There has been much speculation concerning the mechanism for water oxidation by Photosystem 11. Based on recent work on the biophysics of Photosystem I1 and our own work on the reactivity of synthetic manganese complexes, we propose a chemically reasonable mechanistic model for the water oxidation function of this enzyme. An essential feature of the model is the nucleophilic attack by calcium-ligated hydroxide on an electrophilic 0x0 group ligated to high-valent manganese to achieve the critical 0-0 bond formation step. We also present a model for S-state advancement as a series of proton-coupled electron transfer steps, which has been proposed previously [Hoganson et. al., Photosynth. Res. 46, 177 (1995); Gilchrist et. al. Proc. Nat. Acad. Sci, USA. 92, 9545 (1995)], but for which we have developed model systems that allow us to probe the thermodynamics in some detail.One of the great unsolved mysteries in bioinorganic chemistry is the mechanism of water oxidation by the oxygen evolving complex (OEC) of Photosystem I1 (PS 11). This reaction is responsible for nearly all of the dioxygen on our planet and conceptually is the reverse reaction of respiration where dioxygen is converted back to water. Plants use an expansive airay of photopigments in Photosystem 11, four manganese ions, calcium and chloride to carry out these reactions. While intensively studied for many years, only now is a picture emerging as to how this fascinating and essential chemistry may result. The scope of this article is far too limited to allow for a detailed summary of previous studies in the field: therefore, interested readers are directed to recent reviews of this topic( ref. 1,2).In this contribution, we will present studies that are aimed at evaluating the chemical mechanism for water oxidation that is proposed in that proposed by G.T. Babcock(ref. 3, 4) but has significant chemical differences in the high and low S states. Important features of our proposal include: 1) oxidation of the catalytic center through a coupled protodelectron transfer from the manganese cluster to a redox active tyrosyl radical, 2) the generation in the S, state of a strongly electophilic manganyl 0x0 [Mn(V)=O] that can couple to a strongly nucleophilic hydroxyl group making a peroxide inteimediate and 3) oxidation of the transiently formed peroxide by a second 0x0 bridged dimer. Additionally, we p -1 consider the theirnodynamics of the system in order to evaluate implications for the energetics of water oxidation on cluster structure and reactivity. Figure 1 transitions require proton coupled electron transfer from the manganese cluster to a redox active tyrosine that is in close proximity to thc metal center. Functionally, this process is a hydrogen atom abstraction from a manganese bound water (hydroxide) hgand to a neutral tyrosyl radical. It is estimated that the homolytic bond dissociation energy (HBDE) for a tyrosine radical is 86.5 kcal/mol(ref. 6, 7). Thus, for H atom abstraction to be thermodynamically viable in this system, waterhydr...

A number of molecularly specific models for the oxygen-evolving complex in photosystem II (PSII) and of manganese-substrate water intermediates that may occur in this process have been proposed recently. We summarize this work briefly. Fourier transform infrared techniques have emerged as fruitful tools to study the molecular structures of Y(Z) and the manganese complex. We discuss recent work in which mid-IR (1000-2000 cm(-1)) methods have been used in this effort. The low-frequency IR region (<1000 cm(-1)) has been more difficult to access for technical reasons, but good progress has been made in overcoming these obstacles. We update recent low-frequency work on PSII and then present a detailed summary of relevant manganese model compounds that will be of importance in understanding the emerging biological data.

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It was previously shown that the addition of 1 equiv of a strong acid to [Mn(IV)(salpn)(&mgr;-O)](2), 1, generates the oxo/hydroxo complex [{Mn(IV)(salpn)}(2)(&mgr;-O,&mgr;-OH)](CF(3)SO(3)), 2, which emphasized the basicity of the &mgr;(2)-O(2)(-) units in the [Mn(IV)(&mgr;-O)](2) dimers. We now demonstrate the inherent nucleophilicity of those &mgr;(2)-O(2)(-) units by showing that the addition of methyl triflate to 1 results in formation of the oxo/methoxo-bridged Mn(IV) dimer [{Mn(IV)(salpn)}(2)(&mgr;-O,&mgr;-OCH(3))](CF(3)SO(3)), 3. EXAFS analysis of 3 demonstrates that alkylation of an oxo bridge results in the same structural modification of the [Mn(IV)(&mgr;-O)](2) core as an oxo bridge protonation. Electrochemical and spectroscopic comparisons of 3 to 2 indicate that 3 is a good electronic structure analogue for 2 without the complication of proton lability and hydrogen bonding. Indeed, 2 and 3 react nearly identically with hydrogen peroxide and with strong acids. In contrast, the products of their reactions with amines, acetate, and triphenylphosphine are dramatically different. The proton lability of 2 results in simple proton transfer, circumventing the slower redox reactions of these substrates with 3. Isotopic labeling, kinetic, and EPR-monitored radical trap studies lead to a proposed reduction-oxidation mechanistic scheme for the reactions of 3 with amines and triphenylphosphine. The Mn(III) product of this reaction, [Mn(III)(salpn)(Ph(3)PO)](CF(3)SO(3)), was isolated and crystallographically characterized as a dimerized complex. The redox nature of the reactions is confirmed by trapping of a reduced Mn intermediate which is identified by EPR spectroscopy. Comparison of the reactions of 2 and 3 demonstrates the dramatic effect of proton lability and hydrogen bonding on reactivity, and suggests how metalloenzymes may regulate active site reactivity to produce very different catalytic activities with similar active site structures. Furthermore, it also emphasizes that caution should be used when the reactivity of model compounds with easily and rapidly dissociable protons is assessed.