Nitrogen Starvation-Induced Chlorosis in Synechococcus PCC 7942. Low-Level Photosynthesis As a Mechanism of Long-Term Survival (original) (raw)
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Physiologia Plantarum, 2012
Sequential adaptation to nitrogen deprivation and ultimately to full starvation requires coordinated adjustment of cellular functions. We investigated changes in gene expression and cell physiology of the cyanobacterium Synechocystis PCC 6803 during 96 h of nitrogen starvation. During the first 6 h, the transcriptome showed activation of nitrogen uptake and assimilation systems and of the core nitrogen and carbon assimilation regulators. However, the nitrogen-deprived cells still grew at the same rate as the control and even showed transiently increased expression of phycobilisome genes. After 12 h, cell growth decreased and chlorosis started with degradation of the nitrogen-rich phycobilisomes. During this phase, the transcriptome showed suppression of genes for phycobilisomes, for carbon fixation and for de novo protein synthesis. Interestingly, photosynthetic activity of both photosystem I (PSI) and photosystem II was retained quite well. Excess electrons were quenched by the induction of terminal oxidase and hydrogenase genes, compensating for the diminished carbon fixation and nitrate reduction activity. After 48 h, the cells ceased most activities. A marked exception was the retained PSI gene transcription, possibly this supports the viability of Synechocystis cells and enables rapid recovery after relieving from nitrogen starvation. During early recovery, many genes changed expression, supporting the resumed cellular activity. In total, our results distinguished three phases during gradual nitrogen depletion: (1) an immediate response, (2) short-term acclimation and (3) long-term survival. This shows that cyanobacteria respond to nitrogen starvation by a cascade of physiological adaptations reflected by numerous changes in the transcriptome unfolding at different timescales.
Environmental Microbiology
Cyanobacteria evolved sophisticated mechanisms allowing them to cope with environmental depletion of combined nitrogen. Here, we describe progress in understanding the processes involved in acclimation of nondiazotrophic cyanobacteria to nitrogen shortage, known as nitrogen chlorosis. The process includes immediate metabolic changes and degradation of light harvesting complexes as well as long-term acclimation responses. Consequently, quiescent cells substantially differing from vegetative cells are obtained. Thus, the process leading to these considerable metabolic and morphological changes is referred to as a developmental program. Current understanding of the relevant regulatory processes depicts an intricate mechanism involving modulation of transcription activators by proteinaceous interacting components, as well as by small metabolites reporting the energy status and carbon-nitrogen balance of the cell. In addition, we describe in detail the quiescent state characterizing cells under prolonged starvation and the process of recovery from this dormant chlorotic state. Accumulated data provide an in depth understanding of the mechanisms accompanying the cycling of cyanobacterial cells between vegetative growth, the quiescent-state and the recovery program, allowing them to regain proliferative growth upon nutrient replenishment.
Journal of bacteriology, 1992
Cell coloration changes from normal blue-green to yellow or yellow-green when the cyanobacterium Synechococcus sp. strain PCC 7942 is deprived of an essential nutrient. We found that this bleaching process (chlorosis) in cells deprived of sulfur (S) was similar to that in cells deprived of nitrogen (N), but that cells deprived of phosphorus (P) bleached differently. Cells divided once after N deprivation, twice after S deprivation, and four times after P deprivation. Chlorophyll (Chl) accumulation stopped almost immediately upon N or S deprivation but continued for several hours after P deprivation. There was no net Chl degradation during N, S, or P deprivation, although cellular Chl content decreased because cell division continued after Chl accumulation ceased. Levels of the light-harvesting phycobiliproteins declined dramatically in a rapid response to N or S deprivation, reflecting an ordered breakdown of the phycobilisomes (PBS). In contrast, P-deprived cultures continued to ac...
Cyanobacterial phycobilisome (PBS) pigment-protein complexes harvest light and transfer the energy to reaction centers. Previous ensemble studies have shown that cyanobacteria respond to changes in nutrient availability by modifying the structure of PBS complexes, but this process has not been visualized for individual pigments at the single-cell level due to spectral overlap. We characterized the response of four key photosynthetic pigments to nitrogen depletion and repletion at the subcellular level in individual, live Synechocystis sp. PCC 6803 cells using hyperspectral confocal fluorescence microscopy and multivariate image analysis. Our results revealed that PBS degradation and resynthesis comprise a rapid response to nitrogen fluctuations, with coordinated populations of cells undergoing pigment modifications. Chlorophyll fluorescence originating from photosystem I and II decreased during nitrogen starvation, but no alteration in subcellular chlorophyll localization was found. We observed differential rod and core pigment responses to nitrogen deprivation, suggesting that PBS complexes undergo a stepwise degradation process.
Effect of the respiratory activity on photoinhibition of the cyanobacterium Synechocystis sp
Photosynthesis Research - PHOTOSYNTH RES, 2001
The influence of respiratory activity on photosynthesis in Synechocystis cells that had been exposed to high light intensity was studied using distinct conditions of nitrogen supply. The photoinhibitory rate of N-sufficient cells was not influenced by the presence of different nitrogen sources. In contrast, when N-starved cells were resupplied with ammonium, they were protected from photoinhibition. Although N-starved cells presented a higher rate of dark O2 uptake than N-sufficient ones, the photoinhibitory rate increased in both cases after addition of sodium azide or sodium azide plus salicylhydroxamic acid in the photoinhibitory treatment. In the absence of the D1 protein repair mechanism, photodamage to Photosystem II was faster in N-sufficient cells than in N-starved ones. Mitigation of photodamage disappeared when the respiratory activity of N-starved cells was partially suppressed by the addition of sodium azide or sodium azide and salicylhydroxamic acid. Our results suggest that electron flow through cyanobacterial terminal oxidases can assist Photosystem I in removing electrons from the reduced plastoquinone pool, thus contributing to both reopening of Photosystem II reaction centers and avoiding photogeneration of reactive oxygen species under photoinhibitory conditions.
Biochimica Et Biophysica Acta-bioenergetics, 2007
In cyanobacterial membranes photosynthetic light reaction and respiration are intertwined. It was shown that the single hydrogenase of Synechocystis sp. PCC 6803 is connected to the light reaction. We conducted measurements of hydrogenase activity, fermentative hydrogen evolution and photohydrogen production of deletion mutants of respiratory electron transport complexes. All single, double and triple mutants of the three terminal respiratory oxidases and the ndhB-mutant without a functional complex I were studied. After activating the hydrogenase by applying anaerobic conditions in the dark hydrogen production was measured at the onset of light. Under these conditions respiratory capacity and amount of photohydrogen produced were found to be inversely correlated. Especially the absence of the quinol oxidase induced an increased hydrogenase activity and an increased production of hydrogen in the light compared to wild type cells. Our results support that the hydrogenase as well as the quinol oxidase function as electron valves under low oxygen concentrations. When the activities of photosystem II and I (PSII and PSI) are not in equilibrium or in case that the light reaction is working at a higher pace than the dark reaction, the hydrogenase is necessary to prevent an acceptor side limitation of PSI, and the quinol oxidase to prevent an overreduction of the plastoquinone pool (acceptor side of PSII). Besides oxygen, nitrate assimilation was found to be an important electron sink. Inhibition of nitrate reductase resulted in an increased fermentative hydrogen production as well as higher amounts of photohydrogen.
Microbiology, 2009
A Ca 2+ signal is required for the process of heterocyst differentiation in the filamentous diazotrophic cyanobacterium Anabaena sp. PCC 7120. This paper presents evidence that a transient increase in intracellular free Ca 2+ is also involved in acclimation to nitrogen starvation in the unicellular non-diazotrophic cyanobacterium Synechococcus elongatus PCC 7942. The Ca 2+ transient was triggered in response to nitrogen step-down or the addition of 2-oxoglutarate (2-OG), or its analogues 2,2-difluoropentanedioic acid (DFPA) and 2-methylenepentanedioic acid (2-MPA), to cells growing with combined nitrogen, suggesting that an increase in intracellular 2-OG levels precedes the Ca 2+ transient. The signalling protein P II and the transcriptional regulator NtcA appear to be needed to trigger the signal. Suppression of the Ca 2+ transient by the intracellular Ca 2+ chelator N,N9-[1,2-ethanediylbis(oxy-2,1-phenylene)]bis[N-[2-[(acetyloxy)methoxy]-2-oxoethyl]]-,bis[(acetyloxy)methyl] ester (BAPTA-AM) inhibited expression of the glnB and glnN genes, which are involved in acclimation to nitrogen starvation and transcriptionally activated by NtcA. BAPTA-AM treatment partially inhibited expression of the nblA gene, which is involved in phycobiliprotein degradation following nutrient starvation and is regulated by NtcA and NblR; in close agreement, BAPTA-AM treatment partially inhibited bleaching following nitrogen starvation. Taken together, the results presented here strongly suggest an involvement of a defined Ca 2+ transient in acclimation of S. elongatus to nitrogen starvation through NtcA-dependent regulation. Abbreviations: BAPTA-AM, N,N9-[1,2-ethanediylbis(oxy-2,1phenylene)]bis[N-[2-[(acetyloxy)methoxy]-2-oxoethyl]]-,bis[(acetyloxy)methyl] ester; [Ca 2+ ] i , free intracellular calcium concentration; DFPA, difluoropentanedioic acid; 2-MPA, methylenepentanedioic acid; 2-OG, 2-oxoglutarate.
PLANT PHYSIOLOGY, 2008
Light drives the production of chemical energy and reducing equivalents in photosynthetic organisms required for the assimilation of essential nutrients. This process also generates strong oxidants and reductants that can be damaging to the cellular processes, especially during absorption of excess excitation energy. Cyanobacteria, like other oxygenic photosynthetic organisms, respond to increases in the excitation energy, such as during exposure of cells to high light (HL) by the reduction of antenna size and photosystem content. However, the mechanism of how Synechocystis sp. PCC 6803, a cyanobacterium, maintains redox homeostasis and coordinates various metabolic processes under HL stress remains poorly understood. In this study, we have utilized time series transcriptome data to elucidate the global responses of Synechocystis to HL. Identification of differentially regulated genes involved in the regulation, protection, and maintenance of redox homeostasis has offered important insights into the optimized response of Synechocystis to HL. Our results indicate a comprehensive integrated homeostatic interaction between energy production (photosynthesis) and energy consumption (assimilation of carbon and nitrogen). In addition, measurements of physiological parameters under different growth conditions showed that integration between the two processes is not a consequence of limitations in the external carbon and nitrogen levels available to the cells. We have also discovered the existence of a novel glycosylation pathway, to date known as an important nutrient sensor only in eukaryotes. Up-regulation of a gene encoding the rate-limiting enzyme in the hexosamine pathway suggests a regulatory role for protein glycosylation in Synechocystis under HL.