Phosphorous (P) is a limiting macronutrient in many aquatic ecosystems. Phytoplankton, and especially the coccolithophorid Emiliania huxleyi, have remarkable physiological abilities to cope with phosphorous scarcity and to form vast blooms, which have important biogeochemical roles in the marine food webs. Internal phosphorous storages and enzymatic machinery of alkaline phosphatases (APs) and transporters enable E. huxleyi to successfully compete for phosphorous and supply its cellular demands. Despite their importance, little is known about cellular mechanisms that enable E. huxleyi’s acclimation under P-limitation. Here we demonstrate that molecular and structural membrane dynamics are involved in the survival response of P-limited cells. At the molecular level, the fraction of phospholipids out of the total membrane polar lipids dropped from ~30% to <5% under P-limitation, and was substituted for non-phosphorous containing lipids, such as sulfo- and betaine lipids. At the structural level, pronounced formation of intracellular vesicles and their trafficking to the vacuole were observed, suggesting the involvement of an autophagic-like process. Autophagy related genes were transiently induced, and vesicle acidification further supported the possible degradation of intracellular phosphorus containing components, which may sustain starved cells. However, understanding the regulatory mechanisms for AP, lipid remodeling and autophagy in phytoplankton is still in its infancy. Interestingly, the phosphatidylinositide 3-kinases (PI3K) inhibitor wortmannin reduced AP activity and phospholipid substitution, which may imply that PI3K signaling mediates different survival strategies during phosphate stress. Investigating the acclimation response of P-limited phytoplankton at the cellular level may provide insights regarding the ecophysiology of natural populations in the ocean.
