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.