Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics

Abstract

Dinoflagellates 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 earlybranching 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.dinoflagellates | phylogeny | theca | plastids | dinosterol D inoflagellates comprise approximately 2,400 named extant species, of which approximately half are photosynthetic (1). However, this represents a fraction of their estimated diversity: in surface marine waters, dinoflagellates are some of the most abundant and diverse eukaryotes known (2). Dinoflagellates' ecological significance befits their abundance: photosynthetic species are dominant marine primary producers, and phagotrophic species play an important role in the microbial loop through predation and nutrient recycling. Approximately 75-80% of the toxic eukaryotic phytoplankton species are dinoflagellates, and they cause shellfish poisoning and harmful algal blooms of global importance. Symbiotic genera like Symbiodinium participate in interactions with metazoans and are essential for the formation of reef ecosystems, and parasitic forms play a central role in the collapse of harmful algal blooms, including those caused by dinoflagellates themselves (3). Dinoflagellates synthesize important secondary metabolites including sterols, polyketides, toxins, and dimethylsulfide, and several of them have evolved bioluminescence. They ...

Phylogenetic placement of environmental sequences using taxonomically reliable databases helps to rigorously assess dinophyte biodiversity in Bavarian lakes (Germany)

“…Our reference tree comprising the known dinophycean sequence diversity is largely in agreement with previous rRNA approaches (Gu et al, 2013) as well as those based on excessive transcriptome sequence data (although using a much smaller taxon sample: Janouškovec et al, 2017;Price & Bhattacharya, 2017 sequencing amplicons. Our approach to determine dinophyte species using reference trees as inferred from multi-locus rRNA alignments is proven successful to a certain degree, at least for samples from the freshwater environment (providing also some new dinophyte records for Bavaria: Table 2), but also from the marine realm (Elferink et al, 2017;Wohlrab et al, 2018 The most frequently encountered taxa correspond to those that are known from morphological surveys in Bavaria, which comprise Apocalathium (Mauch et al, 2003;Mischke, Riedmüller, Hoehn, Deneke, & Nixdorf, 2015;Schaumburg, 1996), Ceratium (Mauch et al, 2003;Raeder, 1990;Schaumburg, 1996;Schaumburg & Hehl, 2001),…”

Ferredoxin-dependent bilin reductases in eukaryotic algae: Ubiquity and diversity

“…Dinoflagellates (Alveolata) are among the most abundant organisms in surface marine waters (Janouskovec et al, 2017). Photosynthetic dinoflagellates initially acquired photosynthesis via endosymbiosis of a rhodophyte, but the resulting secondary plastid has been replaced in some lineages.…”

“…Other dinoflagellates transiently acquire photosynthesis via kleptoplasty, as in Dinophysis acuminata . Phylotranscriptomic studies implicate both N. scintillans and D. acuminata as having lost functional red-derived plastids in the past (Janouskovec et al, 2017). …”

Deep in shadows, deep in time: the oldest mesophotic coral ecosystems from the Devonian of the Holy Cross Mountains (Poland)

“…However, these differences are minor and do not obscure the general interpretations presented here. It is unclear whether Paleozoic photosymbionts were dinoflagellates or other photosymbiotic microorganisms; therefore, any discussion of particular physiological adaptations for light harvesting at greater depths in the Paleozoic must remain speculative, especially because recent studies suggest that the origin of dinoflagellates might be post-Paleozoic (Janouškovec et al 2016). Similarly, the composition of photosynthetic pigments in symbionts remains unknown.…”