Dynamics of Photosynthesis in a Glycogen-Deficient glgC Mutant of Synechococcus sp. Strain PCC 7002

Abstract

c Cyanobacterial glycogen-deficient mutants display impaired degradation of light-harvesting phycobilisomes under nitrogenlimiting growth conditions and secrete a suite of organic acids as a putative reductant-spilling mechanism. This genetic background, therefore, represents an important platform to better understand the complex relationships between light harvesting, photosynthetic electron transport, carbon fixation, and carbon/nitrogen metabolisms. In this study, we conducted a comprehensive analysis of the dynamics of photosynthesis as a function of reductant sink manipulation in a glycogen-deficient glgC mutant of Synechococcus sp. strain PCC 7002. The glgC mutant showed increased susceptibility to photoinhibition during the initial phase of nitrogen deprivation. However, after extended periods of nitrogen deprivation, glgC mutant cells maintained higher levels of photosynthetic activity than the wild type, supporting continuous organic acid secretion in the absence of biomass accumulation. In contrast to the wild type, the glgC mutant maintained efficient energy transfer from phycobilisomes to photosystem II (PSII) reaction centers, had an elevated PSII/PSI ratio as a result of reduced PSII degradation, and retained a nitrogen-repletetype ultrastructure, including an extensive thylakoid membrane network, after prolonged nitrogen deprivation. Together, these results suggest that multiple global signals for nitrogen deprivation are not activated in the glgC mutant, allowing the maintenance of active photosynthetic complexes under conditions where photosynthesis would normally be abolished. Nitrogen is an essential macronutrient required for the synthesis of pigments, proteins, and nucleic acids in cyanobacteria. When nitrogen availability is limiting for cell growth and proliferation, a defined sequence of stress responses is deployed in most cyanobacteria. The immediate response is to increase the expression of genes associated with nitrogen uptake and assimilation (1-4). This is followed within hours by the cessation of growth and the mobilization of internal nitrogen stores through the degradation of the light-harvesting phycobilisomes, which contain nitrogen-rich phycobiliproteins and phycocyanin (5-7). Phycobilisome degradation also serves to reduce the light-harvesting cross section of the cell, thus avoiding excessive photon absorption, which can result in photooxidative damage in the absence of downstream metabolic oxidation reactions. The simultaneous activation of glycogen biosynthesis, degradation of thylakoid membranes, and reduction in the expression of genes associated with photosynthesis, carbon fixation, and de novo protein synthesis define the short-term acclimation events in response to nitrogen limitation (1-4). The longer-term acclimation in response to nitrogen limitation involves a decrease in metabolic activity to a minimum level that supports cell viability using energy derived from the catabolism of glycogen and cyclic electron transfer around photosystem I (PSI) (2, 3).The reductio...

Transcriptome and proteome analysis of nitrogen starvation responses in Synechocystis 6803 ΔglgC, a mutant incapable of glycogen storage

“…In the absence of glycogen synthesis, glycogen degradation genes are down-regulated. Contrary to a recent proposal [10] based on study in Synechococcus sp. PCC ΔglgC, there are clear similarities between Synechocystis ΔglgC and WT in transcriptional responses associated with nitrogen starvation, indicating that nitrogen status is indeed sensed by the mutant.…”

“…Jackson et al recently showed that remaining phycobilisomes in ΔglgC cells of Synechococcus sp. PCC 7002 remain coupled to Photosystem II [10]. This could indicate that the non-bleaching phenotype underlies a difference between the mutant and WT strains in energy distribution between PSII and PSI, which would possibly be reflected in the identity and abundance of extracellular metabolites that appear in nitrogen starved ΔglgC cultures.…”

“…These responses are relevant not only to biotechnological applications, but may offer insights into the regulation of cyanobacterial physiology. It was recently proposed that the non-bleaching phenotype and other morphological phenotypes in a glycogen-deficient strain of Synechococcus 7002 indicated that the strain is incapable of responding to nitrogen starvation, and the remaining phycobilisomes are shown to be functionally coupled to PSII [10].…”

Combinatorial deletions of glgC and phaCE enhance ethanol production in Synechocystis sp. PCC 6803

“…It has been reported that the photosystem II centers in a glgC mutant in Synechococcus sp. strain PCC 7002 were protected from degradation because they entered a quiescent under nitrogen starvation (Jackson et al, 2015). The contents of phycobilisome and chlorophyll were almost constant in the all strains in the presence of nitrogen.…”

Overexpression of bicarbonate transporters in the marine cyanobacterium Synechococcus sp. PCC 7002 increases growth rate and glycogen accumulation

“…Dry cell weight was measured as an earlier published protocol [35] with some modifications. Cell culture was centrifuged at 2500g for 10 min, and the pellet obtained was washed twice in 8.25 mM Tris-HCl buffer (pH 8.2).…”