Dinoflagellates have drawn worldwide concerns as their large contributions to global primary production and negative impacts of harmful blooms to marine ecosystem. Although our understanding of dinoflagellate blooms has improved over the past half century, little is known about the biological processes occurring during the bloom period. Here, we focused on molecular mechanisms involved in bloom maintenance of a marine dinoflagelate Prorocentrum donghaiense with metatranscriptomics, metaproteomics and isotope techniques. In the blooming phases, an increasing abundance of proteins related to cell cycle, ribosome, carbon, nitrogen, phosphorus, sulfur and lipid metabolisms were observed, revealing active cell division and high nutrient usage. As the bloom grew so did competition for dwindling levels of dissolved nitrogen, phosphorus and CO2 in seawater. In addition to up-regulating the assimilation of inorganic nutrients, proteins responsible for acquisition and reallocation of external organic phosphomonoesters, fatty acids, peptides, amino acids and urea were highly expressed. The utilization of peptide, amino acid and urea largely relieved the stress posed by external dissolved CO2 limitation in the bloom environment. Interestingly, we successfully proved the existence of C4 pathway in P. donghaiense, and the methodical cooperation of carbonic anhydrase, C3 and C4 pathways minimized internal CO2 leakage and guaranteed efficient carbon fixation under low CO2 conditions. Moreover, a novel coupling of C4 cycle and amino acid assimilation was activated to meet the carbon and nitrogen demands. This study demonstrated the molecular behaviors of bloom-derived species from in situ environments and advanced our knowledge on the maintenance of phytoplankton blooms.