Multifaceted Dinoflagellates and the Marine Model Prorocentrum cordatum

Abstract

Background: Dinoflagellates are a monophyletic group within the taxon Alveolata, which comprises unicellular eukaryotes. Dinoflagellates have long been studied for their organismic and morphologic diversity as well as striking cellular features. They have a main size range of 10‒100 µm, a complex "cell covering", exceptionally large genomes (~1‒250 Gbp with a mean of 50,000 protein-encoding genes) spread over a variable number of highly condensed chromosomes, and perform a closed mitosis with extranuclear spindles (dinomitosis). Photosynthetic, marine, and free-living Prorocentrum cordatum is a ubiquitously occurring, bloom-forming dinoflagellate and an emerging model system, particularly with respect to systems biology. Summary: Focused ion beam/scanning electron microscopy (FIB/SEM) analysis of P. cordatum recently revealed (i) a flattened nucleus with unusual structural features and a total of 62 tightly packed chromosomes, (ii) a single, barrel-shaped chloroplast devoid of grana and harboring multiple starch granules, (iii) a single, highly reticular mitochondrion, and (iv) multiple phosphate and lipid storage bodies. Comprehensive proteomics of subcellular fractions suggested (i) major basic nuclear proteins to participate in chromosome condensation, (ii) composition of nuclear pores to differ from standard knowledge, (iii) photosystems I and II, chloroplast complex I, and chlorophyll a–b binding light harvesting complex to form a large megacomplex (>1.5 MDa), and (iv) an extraordinary richness in pigment-binding proteins. Systems biology-level investigation of heat stress response demonstrated a concerted down-regulation of CO2-concentrating mechanisms, CO2-fixation, central metabolism, and monomer biosynthesis, which agrees with reduced growth yields. Key Messages: FIB/SEM analysis revealed new insights into the remarkable subcellular architecture of P. cordatum, complemented by proteogenomic unravelling of novel nuclear structures and a photosynthetic megacomplex. These recent findings are put in the wider context of current understanding of dinoflagellates.