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

Alexei Solovchenko,Elena Lobakova,Olga Baulina,Svetlana Vasilieva,Elizaveta Vinogradova,Alexandr Lukyanov,Tatiana Pugacheva,Olga Chivkunova,Olga Gorelova,Pavel Scherbakov,Olga Karpova,Larisa Semenova,Irina Selyakh

doi:10.3390/cells9091933

Alexei Solovchenko, Elena Lobakova + Show 11 more

Open Access

https://doi.org/10.3390/cells9091933

Copy DOI

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 Nostoc sp. PCC 7118 with inorganic phosphate (Pi), including the kinetics of Pi 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 Pi uptake and polyphosphate formation. The first (fast) phase (1–2 h after Pi refeeding) occurred independently of light and temperature. It was accompanied by a transient accumulation of polyphosphate, still upregulated genes encoding high-affinity Pi 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 Nostoc 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.

Highlights

Phosphorus (P) is an important nutrient central to storing and the exchange of energy and information in the cell [1,2]
We attempted to obtain a deeper insight into luxury P uptake (LPU) through the analysis of changes in the cell ultrastructure and gene expression displayed by the cyanobacterium Nostoc sp
The effects of the added Pi concentration, light, and temperature recorded in this study suggest that this phase of luxury Pi uptake reflects the operation of a passive transport requiring no energy input in the form of ATP

Summary

Introduction

Phosphorus (P) is an important nutrient central to storing and the exchange of energy and information in the cell [1,2]. The availability of P in many habitats dwelled by cyanobacteria is scarce and/or fluctuating. Cyanobacteria developed a broad array of acclimations to cope with P shortage. One of the most widespread is the capability of taking up P in large excess of the current metabolic demand, termed “luxury P uptake” (LPU) [3]. The ability of the P-deprived culture to accumulate excessive amounts of inorganic polyphosphate (PolyP) after refeeding with Pi is known as “hyper-compensation” or “phosphate overplus” [4,5].

Methods

Results

Discussion

Conclusion