Chapter 1
Structural Studies of Oxomanganese Complexes for Water Oxidation Catalysis

Ivan Rivalta, Gary W. Brudvig and Victor S. Batista

Department of Chemistry, Yale University, New Haven, CT, USA

1.1 Introduction

Photosystem II (PSII) is a 650 kDa protein complex embedded in the thylakoid membrane of green plant chloroplasts and the internal membranes of cyanobacteria. It is responsible for catalyzing oxygen evolution by water splitting into oxygen, protons and electrons. The catalytic site is the oxygen-evolving complex (OEC) embedded in the protein subunit D1, an oxomaganese cuboidal core comprising earth-abundant metals ( and ) linked by bridges. The reaction is initiated upon light absorption by an antenna complex, in a process that oxidizes the chlorophyll a species P680 and forms the radical cation a strong oxidizing species that in turns oxidizes tyrosine YZ, a redox-active amino acid residue located in close proximity to the oxomanganese cluster. The oxidized YZ is able to oxidize Mn, storing oxidizing equivalents in the inorganic core of the OEC. This photocatalytic process is repeated multiple times while evolving the OEC through five oxidation storage states (S0–S4) along the catalytic cycle (the so-called Kok cycle) [1, 2]. In the fully oxidized S4 state, the Mn cluster catalyzes oxygen evolution, completing the four-electron water oxidation reaction that splits water into molecular oxygen, protons and electrons, as follows:

The characterization of the OEC structure and overall structural rearrangement during the multistep photocatalytic cycle is crucial for understanding the reaction mechanism and for the design of biomimetic catalytic systems. X-ray spectroscopy has been largely used to reveal the atomistic details of the OEC structure, with several X-ray crystal models proposed in the past decade [3–6]. The most recent breakthroughs in the field have resolved the OEC structure at resolution [7], including the complete coordination of metal centers by water ligands and proteinaceous side chains. However, the high doses of X-ray radiation necessary for data collection are thought to have reduced the Mn centers, changing the geometry of the OEC and leaving uncertain the actual geometry of the oxomanganese complex in its dark-adapted (S1) state [8–11]. A model of the OEC in the S1 state consistent with both high-resolution spectroscopy and X-ray diffraction (XRD) data has been obtained using quantum mechanics/molecular mechanics (QM/MM) hybrid methods, implemented at the density functional theory (DFT) level [12]. The model has been validated through simulations of extended X-ray absorption fine structure (EXAFS) spectroscopy and direct comparisons with experimental measurements [12].

The oxomanganese complex of the OEC of PSII has inspired the development of biomimetic catalysts for water oxidation with high-valent Mn centers linked by bridges, as in the Mn4CaO5 cluster ligated by terminal waters and surrounding amino acid residues. Several complexes with common structural features have been synthesized [13–23] to investigate the structure/function relations responsible for catalytic water oxidation and to provide fundamental insight into the use of catalysts for artificial photosynthetic devices based on earth-abundant metals [24–26]. One of these biomimetic complexes is the Mn–terpy dimer (1) which has terminal water molecules bound to the oxomanganese core, in close analogy to the OEC. Complex 1 also catalyzes water oxidation upon activation by a primary oxidant in homogeneous solutions [27, 28] and when deposited on TiO2 thin films [24, 25, 29] or immobilized in clays [30, 31]. Mechanistic aspects of water oxidation catalyzed by complex 1 are thought to be common to the OEC of PSII, where deprotonation of terminal waters and oxidation of the Mn core is thought to give rise to the formation of a hot oxyl radical intermediate that is susceptible to nucleophilic attack by substrate water. DFT studies of the water splitting catalyzed by 1 have also shown the non-innocent role of acetate buffer as proton acceptor centers during the O–O bond formation step [32]. This chapter reviews these recent advances in computational structural studies of the OEC and biomimetic oxomanganese complexes, including the structural characterization of the OEC in the S1 state and mechanistic studies of water oxidation catalyzed by the OEC and by complex 1 in solution or covalently attached to nanoparticulate semiconductor surfaces.

1.2 Structural Studies of the OEC

An XRD model of the OEC of PSII at resolution [5] suggested a cuboidal cluster CaMn4, with the metal centers at the vertices of a cuboidal frame and a “dangling” Mn linked by bridges (Figure 1.1). While the X-ray model was partially consistent with EXAFS and electron paramagnetic resonance (EPR) studies [33], structural disorder and radiation damage prevented a complete characterization of the complex, including coordination of water and proteinaceous ligands to the metal centers. Consequently, several computational studies were performed to build realistic models with a complete coordination of the metal centers [23, 34–48], including QM/MM structural models with an explicit treatment of the protein environment [23, 35–39]. Several possible ligation schemes were proposed, including models with terminal water ligands bound to Ca and the dangling Mn, as proposed by DFT–QM/MM computational models [6, 7]. Remarkably, the most recent XRD model of PSII at resolution [7] has confirmed the coordination of terminal water molecules bound to and the dangling Mn, the presence of an additional bridge linking the dangling Mn to the cuboidal cluster, the coordination of carboxylate groups bridging the metal centers (Figure 1.1), and the proximity of chloride to the OEC. In addition, the latest XRD data introduce new features that have not been previously proposed by either empirical or computational models, including the bidentate coordination of the D170 side chain bridging the dangling Mn and Ca (Figure 1.1a compares the two XRD models). These advances have stimulated new studies of structural changes of the OEC along the Kok catalytic cycle. In particular, the first challenge was to establish whether the OEC model proposed by the XRD structure at resolution could be assigned to the S1 resting state or if it was perhaps more representative of a mixture of S-state intermediates along the photocatalytic cycle. This question was first addressed by simulations of EXAFS spectroscopy [12] and direct comparisons to experimental data characterizing the structural modifications in the OEC cluster along the S0–S3 transitions [10, 49, 50].

Figure 1.1 Structural models of the OEC of PSII. (a) Superposition of the OEC in the XRD models of PSII at (red) and (blue) resolution. (b–c) Comparison between experimental isotropic EXAFS spectra of S0 (green), S1 (light blue), S2 (dark gray), S3 (brown), and calculated EXAFS spectra of the high-resolution XRD model (blue), including the k3-weighted EXAFS spectra (b) and the corresponding Fourier transform (FT) magnitudes (c).

Figure 1.1 provides a comparison of EXAFS spectra for the S0–S3 states and the spectrum calculated for the XRD model using the ab initio real-space Green function approach [51]. It shows that the calculated isotropic EXAFS spectrum based on the XRD model is significantly different from the experimental spectra of the S-state intermediates. In fact, the Fourier-transformed signals show that the XRD model has metal–ligand and metal–metal distances larger than those observed in the S0–S3 states [12]. These results with relatively large metal–metal and metal–ligand distances suggest that the even the XRD model at resolution suffered from X-ray photoreduction (radiation damage), including the S1 and S2 states [12], in spite of the experimental protocol for data collection, which minimized the level of X-ray exposure [7]. Using bond-valence theory [8] and DFT [52], it was later proposed that the high-resolution XRD model must be a mixture of highly reduced states mainly comprising the S−3 state. It is therefore established that the XRD model at resolution does not provide an accurate description of the OEC cluster in the resting S1 state, or in any catalytically active form.

1.3 The Dark-Stable State of the OEC

DFT calculations have been performed within a hybrid QM/MM scheme to model the resting S1 state of the OEC and have provided the first model consistent with the ligation scheme suggested by XRD data and with intermetallic and metal–ligand distances consistent with EXAFS spectroscopic [12]. Figure 1.2 shows the DFT–QM/MM model of the S1 state calculated at the level of theory [12], comprising four terminal water ligands (including the two substrate water molecules and bound to Ca and Mn(4), respectively), six carboxylate ligands (Asp170, Glu189, Glu333, Asp342, Ala344, and Glu354), and one imidazole ligand (His332). The QM/MM model included a proper description of the hydrogen-bonding network surrounding the OEC (Figure 1.2), including important amino acid residues next to the oxomanganese cluster, which were previously proposed to be critical acid/base-redox cofactors (e.g. Tyr161 (YZ), Asp61, Lys317, and chloride (Cl−)).

Figure 1.2 DFT–QM/MM model of the...