Transcriptomic response to changing ambient phosphorus in the marine dinoflagellate Prorocentrum donghaiense

Dinoflagellates represent major contributors to the harmful algal blooms in the oceans. Phosphorus (P) is an essential macronutrient that limits the growth and proliferation of dinoflagellates. However, the specific molecular mechanisms involved in the P acclimation of dinoflagellates remain poorly understood. Here, the transcriptomes of a dinoflagellate Prorocentrum donghaiense grown under inorganic P-replete, P-deficient, and inorganic- and organic P-resupplied conditions were compared. Genes encoding low- and high-affinity P transporters were significantly down-regulated in the P-deficient cells, while organic P utilization genes were significantly up-regulated, indicating strong ability of P. donghaiense to utilize organic P. Up-regulation of membrane phospholipid catabolism and endocytosis provided intracellular and extracellular organic P for the P-deficient cells. Physiological responses of P. donghaiense to dissolved inorganic P (DIP) or dissolved organic P (DOP) resupply exhibited insignificant differences. However, the corresponding transcriptomic responses significantly differed. Although the expression of multiple genes was significantly altered after DIP resupplementation, few biological processes varied. In contrast, various metabolic processes associated with cell growth, such as translation, transport, nucleotide, carbohydrate and lipid metabolisms, were significantly altered in the DOP-resupplied cells. Our results indicated that P. donghaiense evolved diverse DOP utilization strategies to adapt to low P environments, and that DOPs might play critical roles in the P. donghaiense bloom formation.