Morphology, behavior, and phylogenomics of Oxytoxum lohmannii, Dinoflagellata.

Dinoflagellates are an abundant and diverse group of protists representing a wealth of unique biology and ecology. While many dinoflagellates are photosynthetic or mixotrophic, many taxa are heterotrophs, often with complex feeding strategies. Compared to their photosynthetic counterparts, heterotrophic dinoflagellates remain understudied, as they are difficult to culture. One exception, a long-cultured isolate originally classified as Amphidinium but recently reclassified as Oxytoxum, has been the subject of a number of feeding, growth, and chemosensory studies. This lineage was recently determined to be closely related to Prorocentrum using phylogenetics of ribosomal RNA gene sequences, but the exact nature of this relationship remains unresolved. Using transcriptomes sequenced from culture and three single cells from the environment, we produce a robust phylogeny of 242 genes, revealing Oxytoxum is likely sister to the Prorocentrum clade, rather than nested within it. Molecular investigations uncover evidence of a reduced, nonphotosynthetic plastid and proteorhodopsin, a photoactive proton pump acquired horizontally from bacteria. We describe the ultrastructure of O. lohmannii, including densely packed trichocysts, and a new type of mucocyst. We observe that O. lohmannii feeds preferentially on cryptophytes using myzocytosis, but can also feed on various phytoflagellates using conventional phagocytosis. O. lohmannii is amenable to culture, providing an opportunity to better study heterotrophic dinoflagellate biology and feeding ecology.

Contrasting effects of high-intensity photosynthetically active radiation on two bloom-forming dinoflagellates.

While light limitation can inhibit bloom formation in dinoflagellates, the potential for high-intensity photosynthetically active radiation (PAR) to inhibit blooms by causing stress or damage has not been well-studied. We measured the effects of high-intensity PAR on the bloom-forming dinoflagellates Alexandrium fundyense and Heterocapsa rotundata. Various physiological parameters (photosynthetic efficiency Fv /Fm , cell permeability, dimethylsulfoniopropionate [DMSP], cell volume, and chlorophyll-a content) were measured before and after exposure to high-intensity natural sunlight in short-term light stress experiments. In addition, photosynthesis-irradiance (P-E) responses were compared for cells grown at different light levels to assess the capacity for photophysiological acclimation in each species. Experiments revealed distinct species-specific responses to high PAR. While high light decreased Fv /Fm in both species, A. fundyense showed little additional evidence of light stress in short-term experiments, although increased membrane permeability and intracellular DMSP indicated a response to handling. P-E responses further indicated a high light-adapted species with Chl-a inversely proportional to growth irradiance and no evidence of photoinhibition; reduced maximum per-cell photosynthesis rates suggest a trade-off between photoprotection and C fixation in high light-acclimated cells. Heterocapsa rotundata cells, in contrast, swelled in response to high light and sometimes lysed in short-term experiments, releasing DMSP. P-E responses confirmed a low light-adapted species with high photosynthetic efficiencies associated with trade-offs in the form of substantial photoinhibition and a lack of plasticity in Chl-a content. These contrasting responses illustrate that high light constrains dinoflagellate community composition through species-specific stress effects, with consequences for bloom formation and ecological interactions within the plankton.

Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics.

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 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.