A proposal for water oxidation in photosystem II

Abstract

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...

QM/MM computational studies of substrate water binding to the oxygen-evolving centre of photosystem II

“…Considering that the S 1 /S 2 transition involves oxidation of a manganese centre, the observed acceleration of the exchange of W slow is also intriguing since it implies that the oxidation of a manganese centre must indirectly affect the exchange rate of a calcium-bound water molecule. While these observations are reproducible and unambiguous, it is not clear whether they can be rationalized by previously proposed mechanistic models (Pecoraro et al 1998;Vrettos et al 2001;Messinger 2004). The calculations reported in this paper address both of these observations through the analysis of structural models of the OEC in the S 1 and S 2 states (Sproviero et al 2006a(Sproviero et al ,b, 2007.…”

Functional models for the oxygen-evolving complex of photosystem II

“…This family of mechanisms can be viewed as an adaptation of the 2+2 mechanism mentioned above that has been refashioned to reflect the most recent OEC structural model [45][46][47][48][49]. The result is a mechanism where a high-valent manganese-oxo is formed on the lone dangler manganese.…”

Photosynthetic generation of oxygen

“…The location of one Mn ion (Mn4 or dangler Mn) adjacent to the Ca 2C and their positioning towards the side chains of several key amino acids, including the redox active TyrZ, suggests that they provide the 'catalytic' surface for binding the two substrate water molecules and their subsequent oxidation. One well-championed mechanism (Messinger et al 1995;Pecoraro et al 1998;Messinger 2004;McEvoy & Brudvig 2004, 2006 suggests that the substrate water, associated with Mn4, is deprotonated during the S-state cycle. This mechanism is dependent on Mn4 being converted to a high-oxidation state (possible Mn(V )) during progression to the S4-state just prior to O-O bond formation.…”