Phytoplankton face environmental nutrient variations that occur in the dynamic upper layers of the ocean. Phytoplankton cells are able to rapidly acclimate to nutrient fluctuations by adjusting their nutrient-uptake system and metabolism. Disentangling these acclimation responses is a critical step in bridging the gap between phytoplankton cellular physiology and community ecology. Here, we analyzed the dynamics of phosphate (P) uptake acclimation responses along different P temporal gradients by using batch cultures of the diatom Phaeodactylum tricornutum. We employed a multidisciplinary approach that combined nutrient-uptake bioassays, transcriptomic analysis, and mathematical models. Our results indicated that cells increase their maximum nutrient-uptake rate (Vmax) both in response to P pulses and strong phosphorus limitation. The upregulation of three genes coding for different P transporters in cells experiencing low intracellular phosphorus levels supported some of the observed Vmax variations. In addition, our mathematical model reproduced the empirical Vmax patterns by including two types of P transporters upregulated at medium-high environmental and low intracellular phosphorus levels, respectively. Our results highlight the existence of a sequence of acclimation stages along the phosphate continuum that can be understood as a succession of acclimation responses. We provide a novel conceptual framework that can contribute to integrating and understanding the dynamics and wide diversity of acclimation responses developed by phytoplankton.