Computational studies of the O(2)-evolving complex of photosystem II and biomimetic oxomanganese complexes

Abstract

In recent years, there has been considerable interest in studies of catalytic metal clusters in metalloproteins based on Density Functional Theory (DFT) quantum mechanics/molecular mechanics (QM/MM) hybrid methods. These methods explicitly include the perturbational influence of the surrounding protein environment on the structural/functional properties of the catalytic centers. In conjunction with recent breakthroughs in X-ray crystallography and advances in spectroscopic and biophysical studies, computational chemists are trying to understand the structural and mechanistic properties of the oxygen-evolving complex (OEC) embedded in photosystem II (PSII). Recent studies include the development of DFT-QM/MM computational models of the Mn(4)Ca cluster, responsible for photosynthetic water oxidation, and comparative quantum mechanical studies of biomimetic oxomanganese complexes. A number of computational models, varying in oxidation and protonation states and ligation of the catalytic center by amino acid residues, water, hydroxide and chloride have been characterized along the PSII catalytic cycle of water splitting. The resulting QM/MM models are consistent with available mechanistic data, Fourier-transform infrared (FTIR) spectroscopy, X-ray diffraction data and extended X-ray absorption fine structure (EXAFS) measurements. Here, we review these computational efforts focused towards understanding the catalytic mechanism of water oxidation at the detailed molecular level.

Figure 1

Molecular structure of the photosystem II dimer proposed by the 1S5L X-ray diffraction model from Thermosynechococcus elongatus [20] and inset QM/MM description of the oxygen-evolving complex (OEC) [13], including substrate water pathways from the lumen. Purple: Mn, Red: O; Yellow: Ca²⁺; and Green: Cl⁻.

Figure 2

Schematic representation of Photosystem II and its components embedded in the thylakoid membrane. The driving force for the Kok cycle is the repeated oxidation of P680 via successive absorption of photons. Note that the dashed and solid arrows indicate secondary and primary paths of electron transfer, respectively

Figure 3

Catalytic cycle proposed by Joliot and Kok for water splitting into dioxygen, protons and electrons at the OEC in PSII [1,2]. Dashed arrows indicate spontaneous interconversion processes in the dark. The steps for substrate water attachment and proton release are only tentatively proposed and might change with pH.

Figure 4

The OEC and its surrounding molecular environment proposed by the X-ray diffraction structure 1S5L [20], including the pentanuclear Mn₄Ca cluster and the redox active D1-Y161 (Y_Z).

Figure 5

Molecular structure of complex [Mn^IIIMn^IV(O)₂(phen)₄]³⁺ (phen = 1,10-phenanthroline) (a) and simplified model system (b), optimized at the broken symmetry unrestricted B3LYP level with the following basis set: LACVP for manganese, 6−31G(d) for oxo-bridge oxygen atoms, 6−31G for water oxygen atoms and N, 3−21G for carbon and hydrogen [14].

Figure 6

Proposed structural model of the OEC of PSII in the S₁ state (top), as described by the DFT QM/MM hybrid model obtained at the ONIOM-EE (UHF B3LYP/lacvp,6−31G(2df),6−31G:AMBER) level where the putative substrate waters labeled *fast and *slow are coordinated to Mn(4) and Ca²⁺, respectively [13], and superposition with the 1S5L X-ray diffraction model [20] (blue, bottom panel), shown in Figure 4. All amino acid residues correspond to the D1 protein subunit unless otherwise indicated.

Figure 7

Comparison between experimental [41] (red) and calculated [13] (blue,green and black) EXAFS spectra in k-space (left) and Fourier transform of the EXAFS spectra in R-space (right) for the OEC of PSII, as described by the 1S5L X-ray diffraction model (top) and the DFT QM/MM models of the S₁ state, obtained at the ONIOM-EE (UHF B3LYP/lacvp,6−31G(2df),6−31G:AMBER) level, including model (a) where the dangling manganese is pentacoordinated and the oxidation states are Mn(1) = IV, Mn(2) = IV, Mn(3) = III, Mn(4) = III; and (b) where the dangling manganese is hexacoordinated with an additional water and the oxidation states are Mn(1)=IV, Mn(2)=III, Mn(3)=III, Mn(4)=IV.

Figure 8

Comparison of calculated EXAFS spectra associated with the oxomanganese complex of PSII described by structures I, II, IIa, and III, proposed by Yano et al. [44] (green, black, dark yellow and blue, respectively), and model (a), obtained according to DFT QM/MM hybrid methods (red) [13,15,39].

Figure 9

DFT-QM/MM energy profiles, as a function of the coordination bond lengths between substrate water molecules attached to Ca²⁺ (red) and the dangling Mn³⁺ (black), for the OEC of PSII in the S₁ (dash) and S₂ (solid) states [18]. ESP ionic charges are indicated in parenthesis (q). The energy barriers are 21.2, 16.6, 8.4 and 7.9 kcal mol⁻¹, for water exchange from Ca²⁺(S₁), Ca²⁺(S₂), Mn³⁺(S₂) and Mn³⁺(S₁), respectively.

Figure 10

Comparison between experimental (red) [41] and calculated [39] (black) EXAFS spectra of OEC S-state intermediates of water splitting. Left: k-weighted EXAFS spectra. Right: Fourier-transformed spectra in r-space, showing three prominent peaks corresponding to scattering centers in the first (O,N), second (Mn in the core), and third (dangling Mn, Ca) coordination shells of Mn, respectively. Vertical dashed lines are included to facilitate the comparison.

Figure 11

Catalytic cycle of water splitting suggested by DFT QM/MM models of the OEC of PSII [39]. Dashed arrows in dark yellow indicate transformations leading to the following S-state in the cycle. Changes caused by an S-state transition are highlighted in red. The blue circles highlight substrate water molecules (also shown in blue). Coordination bonds elongated by Jahn-Teller distortions are marked in green. The orientation of the metal cluster corresponds to Figure 6, where Mn(1), Mn(2), Mn(3) and Mn(4) are indicated.

Figure 12

Proton exit channel suggested by the hydrated DFT QM/MM structural models, including a network of hydrogen bonds extended from substrate water molecules ’s’ (slow) and ’f’ (fast), via CP43-R357, to the first residue (D1-D61) leading to the lumenal side of the membrane [13,15,39]. Proton translocation events are indicated by blue and white arrows; the O=O bond formation event is indicated by a red arrow, as promoted by water exchange from Ca²⁺. Amino acid residues labeled with one-letter symbols correspond to the D1 protein subunit.