The Complex Regulation of the Phosphate Uptake System of Cyanobacteria

Abstract

Owing to the capacity of cyanobacteria to adapt physiologically to alterations of the environmental phosphate concentration, the phosphate uptake system exhibits complex bioenergetic properties under phosphate deficient growth conditions. Physiological adaptation to changes in the external phosphate concentration affects two energy dependent processes, namely the transport of phosphate through the cell membrane and the subsequent conversion of internal phosphate to ATP, which is in equilibrium with polyphosphates. In adapted states the energetic and kinetic properties of the phosphate transport system and the ATPsynthase are conformed to each other, such that energy dissipation is minimal under the prevailing growth conditions. Due to this energetic constraint, any persistent change in the external phosphate concentration provokes a reconstruction of the two energy converting subsystems, directed towards emergence of a new and energetically efficient adapted state.

The complex adaptive features of the uptake system are revealed when the physiological response to changes in phosphate supply is dissected into a sequence of individual adaptive events. In each of these events the uptake system passes, via an adaptive operation mode, from one adapted state to the next. During every adaptive operation mode the outcome of the antecedent adaptation to elevated phosphate concentrations guides the emergence of the subsequent adapted state in a distinct manner. The resulting connectivity of adaptive events is the basis for information processing about external phosphate fluctuations, enabling cyanobacteria to transcribe different patterns of phosphate fluctuations into varying adaptive responses. Information about alterations in phosphate supply can then even be transferred to daughter generations.

Using non equilibrium thermodynamics to analyze the adaptive self-organization process, we show that adapted states are characterized by an extended range of validity, over which there is a linear dependence of the uptake rate on the driving force of this process. In contrast, during adaptive operation modes, in which an alteration in the external phosphate concentration is “interpreted” in the light of environmental phosphate fluctuations, experienced by the cells in the past, the uptake rate depends on the driving force in a non linear manner.