Oxidative stress and photoinhibition can be separated in the cyanobacterium Synechocystis sp. PCC 6803 (original) (raw)
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Biochimica et Biophysica Acta (BBA) - Bioenergetics, 2004
The Photosystem II complex (PSII) is susceptible to inactivation by strong light, and the inactivation caused by strong light is referred to as photoinactivation or photoinhibition. In photosynthetic organisms, photoinactivated PSII is rapidly repaired and the extent of photoinactivation reflects the balance between the light-induced damage (photodamage) to PSII and the repair of PSII. In this study, we examined these two processes separately and quantitatively under stress conditions in the cyanobacterium Synechocystis sp. PCC 6803. The rate of photodamage was proportional to light intensity over a range of light intensities from 0 to 2000 AE m À 2 s À 1 , and this relationship was not affected by environmental factors, such as salt stress, oxidative stress due to H 2 O 2 , and low temperature. The rate of repair also depended on light intensity. It was high under weak light and reached a maximum of 0.1 min À 1 at 300 AE m À 2 s À 1 . By contrast to the rate of photodamage, the rate of repair was significantly reduced by the above -mentioned environmental factors. Pulse-labeling experiments with radiolabeled methionine revealed that these environmental factors inhibited the synthesis de novo of proteins. Such proteins included the D1 protein which plays an important role in the photodamage -repair cycle. These observations suggest that the repair of PSII under environmental stress might be the critical step that determines the outcome of the photodamage -repair cycle. D
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.
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.
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.
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.
Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery
EMBO Journal, 2001
Absorption of excess light energy by the photosynthetic machinery results in the generation of reactive oxygen species (ROS), such as H 2 O 2. We investigated the effects in vivo of ROS to clarify the nature of the damage caused by such excess light energy to the photosynthetic machinery in the cyanobacterium Synechocystis sp. PCC 6803. Treatments of cyanobacterial cells that supposedly increased intracellular concentrations of ROS apparently stimulated the photodamage to photosystem II by inhibiting the repair of the damage to photosystem II and not by accelerating the photodamage directly. This conclusion was con®rmed by the effects of the mutation of genes for H 2 O 2-scavenging enzymes on the recovery of photosystem II. Pulse labeling experiments revealed that ROS inhibited the synthesis of proteins de novo. In particular, ROS inhibited synthesis of the D1 protein, a component of the reaction center of photosystem II. Northern and western blot analyses suggested that ROS might in¯uence the outcome of photodamage primarily via inhibition of translation of the psbA gene, which encodes the precursor to D1 protein. Keywords: cyanobacterium/D1 protein/H 2 O 2-scavenging enzyme/photosystem II/reactive oxygen species
PLANT PHYSIOLOGY, 2011
Marine Synechococcus undergo a wide range of environmental stressors, especially high and variable irradiance, which may induce oxidative stress through the generation of reactive oxygen species (ROS). While light and ROS could act synergistically on the impairment of photosynthesis, inducing photodamage and inhibiting photosystem II repair, acclimation to high irradiance is also thought to confer resistance to other stressors. To identify the respective roles of light and ROS in the photoinhibition process and detect a possible light-driven tolerance to oxidative stress, we compared the photophysiological and transcriptomic responses of Synechococcus sp. WH7803 acclimated to low light (LL) or high light (HL) to oxidative stress, induced by hydrogen peroxide (H 2 O 2 ) or methylviologen. While photosynthetic activity was much more affected in HL than in LL cells, only HL cells were able to recover growth and photosynthesis after the addition of 25 mM H 2 O 2 . Depending upon light conditions and H 2 O 2 concentration, the latter oxidizing agent induced photosystem II inactivation through both direct damage to the reaction centers and inhibition of its repair cycle. Although the global transcriptome response appeared similar in LL and HL cells, some processes were specifically induced in HL cells that seemingly helped them withstand oxidative stress, including enhancement of photoprotection and ROS detoxification, repair of ROS-driven damage, and regulation of redox state. Detection of putative LexA binding sites allowed the identification of the putative LexA regulon, which was downregulated in HL compared with LL cells but up-regulated by oxidative stress under both growth irradiances.
Photochemistry and Photobiology, 1995
A high light-tolerant mutant of Anczcystis was able to tolerate about threefold higher light energy irradiance (30 W m-?) than the wild type (10 W m-". The loss of sulfhydryl content and rate of lipid peroxidation in the wild-type cells is lower than in the mutant cells at high light irradiance. This phenomenon in the wild type i s probably due to high light-induced severe photoinhibitory conditions resulting in a decreased rate of O2 evolution. Results on the bleaching of the N,N'-dimethyl-,fnitrosoaniline at high light irradiance show a higher rate of bleaching in the wild-type than in the mutant cells. Further, results on the rate of N,N'-dimethyl-p-nitrosoaniline bleaching in the presence of radical scavengers like sodium azide, histidine and sodium formate (I0 mM, each) suggest that singlet oxygen is the predominant oxygen species produced in both the wild-type and mutant cells under high light. However, a similar quenching effect of formate in the mutant cells is indicative of increased formation of hydroxyl radicals. This observation is further corroborated by higher rate of lipid peroxidation. In addition to this, the superoxide dismutase activity is higher in the mutant (1.2 unit) than in the wild type. Taken together, these results suggest that the cells of the high light-tolerant mutant have an efficient intracellular mechanism to transform the free oxygen radicals.