Group 2 Sigma Factor Mutant sigCDE of the Cyanobacterium Synechocystis sp. PCC 6803 Reveals Functionality of Both Carotenoids and Flavodiiron Proteins in Photoprotection of Photosystem II (original) (raw)
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Plant and Cell Physiology, 2013
Adjustment of gene expression during acclimation to stress conditions, such as bright light, in the cyanobacterium Synechocystis sp. PCC 6803 depends on four group 2 s factors (SigB, SigC, SigD, SigE). A ÁsigCDE strain containing the stress-responsive SigB as the only functional group 2 s factor appears twice as resistant to photoinhibition of photosystem II (PSII) as the control strain. Microarray analyses of the ÁsigCDE strain indicated that 77 genes in standard conditions and 79 genes in high light were differently expressed compared with the control strain. Analysis of possible photoprotective mechanisms revealed that high carotenoid content and up-regulation of the photoprotective flavodiiron operon flv4-sll0218-flv2 protected PSII in ÁsigCDE, while up-regulation of pgr5-like, hlipB or isiA genes in the mutant strain did not offer particular protection against photoinhibition. Photoinhibition resistance was lost if ÁsigCDE was grown in high CO 2 , where carotenoid and Flv4, Sll0218, and Flv2 contents were low. Additionally, photoinhibition resistance of the ÁrpoZ strain (lacking the omega subunit of RNA polymerase), with high carotenoid but low Flv4-Sll0218-Flv2 content, supported the importance of carotenoids in PSII protection. Carotenoids likely protect mainly by quenching of singlet oxygen, but efficient nonphotochemical quenching in ÁsigCDE might offer some additional protection. Comparison of photoinhibition kinetics in control, ÁsigCDE, and ÁrpoZ strains showed that protection by the flavodiiron operon was most efficient during the first minutes of highlight illumination.
Biochimica et Biophysica Acta (BBA) - Bioenergetics, 2008
Excess light is harmful for photosynthetic organisms. The cyanobacterium Synechocystis PCC 6803 protects itself by dissipating the excess of energy absorbed by the phycobilisome, the water-soluble antenna of Photosystem II, into heat decreasing the excess energy arriving to the reaction centers. Energy dissipation results in a detectable decrease of fluorescence. The soluble Orange Carotenoid Protein (OCP) is essential for this blue-green light induced mechanism. OCP genes appear to be highly conserved among phycobilisomecontaining cyanobacteria with few exceptions. Here, we show that only the strains containing a whole OCP gene can perform a blue-light induced photoprotective mechanism under both iron-replete and ironstarvation conditions. In contrast, strains containing only N-terminal and/or C-terminal OCP-like genes, or no OCP-like genes at all lack this light induced photoprotective mechanism and they were more sensitive to high-light illumination. These strains must adopt a different strategy to longer survive under stress conditions. Under iron starvation, the relative decrease of phycobiliproteins was larger in these strains than in the OCP-containing strains, avoiding the appearance of a population of dangerous, functionally disconnected phycobilisomes. The OCP-containing strains protect themselves from high light, notably under conditions inducing the appearance of disconnected phycobilisomes, using the energy dissipation OCPphycobilisome mechanism.
Biochimica et Biophysica Acta (BBA) - Bioenergetics, 2014
Roles of oxidative stress and photoinhibition in high light acclimation were studied using a regulatory mutant of the cyanobacterium Synechocystis sp. PCC 6803. The mutant strain ΔsigCDE contains the stress responsive SigB as the only functional group 2 σ factor. The ΔsigCDE strain grew more slowly than the control strain in methylviologen-induced oxidative stress. Furthermore, a fluorescence dye detecting H 2 O 2 , hydroxyl and peroxyl radicals and peroxynitrite, produced a stronger signal in ΔsigCDE than in the control strain, and immunological detection of carbonylated residues showed more protein oxidation in ΔsigCDE than in the control strain. These results indicate that ΔsigCDE suffers from oxidative stress in standard conditions. The oxidative stress may be explained by the findings that ΔsigCDE had a low content of glutathione and low amount of Flv3 protein functioning in the Mehler-like reaction. Although ΔsigCDE suffers from oxidative stress, up-regulation of photoprotective carotenoids and Flv4, Sll2018, Flv2 proteins protected PSII against light induced damage by quenching singlet oxygen more efficiently in ΔsigCDE than in the control strain in visible and in UV-A/B light. However, in UV-C light singlet oxygen is not produced and PSII damage occurred similarly in the ΔsigCDE and control strains. According to our results, resistance against the light-induced damage of PSII alone does not lead to high light tolerance of the cells, but in addition efficient protection against oxidative stress would be required.
Plant and Cell Physiology
Orange carotenoid protein (OCP) plays a vital role in the thermal dissipation of excitation energy in the photosynthetic machinery of the cyanobacterium Synechocystis sp. PCC 6803. To clarify the role of OCP in the protection of PSII from strong light, we generated an OCP-overexpressing strain of Synechocystis and examined the effects of overexpression on the photoinhibition of PSII. In OCP-overexpressing cells, thermal dissipation of energy was enhanced and the extent of photoinhibition of PSII was reduced. However, photodamage to PSII, as monitored in the presence of lincomycin, was unaffected, suggesting that overexpressed OCP protects the repair of PSII. Furthermore, the synthesis de novo of proteins in thylakoid membranes, such as the D1 protein which is required for the repair of PSII, was enhanced in OCP-overexpressing cells under strong light, while the production of singlet oxygen was suppressed. Thus, the enhanced thermal dissipation of energy via overexpressed OCP might support the repair of PSII by protecting protein synthesis from oxidative damage by singlet oxygen under strong light, with the resultant mitigation of photoinhibition of PSII.
Frontiers in Plant Science, 2020
The tolerance of photosynthesis to strong light increases in photosynthetic organisms during acclimation to strong light. We investigated the role of carotenoids in the protection of photosystem II (PSII) from photoinhibition after acclimation to strong light in the cyanobacterium Synechocystis sp. PCC 6803. In cells that had been grown under strong light at 1,000 mmol photons m −2 s −1 (SL), specific carotenoids, namely, zeaxanthin, echinenone, and myxoxanthophyll, accumulated at high levels, and the photoinhibition of PSII was less marked than in cells that had been grown under standard growth light at 70 mmol photons m −2 s −1 (GL). The rate of photodamage to PSII, as monitored in the presence of lincomycin, did not differ between cells grown under SL and GL, suggesting that the mitigation of photoinhibition after acclimation to SL might be attributable to the enhanced ability to repair PSII. When cells grown under GL were transferred to SL, the mitigation of photoinhibition of PSII occurred in two distinct stages: a first stage that lasted 4 h and the second stage that occurred after 8 h. During the second stage, the accumulation of specific carotenoids was detected, together with enhanced synthesis de novo of proteins that are required for the repair of PSII, such as the D1 protein, and suppression of the production of singlet oxygen (1 O 2). In the DcrtRDcrtO mutant of Synechocystis, which lacks zeaxanthin, echinenone, and myxoxanthophyll, the mitigation of photoinhibition of PSII, the enhancement of protein synthesis, and the suppression of production of 1 O 2 were significantly impaired during the second stage of acclimation. Thus, elevated levels of the specific carotenoids during acclimation to strong light appeared to protect protein synthesis from 1 O 2 , with the resultant mitigation of photoinhibition of PSII.
Frontiers in Microbiology
Carotenoids in cyanobacteria play an important role in protecting against and in repairing damage against low level UV-B radiation. Here we use transcriptomics and metabolomic HPLC pigment analysis to compare carotenoid pathway regulation in the filamentous cyanobacterium Chlorogloeopsis fritschii PCC 6912 exposed to white light and to white light supplemented with low level UV-B. Under UV-B changes in carotenoid transcription regulation were found associated with carotenogenesis (carotenoid synthesis), photoprotection and carotenoid cleavage. Transcriptional regulation was reflected in corresponding pigment signatures. All carotenogenesis pathway genes from geranylgeranyl-diphosphate to lycopene were upregulated. There were significant increases in expression of gene homologs (crtW, crtR, cruF, and cruG) associated with routes to ketolation to produce significant increases in echinenone and canthaxanthin concentrations. There were gene homologs for four β-caroteneketolases (crtO and crtW) present but only one crtW was upregulated. Putative genes encoding enzymes (CruF, CrtR, and CruG) for the conversion of γ-carotene to myxol 2-methylpentoside were upregulated. The hydroxylation pathway to nostaxanthin via zeaxanthin and caloxanthin (gene homologs for CrtR and CrtG) were not upregulated, reflected in the unchanged corresponding pigment concentrations in zeaxanthin, caloxanthin and nostaxanthin, Transcripts for the non-photochemical quenching related Orange-Carotenoid-Protein (OCP) and associated Fluoresence-Recovery-Protein (FRP) associated with photoprotection were upregulated, and one carotenoid binding Helical-Carotenoid-Protein (HCP) gene homolog was downregulated. Multiple copies of genes encoding putative apocarotenoid related carotenoid oxygenases responsible for carotenoid cleavage were identified, including an upregulated apo-β-carotenaloxygenase gene homologous to a retinal producing enzyme. Our study provides holistic insight into the photoregulatory processes that modulate the synthesis,
Additional families of orange carotenoid proteins in the photoprotective system of cyanobacteria
Nature plants, 2017
The orange carotenoid protein (OCP) is a structurally and functionally modular photoactive protein involved in cyanobacterial photoprotection. Using phylogenomic analysis, we have revealed two new paralogous OCP families, each distributed among taxonomically diverse cyanobacterial genomes. Based on bioinformatic properties and phylogenetic relationships, we named the new families OCP2 and OCPx to distinguish them from the canonical OCP that has been well characterized in Synechocystis, denoted hereafter as OCP1. We report the first characterization of a carotenoprotein photoprotective system in the chromatically acclimating cyanobacterium Tolypothrix sp. PCC 7601, which encodes both OCP1 and OCP2 as well as the regulatory fluorescence recovery protein (FRP). OCP2 expression could only be detected in cultures grown under high irradiance, surpassing expression levels of OCP1, which appears to be constitutive; under low irradiance, OCP2 expression was only detectable in a Tolypothrix m...
Biochimica et Biophysica Acta (BBA) - Bioenergetics
Photosynthetic organisms need to sense and respond to fluctuating environmental conditions, to perform efficient photosynthesis and avoid the formation of harmful reactive oxygen species. Cyanobacteria have developed a photoprotective mechanism that decreases the energy arriving at the reaction centers by increasing thermal energy dissipation at the level of the phycobilisome, the extramembranal light-harvesting antenna. This mechanism is triggered by the photoactive orange carotenoid protein (OCP). In this study, we characterized OCP and the related photoprotective mechanism in non-stressed and light-stressed cells of three different strains of Planktothrix that can form impressive blooms. In addition to changing lake ecosystemic functions and biodiversity, Planktothrix blooms can have adverse effects on human and animal health as they produce toxins (e.g., microcystins). Three Planktothrix strains were selected: two green strains, PCC 10110 (microcystin producer) and PCC 7805 (non-microcystin producer), and one red strain, PCC 7821. The green strains colonize shallow lakes with higher light intensities while red strains proliferate in deep lakes. Our study allowed us to conclude that there is a correlation between the ecological niche in which these strains proliferate and the rates of induction and recovery of OCP-related photoprotection. However, differences in the resistance to prolonged highlight stress were correlated to a better replacement of damaged D1 protein and not to differences in OCP photoprotection. Finally, microcystins do not seem to be involved in photoprotection as was previously suggested.