dinoflagellates may be linked to plastidic tetrapyrrole biosynthesis. Finally, we use our phylogenetic framework to show that dinoflagellate nuclei have recruited DNA-binding proteins in three distinct evolutionary waves, which included two independent acquisitions of bacterial histone-like proteins.
Summary(Plain Language Summary, not published)
A full understanding of the evolution of dinoflagellates is necessary to permit better utilization in biostratigraphic and paleoenvironmental research in basin analysis studies. Collaboration with biologists ensures that the fossil record is taken into account in modern studies of dinoflagellate evolution, which is dominated nowadays by molecular phylogeneticists. Previous phylogenetic molecular studies have focused on particular RNA molecules and have not agreed in some important particulars with the evolution of the group as indicated by the fossil record. This study for the first time uses another type of molecules, known as transcriptomes, for evolutionary analysis. This method shows strong agreement with predictions from the fossil record. It supports an initial major radiation of dinoflagellates during the early Mesozoic, as we see in the fossil record, and suggests that supposed Paleozoic biochemical biomarkers in the Paleozoic, previously thought to be from dinoflagellates, were in all probability derived from non-dinoflagellate organisms.