Unraveling the molecular mechanism of the response to changing ambient phosphorus in the dinoflagellate Alexandrium catenella with quantitative proteomics.

Phosphorus (P) is a key macronutrient limiting cell growth and bloom formation of marine dinoflagellates. Physiological responses to changing ambient P have been investigated in dinoflagellates; however, the molecular mechanisms behind these responses remain limited. Here, we compared the protein expression profiles of a marine dinoflagellate Alexandrium catenella grown in inorganic P-replete, P-deficient, and inorganic- and organic-P resupplied conditions using an iTRAQ-based quantitative proteomic approach. P deficiency inhibited cell growth and enhanced alkaline phosphatase activity (APA) but had no effect on photosynthetic efficiency. After P resupply, the P-deficient cells recovered growth rapidly and APA decreased. Proteins involved in sphingolipid metabolism, organic P utilization, starch and sucrose metabolism, and photosynthesis were up-regulated in the P-deficient cells, while proteins associated with protein synthesis, nutrient assimilation and energy metabolism were down-regulated. The responses of the P-deficient A. catenella to the resupply of organic and inorganic P presented significant differences: more biological processes were enhanced in the organic P-resupplied cells than those in the inorganic P-resupplied cells; A. catenella might directly utilize G-6-P for nucleic acid synthesis through the pentose phosphate pathway. Our results indicate that A. catenella has evolved diverse adaptive strategies to ambient P deficiency and specific mechanisms to utilize dissolved organic P, which might be an important reason resulting in A. catenella bloom in the low inorganic P environment. BIOLOGICAL SIGNIFICANCE: The ability of marine dinoflagellates to utilize different phosphorus (P) species and adapt to ambient P deficiency determines their success in the ocean. In this study, we investigated the response mechanisms of a dinoflagellate Alexandrium catenella to ambient P deficiency, and resupply of inorganic- and organic-P at the proteome level. Our results indicated that A. catenella initiated multiple adaptive strategies to ambient P deficiency, e.g. utilizing nonphospholipids and glycosphingolipids instead of phospholipids, enhancing expression of acid phosphatase to utilize organic P, and reallocating intracellular energy. Proteome responses of the P-deficient A. catenella to resupply of inorganic- and organic-P differed significantly, indicating different utilization pathways of inorganic and organic P, A. catenella might directly utilize low molecular weight organic P, such as G-6-P as both P and carbon sources.