Mechanism of light induced water splitting in Photosystem II of oxygen evolving photosynthetic organisms

AbstractThe reactions of light induced oxidative water splitting were analyzed within the framework of the empirical rate constant–distance relationship of non-adiabatic electron transfer in biological systems (C. C. Page, C. C. Moser, X. Chen , P. L. Dutton, Nature 402 (1999) 47–52) on the basis of structure information on Photosystem II (PS II) (A. Guskov, A. Gabdulkhakov, M. Broser, C. Glöckner, J. Hellmich, J. Kern, J. Frank, W. Saenger, A. Zouni, Chem. Phys. Chem. 11 (2010) 1160–1171, Y. Umena, K. Kawakami, J-R Shen, N. Kamiya, Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9Å. Nature 47 (2011) 55–60). Comparison of these results with experimental data leads to the following conclusions: 1) The oxidation of tyrosine Yz by the cation radical P680+· in systems with an intact water oxidizing complex (WOC) is kinetically limited by the non-adiabatic electron transfer step and the extent of this reaction is thermodynamically determined by relaxation processes in the environment including rearrangements of hydrogen bond network(s). In marked contrast, all Yzox induced oxidation steps in the WOC up to redox state S3 are kinetically limited by trigger reactions which are slower by orders of magnitude than the rates calculated for non-adiabatic electron transfer. 3) The overall rate of the triggered reaction sequence of Yzox reduction by the WOC in redox state S3 eventually leading to formation and release of O2 is kinetically limited by an uphill electron transfer step. Alternative models are discussed for this reaction. The protein matrix of the WOC and bound water molecules provide an optimized dynamic landscape of hydrogen bonded protons for catalyzing oxidative water splitting energetically driven by light induced formation of the cation radical P680+·. In this way the PS II core acts as a molecular machine formed during a long evolutionary process. This article is part of a Special Issue entitled: Photosynthesis Research for Sustainability: from Natural to Artificial

Measurements of Penetration and Detoxification of PS II Herbicides in Whole Leaves by a Fluorometric Method

The effect of herbicides that inhibit the photosynthetic electron transport at the photosystem II acceptor side has been analyzed in whole plants by using a fluorometric method. The data reported indicate that the apparent variable fluorescence of the induction curve normalized to the control value provides reliable information about the penetration rate and metabolic detoxification of PS II herbicides in whole plants

Studies on the Functional Mechanism of System II Herbicides in Isolated Chloroplasts

The effect of specific proteolytic enzymes on variable fluorescence, p-benzoquinone-mediated oxygen evolution, PS II herbicide (atrazine and bromoxynil) binding, and protein degradation has been analyzed in isolated class II pea chloroplasts. It was found that: 1. Trypsin and a lysine-specific protease effectively reduce the maximum chlorophyll-a fluorescence yield, whereas the initial fluorescence remains almost constant. At the same number of enzymatic activity units both proteases have practically the same effect. 2. Trypsin and a lysine-specific protease inhibit the p-benzoquinone-mediated flash-induced oxygen evolution with trypsin being markedly more effective at the same number of activity units of both enzymes. Unstacked thylakoids exhibit a higher sensitivity to proteolytic degradation by both enzymes. 3. Trypsin and a lysine-specific protease reduce the binding capacity of [14C]atrazine, but enhance that of [14C]bromoxynil (at long incubation times trypsin treatment also impairs bromoxynil binding). At the same specific activity a markedly longer treatment is required for the lysine-specific protease in order to achieve the same degree of modification as with trypsin. 4. Trypsin was found to attack the rapidly-turned-over 32 kDa-protein severely, whereas the lysine-specific protease does not modify this polypeptide. On the other hand, the lysine-specific protease attacks the light harvesting complex II. 5. Under our experimental conditions an arginine-specific protease did not affect chlorophyll-a fluorescence yield, p-benzoquinone-mediated oxygen evolution, herbicide binding and the poly- peptide pattern. Based on these results a mechanism is proposed in which an as yet unidentified polypeptide with exposable lysine residues, as well as the lysine-free “QB-protein” regulate the electron transfer from Q-A to QB and are involved in herbicide binding

Herbicide/Quinone Binding Interactions in Photosystem II

Many inhibitors prevent the oxidation of the primary electron-accepting quinone (QA) by the secondary quinone (Qв) in photosystem II by displacement of Qв from its binding site. On the other hand, plastoquinone-1 and 6-azido-5-decyl-2,3-dim ethoxy-p-benzoquinone displace herbicides. Binding studies show the herbicide/quinone interaction to be (apparently) competitive.The herbicide binding is influenced differentially by various treatments. In this paper it is shown that the affinity of, for example, bromoxynil is decreased by thylakoid unstacking or by light-or reductant-induced reduction of certain thylakoid components, whereas atrazine affinity remains unchanged. Furthermore, absence of HCO-3 in the presence of form ate leads to an affinity decrease of bromoxynil and atrazine, but to an increase in i-dinoseb affinity. Other differential photosystem II herbicide effects are known from the literature.Since different and unrelated groups of Q-A oxidation inhibitors have been found, and because of the above-mentioned dissimilarities in binding characteristics for different inhibitor groups, the hypothesis of non-identical, but “overlapping” binding sites for different herbicide groups and the native quinone must be more extensively defined. In this manuscript we evaluate both the competitive herbicide/quinone binding model, and a model in which binding of one ligand alters the protein conformation resulting in a dramatic decrease in the binding affinity of ligands from other chemical groups; in this model ligands from the same or related chemical groups bind competitively. Thus, the latter model proposes that only one herbicide or quinone molecule can be bound with high affinity to the herbicide/quinone binding environment, but it depends on the chemical structure of the ligands whether the binding interaction between two ligands is truly competitive or more indirect (allosteric), mediated through the protein conformation

© 1985 Martinus Ni]hoff/Dr W. Junk Publishers, Dordrecht. Printed in the Netherlands.

Abstract. Photosynthetic water oxidation is unique to plants and cyanobacteria, it occurs in thylakoid membranes. The components associated with this process include: a reaction center polypeptide, having a molecular weight (Mr) of 47-50 kilodaltons (kDa), containing a reaction center chlorophyll a labeled as P680, a plastoquinol(?)electron donor Z, a primary electron acceptor pheophytin, and a quinone electron acceptor QA; three 'extrinsic ' polypeptides having Mr of approximately 17kDa, 23 kDa, and 33 kDa; and, in all likelihood, an approximately 34 kDa 'intrinsic ' polypeptide associated with manganese (Mn) atoms. In addition, chloride and calcium ions appear to be essential components for water oxidation. Photons, absorbed by the so-called photosystem II, provide the necessary energy for the chemical oxidation-reduction at P680; the oxidized P680 (P680+), then, oxidizes Z, which then oxidizes the watermanganese system contained, perhaps, in a protein matrix. The oxidation of water, leading to 02 evolution and H + release, requires four such independent acts, i.e., there is a charge accumulating device (the so-called S-states). In this minireview, we have presented our current understanding of the reaction center P680, the chemical natur

Photosynthetic Light-Harvesting (Antenna) Complexes - Structures and Functions

Chlorophylls and bacteriochlorophylls, together with carotenoids, serve, noncovalently bound to specific apoproteins, as principal light-harvesting and energy-transforming pigments in photosynthetic organisms. In recent years, enormous progress has been achieved in the elucidation of structures and functions of light-harvesting (antenna) complexes, photosynthetic reaction centers and even entire photosystems. It is becoming increasingly clear that light-harvesting complexes not only serve to enlarge the absorption cross sections of the respective reaction centers but are vitally important in short- and long-term adaptation of the photosynthetic apparatus and regulation of the energy-transforming processes in response to external and internal conditions. Thus, the wide variety of structural diversity in photosynthetic antenna “designs” becomes conceivable. It is, however, common for LHCs to form trimeric (or multiples thereof) structures. We propose a simple, tentative explanation of the trimer issue, based on the 2D world created by photosynthetic membrane systems

Interconversion of Low- and High-Potential Forms of Cytochrome b559 in Tris-Washed Photosystem II Membranes under Aerobic and Anaerobic Conditions

In this study, the reversible conversion between the high- (HP) and low-potential (LP) forms of Cytb559 has been analyzed in Tris-washed photosystem II (PSII) enriched membranes. These samples are deprived of the Mn cluster of the water-oxidizing complex (WOC) and the extrinsic regulatory proteins. The results obtained by application of optical and EPR spectroscopy reveal that (i) under aerobic conditions, the vast majority of Cytb559 exhibits a low midpoint potential, (ii) after removal of O2 in the dark, a fraction of Cytb559 is converted to the high-potential form which reaches level of about 25% of the total Cytb559, (iii) a similar dark transformation of LP HP Cytb559 occurs under reducing conditions (8 mM hydroquinone), (iv) under anaerobic conditions and in the presence of 8 mM hydroquinone, about 60% of the Cytb559 attains the HP form, (v) the interconversion is reversible with the re-establishment of aerobic conditions, and (vi) aerobic and oxidizing conditions (2 mM ferricyanide or 0.5 mM potassium iridate) induce a decrease of the amount of the HP form, also showing that the conversion is reversible. This reversible interconversion between LP and HP Cytb559 is not observed in PSII membrane fragments with an intact WOC. On the basis of these findings, the possibility is discussed that the O2-dependent conversion of Cytb559 in PSII complexes lacking a functionally competent WOC is related to a protective role of Cytb559 in photoinhibition and/or that it is involved in the regulation of the assembly of a competent water-oxidizing complex in PSII