All cyanobacteria, algae, and plants use a similar water-oxidizing catalyst for water oxidation. This catalyst is housed in Photosystem II, a membrane-protein complex that functions as a light-driven water oxidase in oxygenic photosynthesis. Water oxidation is also an important reaction in artificial photosynthesis because it has the potential to provide cheap electrons from water for hydrogen production or for the reduction of carbon dioxide on an industrial scale. The water-oxidizing complex of Photosystem II is a Mn-Ca cluster that oxidizes water with a low overpotential and high turnover frequency number of up to 25-90 molecules of O2 released per second. In this Review, we discuss the atomic structure of the Mn-Ca cluster of the Photosystem II water-oxidizing complex from the viewpoint that the underlying mechanism can be informative when designing artificial water-oxidizing catalysts. This is followed by consideration of functional Mn-based model complexes for water oxidation and the issue of Mn complexes decomposing to Mn oxide. We then provide a detailed assessment of the chemistry of Mn oxides by considering how their bulk and nanoscale properties contribute to their effectiveness as water-oxidizing catalysts.

This review summarizes our current state of knowledge on the structural organization and functional pattern of photosynthetic water splitting in the multimeric Photosystem II (PS II) complex, which acts as a light-driven water: plastoquinone-oxidoreductase. The overall process comprises three types of reaction sequences: (1) photon absorption and excited singlet state trapping by charge separation leading to the ion radical pair [Formula: see text] formation, (2) oxidative water splitting into four protons and molecular dioxygen at the water oxidizing complex (WOC) with P680+* as driving force and tyrosine Y(Z) as intermediary redox carrier, and (3) reduction of plastoquinone to plastoquinol at the special Q(B) binding site with Q(A)-* acting as reductant. Based on recent progress in structure analysis and using new theoretical approaches the mechanism of reaction sequence (1) is discussed with special emphasis on the excited energy transfer pathways and the sequence of charge transfer steps: [Formula: see text] where (1)(RC-PC)* denotes the excited singlet state (1)P680* of the reaction centre pigment complex. The structure of the catalytic Mn(4)O(X)Ca cluster of the WOC and the four step reaction sequence leading to oxidative water splitting are described and problems arising for the electronic configuration, in particular for the nature of redox state S(3), are discussed. The unravelling of the mode of O-O bond formation is of key relevance for understanding the mechanism of the process. This problem is not yet solved. A multistate model is proposed for S(3) and the functional role of proton shifts and hydrogen bond network(s) is emphasized. Analogously, the structure of the Q(B) site for PQ reduction to PQH(2) and the energetic and kinetics of the two step redox reaction sequence are described. Furthermore, the relevance of the protein dynamics and the role of water molecules for its flexibility are briefly outlined. We end this review by presenting future perspectives on the water oxidation process.

Nonphotochemical hole burning and pressure-dependent absorption and hole-burning results are presented for the isolated (disaggregated) chlorophyll a/b light-harvesting II trimer antenna complex of green plants. Analysis of the 4.2 K burn-fluence dependent hole spectra and zero-phonon hole action spectra indicates that the three lowest energy states (Q y ) lie at 677.1, 678.4 and 679.8 nm. Their combined absorption intensity is equivalent to that of three Chl a molecules. The inhomogeneous broadening of their absorption bands is 70 cm-1. It is argued that these states, separated by 30 cm-1, are associated with the lowest energy state of the trimer subunit with the 30 cm-1 separations due to the indigenous structural heterogeneity of protein complexes. The linear electron−phonon coupling of the 679.8 nm state is weak and characterized, in part, by a mean phonon frequency of ωm = 18 cm-1 and Huang−Rhys factor of S m = 0.8, values which yield the correct Stokes shift for fluorescence from the 679.8 nm state at 4.2 K. The temperature dependence of the zero-phonon hole (ZPH) width for that state is consistent with optical dynamics due to coupling with glasslike two-level systems of the protein. The ZPH width at 1.9 K is 0.037 cm-1. Satellite hole structure produced by burning in the above three states as well as their low linear pressures shift rates (about − 0.08 cm-1/MPa) indicate that the Chl a molecule of the subunit associated with them is weakly coupled to other Chl molecules. The linear pressure shift rates for the main Q y -absorption bands are also low. The shift rates appear to be dictated by protein−Chl interactions rather than excitonic couplings. Holes burned into the 650 nm absorption band reveal energy transfer times of 1 ps and ∼100 fs which are discussed in terms of time domain measurements of the Chl b → Chl a transfer rates (Connelly et al. J. Phys. Chem. B 1997, 101, 1902). The holewidths associated with burning into the 676 nm absorption band lead to Chl a → Chl a transfer times in the 6−10 ps range, in good agreement with the time domain values (Savikhin et al. Biophys. J. 1994, 66, 1597).

Time-local and time-nonlocal theories are used in combination with optical spectroscopy to characterize the water-soluble chlorophyll binding protein complex (WSCP) from cauliflower. The recombinant cauliflower WSCP complexes reconstituted with either chlorophyll b (Chl b) or Chl a/Chl b mixtures are characterized by absorption spectroscopy at 77 and 298 K and circular dichroism at 298 K. On the basis of the analysis of these spectra and spectra reported for recombinant WSCP reconstituted with Chl a only (Hughes, J. L.; Razeghifard, R.; Logue, M.; Oakley, A.; Wydrzynski, T.; Krausz, E. J. Am. Chem. Soc. U.S.A. 2006, 128, 3649), the "open-sandwich" model proposed for the structure of the pigment dimer is refined. Our calculations show that, for a reasonable description of the data, a reduction of the angle between pigment planes from 60 degrees of the original model to about 30 degrees is required when exciton relaxation-induced lifetime broadening is included in the analysis of optical spectra. The temperature dependence of the absorption spectrum is found to provide a unique test for the two non-Markovian theories of optical spectra. Based on our data and the 1.7 K spectra of Hughes et al. (2006), the time-local partial ordering prescription theory is shown to describe the experimental results over the whole temperature range between 1.7 K and room temperature, whereas the alternative time-nonlocal chronological ordering prescription theory fails at high temperatures. Modified-Redfield theory predicts sub-100 fs exciton relaxation times for the homodimers and a 450 fs time constant in the heterodimers. Whereas the simpler Redfield theory gives a similar time constant for the homodimers, the one for the heterodimers deviates strongly in the two theories. The difference is explained by multivibrational quanta transitions in the protein which are neglected in Redfield theory.

The 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 Y(z) 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 Y(z)(ox) induced oxidation steps in the WOC up to redox state S(3) 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 Y(z)(ox) reduction by the WOC in redox state S(3) eventually leading to formation and release of O(2) 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.

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The influence of UV‐B irradiation on photosystem II activities has been investigated using isolated photosystem II membrane fragments from spinach. It was found: (a) The average amount of DCIP reduced per flash declined drastically with increasing irradiation time in the absence of DPC but remained almost unaffected in its presence, (b) After UV‐B irradiation, the maximum amplitude of laser flash induced 830 nm absorption changes decreases only slightly; whereas the relaxation kinetics exhibit marked effects: the (JLS components dominate the decay at the expense of ns components. The γ.s kinetics already arise after illumination with a single flash of dark adapted samples, (c) The manganese content decreases only partly at irradiation times where the oxygen evolution capacity is almost completely lost, (d) The polypeptide pattern is hardly affected; the number of atrazine binding sites markedly decreases. Based on the results of this study, UV‐B irradiation is inferred to deteriorate primarily the function of water oxidation. The action spectrum of the UV‐B effect does not reveal a specific target molecule. It is assumed that structural changes of the D‐l/D‐2 polypeptide matrix are responsible for the modification by UV‐B irradiation of the capacity of water oxidation and atrazine binding.

The effect of the reductant hydrazine on the flash-induced oxygen oscillation patterns of spinach thylakoids was used to characterize a new super-reduced redox state of the water oxidase in photosystem II. The formation of a discrete S(-3) state is evident from the shift of the first maximum of oxygen evolution from the 3rd flash through the 5th flash to the 7th flash during a 90 min incubation of dark-adapted thylakoids with 10 mM hydrazine sulfate at pH 6.8 on ice. A distinct period four oscillation with further maxima on the 11th and 15th flashes is still observed at this stage of the incubation. The data analysis within the framework of an extended Kok model reveals that a S(-3) state population of almost 50% can be achieved by this treatment. A prolonged incubation of the S(-3) sample with 10 mM hydrazine (and even 100 mM) does not lead to a further shift of the first maximum toward the 9th flash that could reflect the formation of the S(-5) state. Instead, a slow oxidation of S(-3) to S(-2) takes place by an as yet unidentified electron acceptor. A consistent simulation of all the measured oxygen oscillation patterns of this study could, however, only be achieved by including the formal redox states S(-4) and S(-5) in the fits (S(-4) + S(-5) up to 35%). The implications of these findings for the oxidation states of the manganese in the tetranuclear cluster of the water oxidase are discussed.