Phosphorus Feast and Famine in Cyanobacteria: Is Luxury Uptake of the Nutrient Just a Consequence of Acclimation to Its Shortage?

Abstract

To cope with fluctuating phosphorus (P) availability, cyanobacteria developed diverse acclimations, including luxury P uptake (LPU)-taking up P in excess of the current metabolic demand. LPU is underexplored, despite its importance for nutrient-driven rearrangements in aquatic ecosystems. We studied the LPU after the refeeding of P-deprived cyanobacterium <i>Nostoc</i> sp. PCC 7118 with inorganic phosphate (P<i>_i</i>), including the kinetics of P<i>_i</i> uptake, turnover of polyphosphate, cell ultrastructure, and gene expression. The P-deprived cells deployed acclimations to P shortage (reduction of photosynthetic apparatus and mobilization of cell P reserves). The P-starved cells capable of LPU exhibited a biphasic kinetic of the P<i>_i</i> uptake and polyphosphate formation. The first (fast) phase (1-2 h after P<i>_i</i> refeeding) occurred independently of light and temperature. It was accompanied by a transient accumulation of polyphosphate, still upregulated genes encoding high-affinity P<i>_i</i> transporters, and an ATP-dependent polyphosphate kinase. During the second (slow) phase, recovery from P starvation was accompanied by the downregulation of these genes. Our study revealed no specific acclimation to ample P conditions in <i>Nostoc</i> sp. PCC 7118. We conclude that the observed LPU phenomenon does not likely result from the activation of a mechanism specific for ample P conditions. On the contrary, it stems from slow disengagement of the low-P responses after the abrupt transition from low-P to ample P conditions.