Influence of the Redox Potential of the Primary Quinone Electron Acceptor on Photoinhibition in Photosystem II

Abstract

We report the characterization of the effects of the A249S mutation located within the binding pocket of the primary quinone electron acceptor, Q A , in the D2 subunit of photosystem II in Thermosynechococcus elongatus. This mutation shifts the redox potential of Q A by ϳ؊60 mV. This mutant provides an opportunity to test the hypothesis, proposed earlier from herbicide-induced redox effects, that photoinhibition (light-induced damage of the photosynthetic apparatus) is modulated by the potential of Q A . Thus the influence of the redox potential of Q A on photoinhibition was investigated in vivo and in vitro. Compared with the wild-type, the A249S mutant showed an accelerated photoinhibition and an increase in singlet oxygen production. Measurements of thermoluminescence and of the fluorescence yield decay kinetics indicated that the charge-separated state involving Q A was destabilized in the A249S mutant. These findings support the hypothesis that a decrease in the redox potential of Q A causes an increase in singlet oxygen-mediated photoinhibition by favoring the back-reaction route that involves formation of the reaction center chlorophyll triplet. The kinetics of charge recombination are interpreted in terms of a dynamic structural heterogeneity in photosystem II that results in high and low potential forms of Q A . The effect of the A249S mutation seems to reflect a shift in the structural equilibrium favoring the low potential form. Photosystem II (PSII),2 the water/plastoquinone oxidoreductase, uses light energy to extract four electrons from water, producing oxygen (1-4). Each electron is transferred over a chain of redox cofactors to the terminal plastoquinone Q B , which accepts two electrons and two protons (5). The efficiency of PSII in converting light energy into a charge-separated state is remarkably high (5). The univalent photochemistry must interface with the four-electron chemistry occurring at the electron donor side with the two-electron chemistry at the acceptor side. This is achieved by different mechanisms. On the donor side, the so-called oxygen-evolving complex (OEC) accumulates four redox equivalents before it extracts four electrons from two water molecules. Accumulation is necessary, because the energy needed to extract the electrons one by one from water requires more driving force than visible light provides (4). During the catalytic cycle, the OEC exists in different oxidation states. These are designated S 0 , S 1 , S 2 , S 3 , and S 4 , where the subscript indicates the number of accumulated oxidation equivalents. The cycle is completed when the S 4 state performs a 4-electron oxidation of water, with the OEC being returned to the most reduced of the so-called S states, S 0 . The OEC consists of four manganese ions, one calcium ion (3, 4, 6, 7), and probably one chloride ion (Ref .8, but see also Ref. 9).On the electron acceptor side, electron transfer involves two plastoquinones, the primary and secondary quinone acceptors (Q A and Q B ). Although both are plastoquinones, thei...

Evidence for a Role of VIPP1 in the Structural Organization of the Photosynthetic Apparatus in Chlamydomonas

“…The downshift of the maximum temperature of the Q-band in VIPP1-RNAi cells reflects a lowering of the midpoint potential of the redox couple Q A /Q A 2 (Krieger-Liszkay and Rutherford, 1998). A lower midpoint potential of Q A was shown to increase the yield of 1 O 2 generation in the light (Fufezan et al, 2007) and therefore might represent the mechanism underlying high light sensitivity of VIPP1-RNAi cells.…”

“…Also not consistent with a simple lack of PG in PSII of VIPP1-RNAi cells is our finding that the midpoint potential of the Q A /Q A 2 redox couple in PSII is lowered (Table 2). This points to a problem with the integrity of the Q A site (Fufezan et al, 2007) instead of the Q B site, which was affected by PG depletion in cyanobacteria (Gombos et al, 2002). Certainly, a more negative midpoint potential of the Q A /Q A 2 redox couple has been shown to increase the yield of 1 O 2 (Krieger-Liszkay and Rutherford, 1998;Fufezan et al, 2007) and most likely is causing the high light sensitivity of the VIPP1-RNAi cells.…”

“…This points to a problem with the integrity of the Q A site (Fufezan et al, 2007) instead of the Q B site, which was affected by PG depletion in cyanobacteria (Gombos et al, 2002). Certainly, a more negative midpoint potential of the Q A /Q A 2 redox couple has been shown to increase the yield of 1 O 2 (Krieger-Liszkay and Rutherford, 1998;Fufezan et al, 2007) and most likely is causing the high light sensitivity of the VIPP1-RNAi cells. Phenotypes that very closely resemble those of the VIPP1-RNAi strains were observed in the C. reinhardtii hf-2 mutant, which is defective in the biosynthesis of SQDG.…”

Engineering of an alternative electron transfer path in photosystem II

“…Q 2− B is doubly protonated and released from the RC as PQH 2 into the membrane. The lifetime of Q − A is about 100 μsec in the presence of oxidized Q B , while in the presence of Q B site inhibitors, such as 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU), the lifetime of Q − A can be on the order of seconds (10). The redox potential of Q A ∕Q − A is altered by the presence of the Q B site inhibitors (11), showing that small structural changes in the PSII RC can change the electrochemical properties of the cofactors.…”

Use of the aqueous extract of Eucalyptus microcorys for the treatment in microcosm, of water containing Enterococcus faecalis: hierarchisation of cells' inhibition factors

“…The established photodynamic activity is attributable to the presence of psoralens or furocoumarins and/or quinones and anthraquinones from some plants (Serrano et al 2008). These latter compounds are often described as singlet oxygen generators (Fufezan et al 2007). Thus, the luminous intensity acts as a facilitator of E. microcorys extract activities.…”