Short Review
Application of computational chemistry to understanding the structure and mechanism of the Mn catalytic site in photosystem II – A review

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Abstract

Applications of Density Functional Theory (DFT) computational techniques to studies of the molecular structure and mechanism of the oxygen evolving, water oxidising Mn4/Ca catalytic site in Photosystem II are reviewed. We summarise results from the earlier studies (pre 2000) but concentrate mainly on those developments which have occurred since publication of several PS II crystal structures of progressively increasing resolution, starting in 2003. The work of all computational groups actively involved in PS II studies is examined, in the light of direct PS II structural information from X-ray diffraction crystallography and EXAFS on the metals in the catalytic site. We further address the consistency of the various computational models with results from a range of spectroscopic studies on the PS II site, in all of those functionally intermediate states (S-states) amenable to study. Experimental data considered include Mn K-edge XANES studies, hyperfine coupling of Mn nuclei and various ligand nuclei (including those from substrate water) seen by several EPR techniques applied to the net spin half intermediates, S0 and S2, at low temperatures. Finally we consider proposed catalytic mechanisms for the O–O bond formation step, from two groups, in the light of the available experimental evidence bearing on this process, which we also summarise.

Research highlights

► We review the theoretical contributions of all computational groups involved in PSII. ► Studies of molecular structure and the oxygen evolving mechanism are summarised. ► The most recently proposed O–O bond formation mechanisms are examined. ► Theoretical results are tested for consistency by comparison with experimental data.

Introduction

Over the last decade and a half, computational chemistry, particularly using Density Functional Theory (DFT) techniques [1], has advanced to the point where chemically realistic study of medium size systems (up to ∼200 atoms including transition metals), is possible. Given the importance and complexity of the Mn4Ca water oxidizing catalytic centre in Photosystem II (PS II) and the experimental difficulty in probing the structure and detailed electronic processes occurring within this site, it has been a natural candidate for attempts to reveal the catalytic mechanism through computational methods. This is motivated by the biologically unique chemistry of water splitting in the site, achieved almost at the thermodynamic limit of efficiency, and its possible utility as a model for ‘bio-inspired’ catalytic systems to electrolytically generate hydrogen fuel.

In PS II, electrons are electrochemically extracted from water within the Water Oxidising Complex (WOC, also called the oxygen evolving complex, OEC), a region of the PS II multi-peptide assembly near the chlorophyll containing photochemical reaction centre, P680 [2]. The reaction proceeds through five intermediates, four meta-stable states labelled S0, S1, S2 and S3, and a short-lived ‘final’ state, S4, where the subscript refers to the number of stored oxidising equivalents in the catalytic centre. Water remains exchangeable with this site up to S3 [3], and the final oxidation of two water molecules to di-oxygen occurs in a concerted, four electron step. The WOC is generally taken to comprise the redox accumulating water binding Mn4/Ca catalytic site, its immediate protein surroundings (metal ligands, Cl anion, etc.), as well as the adjacent redox active tyrosine, Yz (D1 Y161), which mediates electron transfer between the Mn4/Ca cluster and P680. These components are contained mainly within a membrane bound peptide hetero-dimer, consisting of the reaction centre peptides D1 and D2 [2], near the luminal membrane surface (in chloroplasts). No experimental technique has yet revealed the full structure of the water oxidizing complex at atomic level, although XRD structures to near atomic resolution (3.5–2.9 Å) [4], [5], [6], [7] are now available, revealing details of metal positions and protein side chains. These structures should correspond to the ‘dark stable’ S1 state, although questions concerning radiation induced Mn reduction during the XRD data collection remain [8]. These structures have strongly influenced directions in recent computational studies of the WOC, which we review.

Section snippets

Historical development of computational structural forms

It has long been established that a dominant structural motif in the WOC Mn4/Ca cluster is the presence of di-μ-oxo bridged Mn pairs in the III and IV oxidation states [2], [9]. This is also consistent with the current XRD structures, although these do not yet yield details of bridging species, etc. EXAFS had suggested that Ca is close to one or more Mn, at distances of ∼3.2–3.5 Å [9] and no evidence of close approach to Mn by Cl was found [10]. Both of these conclusions were subsequently

The S-state cycle

To date, experimental studies have not yielded an unambiguous determination of the Mn oxidations states throughout the S-state cycle. The problem is partially constrained by EPR spectroscopy, both the S0 and S2 states have spin ½ ground configurations of the coupled tetra-nuclear Mn cluster [2]. Thus the S1 state has net even spin and because its mean Mn oxidation level must be at least 3.0, only two possibilities are reasonable; S1 is Mn(III)4 or Mn(III)2(IV)2, or equivalent net spin

Spectroscopy and electronic structure

A great body of spectroscopic data exists for the WOC [2], which often for its interpretation requires reference to defined chemical analogs, model systems, etc. The latter obviously resemble the unique structural/chemical circumstances in the WOC to variable extent. Computational modelling of the WOC, particularly the Mn, their magnetic couplings and oxidation states, is now starting to give insights to aid interpretation of the spectroscopic data.

Catalytic mechanism: O–O bond formation

Understanding the mechanism of water oxidation is, of course, the ultimate goal of WOC research. In the view of the authors, computational chemistry will play a crucial, probably central role in this. However it is also our view that too much uncertainty as yet surrounds fundamental matters, such as Mn oxidation levels and substrate binding locations, for current computational studies of the mechanism to be other than indicative. We confine our discussion to this broader level.

There is a

Summary

In conclusion it is clear that computational studies on the OEC and its mechanism are now assuming a high level of sophistication and ‘realism’. While many detailed distinctions remain between the various proposals, there is now a convergence in several areas. It seems likely that the ligation pattern derived from the Berlin structures is essentially that which obtains in the functional enzyme, but some ‘flexibility’ within this exists. Such would be consistent with a number of experimental

Acknowledgments

The authors gratefully acknowledge financial assistance from the Australian Research Council. PG acknowledges receipt of an ANU Post Graduate Award. Computations were performed using the platforms of the Australian Partnership for Advanced Computing, operating through the Australian National University Supercomputer Facility.

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