Metaproteomics reveals the molecular mechanism underlying bloom maintenance of a marine dinoflagellate under low ambient CO₂ and inorganic nutrients

Dinoflagellate blooming periods are paradoxically characterized by high biomass growth rate and low ambient dissolved CO₂ and inorganic nutrients, however, the underlying mechanisms linking cell growth and nutrient acquisition are poorly understood. Here, we compared metaproteomes of non-bloom, mid-blooming and late-blooming cells of a marine dinoflagellate Prorocentrum donghaiense. Cell division, metabolism of carbon, nitrogen, phosphorus, lipid, porphyrin and chlorophyll were more active in blooming cells than in non-bloom cells. Up-regulation of carbonic anhydrase, ribulose-1,5-bisphosphate carboxylase/oxygenase II, and C₄-cycle proteins enhanced CO₂ assimilation of P. donghaiense. Proteins participating in external organic nutrient acquisition and conversion, such as transporters for fatty acids, peptides and amino acids, external- and internal-phosphomonoester hydrolase, and diverse peptidases and amino acid transaminases, exhibited higher expression in blooming cells relative to non-bloom cells. Interestingly, dissolved organic nitrogen (DON) such as urea and aspartate significantly down-regulated expression and activity of carbon assimilation proteins except for RuBisCO form II, suggesting that DON provided sufficient carbon source which reduced the need to concentrate internal CO₂. This study demonstrates that coupling of efficient CO₂ assimilation with DON utilization are essential for bloom maintenance of P. donghaiense, and future efforts should be devoted to dissolved organic nutrients for prevention and management of dinoflagelllate blooms.