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Generalized approximate spin projection calculations of effective exchange integrals of the CaMn4O5 cluster in the S-1 and S-3 states of the oxygen evolving complex of photosystem II
Abstract
Full geometry optimizations followed by the vibrational analysis were performed for eight spin configurations of the CaMn4O4X(H2O)3Y (X = O, OH; Y = H2O, OH) cluster in the S1 and S3 states of the oxygen evolution complex (OEC) of photosystem II (PSII). The energy gaps among these configurations obtained by vertical, adiabatic and adiabatic plus zero-point-energy (ZPE) correction procedures have been used for computation of the effective exchange integrals (J) in the spin Hamiltonian model. The J values are calculated by the (1) analytical method and the (2) generalized approximate spin projection (AP) method that eliminates the spin contamination errors of UB3LYP solutions. Using J values derived from these methods, exact diagonalization of the spin Hamiltonian matrix was carried out, yielding excitation energies and spin densities of the ground and lower-excited states of the cluster. The obtained results for the right (R)- and left (L)-opened structures in the S1 and S3 states are found to be consistent with available optical and magnetic experimental results. Implications of the computational results are discussed in relation to (a) the necessity of the exact diagonalization for computations of reliable energy levels, (b) magneto-structural correlations in the CaMn4O5 cluster of the OEC of PSII, (c) structural symmetry breaking in the S1 and S3 states, and (d) the right- and left-handed scenarios for the O-O bond formation for water oxidation.
... bond formation to occur in the following steps. Similarly, there have been suggestions of isomorphism in the S 1 (S total = 0 and S total = 1) and S 3 states (S total = 3 and an undetermined higher spin state that is not detected by EPR), all of which are detected under cryogenic temperatures (Boussac et al. 2009, Cox et al. 2014, Lubitz et al. 2014, Isobe et al. 2014, Isobe et al. 2016, Shoji et al. 2018. The presence and population of the isomers in each S-state under physiological conditions remains to be established. ...
... In the S 2 state, EPR studies by several groups (Krewald et al. 2016, reviewed in (Haddy 2007, Pokhrel and Brudvig 2014) suggest the presence of isomorphous structures within the same redox/intermediate S-state, i.e. S 2 with a high-spin (HS, S total =5/2) and a low spin (LS, S total =1/2) form ( Fig. 1A, B). As discussed above, it has been proposed that such geometric and electronic structural flexibility in S 2 may play a role in the formation of the S 3 state through water binding (Ugur et al. 2016, Pantazis et al. 2012, Cox et al. 2013, Cox and Messinger 2013, Isobe et al. 2014, Boussac et al. 2018). Our XAS studies using synchrotron radiation (SR) at cryogenic temperature also shows differences in the geometric and electronic structure of the cryo-trapped HS and LS S 2 states (Chatterjee et al. 2016). ...
... Recently, density functional theory (DFT) calculations suggested theoretical structural models corresponding to the two spin states (Pantazis et al. 2012, Isobe et al. 2014, Bovi et al. 2013, Narzi et al. 2014) and concluded that the two spin states, LS S 2 and HS S 2 , are almost isoenergetic. Ab initio molecular dynamics simulations by Bovi et al. (2013) showed that they can interconvert over a low barrier (ΔG # of 10.6 kcal mol -1 ). ...
In nature, an oxo‐bridged Mn4CaO5 cluster embedded in Photosystem II (PSII), a membrane‐bound multi‐subunit pigment protein complex, catalyzes the water oxidation reaction that is driven by light‐induced charge separations in the reaction center of PSII. The Mn4CaO5 cluster accumulates four oxidizing equivalents to enable the four‐electron four‐proton catalysis of two water molecules to one dioxygen molecule and cycles through five intermediate S‐states, S0 – S4 in the Kok cycle. One important question related to the catalytic mechanism of the oxygen‐evolving complex (OEC) that remains is, whether structural isomers are present in some of the intermediate S‐states and if such equilibria are essential for the mechanism of the O‐O bond formation. Here we compare results from electron paramagnetic resonance (EPR) and X‐ray absorption spectroscopy (XAS) obtained at cryogenic temperatures for the S2 state of PSII with structural data collected of the S1, S2 and S3 states by serial crystallography at neutral pH (~6.5) using an X‐ray free electron laser at room temperature. While the cryogenic data demonstrate the presence of at least two structural forms of the S2 state, the room temperature crystallography data can be well‐described by just one S2 structure. We discuss the deviating results and outline experimental strategies for clarifying this mechanistically important question.
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... Recently, density functional theory (DFT) calculations by two groups suggest theoretical structural models corresponding to the two spin states 21,47 and conclude that the two spin states are almost isoenergetic. Ab initio molecular dynamics simulations by Bovi et al. showed that these two states could interconvert over a low barrier (DG # of 10.6 kcal mol À1 ). ...
... The HS and LS structural models that involve interconversion of the Mn III position in these two species have been proposed by Pantazis et al. 21 and Isobe et al. 47 based on EPR results and from quantum chemical calculations. In the LS S 2 , Mn III is located at the Mn D1 position that is ligated to His332 of D1 chain, while in the HS S 2 state Mn III is at the Mn A4 position of the cluster, which has two water ligands (Fig. S7 †). ...
... In these models, we kept the formal oxidation state assignment of each Mn as suggested by Pantazis et al. 21 and Isobe et al., 47 in which Mn III is located at the Mn D1 in LS S 2 form, while it is at the Mn A4 in HS form. Within our current knowledge, it is reasonable to think that the S total ¼ 1/2 being formed with anti-ferromagnetically-coupled Mn III and Mn IV along with two anti-ferromagnetically-coupled Mn IV , and S total ¼ 5/2 being formed with three ferro-magnetically coupled Mn IV in the cubane moiety with anti-ferromagnetically-coupled Mn III at Mn A4 . ...
The Mn4CaO5 cluster in photosystem II catalyzes the four-electron redox reaction of water oxidation in natural photosynthesis. This catalytic reaction cycles through four intermediate states (Si, i = 0 to 4), involving changes in the redox state of the four Mn atoms in the cluster. Recent studies suggest the presence and importance of isomorphous structures within the same redox/intermediate S-state. It is highly likely that geometric and electronic structural flexibility play a role in the catalytic mechanism. Among the catalytic intermediates that have been identified experimentally thus far, there is clear evidence of such isomorphism in the S2 state, with a high-spin (5/2) (HS) and a low spin (1/2) (LS) form, identified and characterized by their distinct electron paramagnetic resonance (EPR spectroscopy) signals. We studied these two S2 isomers with Mn extended X-ray absorption fine structure (EXAFS) and absorption and emission spectroscopy (XANES/XES) to characterize the structural and electronic structural properties. The geometric and electronic structure of the HS and LS S2 states are different as determined using Mn EXAFS and XANES/XES, respectively. The Mn K-edge XANES and XES for the HS form are different from the LS and indicate a slightly lower positive charge on the Mn atoms compared to the LS form. Based on the EXAFS results which are clearly different, we propose possible structural differences between the two spin states. Such structural and magnetic redox-isomers if present at room temperature, will likely play a role in the mechanism for water-exchange/oxidation in photosynthesis.
... 1.5 kcal mol −1 over the closed cubane, high-spin form. Similar conclusions were drawn by Bovi et al. [31] using QM/MM free energy calculations, and this has been central in subsequent mechanistic studies from several groups [30,[40][41][42]. ...
... Using computational studies based on the high resolution PSII structure, Isobe et al. [40,41] also provided evidence that like the S 2 state, the S 1 and S 3 states can exist in energetically accessible spin states that are structurally distinct. Recently, Retegan et al. [42] showed that neither the open nor the closed S 2 structure was able to undergo oxidation when Y Z • was present. ...
... In addition, the S 2 → S 3 transition of the previously suggested mechanism [35] does not seem immediately to conform to the suggestion of Narzi et al. [49] that a closed cubane/high spin form of S 2 is formed prior to formation of the S 3 state. The structure and energetics of the Mn 4 CaO 5 have been studied computationally by several research groups and this approach is playing an increasingly important role in establishing rigorous connections between the molecular structures and spectroscopic results [30,31,35,[40][41][42][43][44][45][46][47][48][49][50][51]. The combination of the high resolution structure, sophisticated spectroscopic methods and computational chemistry has made great progress in understanding the mechanism of biological water oxidation. ...
Photosystem II (PSII) catalyzes light-driven water splitting in nature and is the key enzyme for energy input into the biosphere. Important details of its mechanism are not well understood. In order to understand the mechanism of water splitting, we perform here large-scale density functional theory (DFT) calculations on the active site of PSII in different oxidation, spin and ligand states. Prior to formation of the O-O bond, we find that all manganese atoms are oxidized to Mn(IV) in the S3 state, consistent with earlier studies. We find here, however, that the formation of the S3 state is coupled to the movement of a calcium-bound hydroxide (W3) from the Ca to a Mn (Mn1 or Mn4) in a process that is triggered by the formation of a tyrosyl radical (Tyr-161) and its protonated base, His-190. We find that subsequent oxidation and deprotonation of this hydroxide on Mn1 result in formation of an oxyl-radical that can exergonically couple with one of the oxo-bridges (O5), forming an O-O bond. When O2 leaves the active site, a second Ca-bound water molecule reorients to bridge the gap between the manganese ions Mn1 and Mn4, forming a new oxo-bridge for the next reaction cycle. Our findings are consistent with experimental data, and suggest that the calcium ion may control substrate water access to the water oxidation sites.
... At room temperature, under turnover conditions, only the opencubane form has been observed crystallographically thus far. [6,36] While experimental data remains very limited, two synthetic CaMn 3 IV O 4 model complexes have been reported with S G = 9/2 ( Figure 2), [37][38][39] supporting the coupling scheme for the closedcubane structure and the possible structural flexibility of the OEC core as an explanation for the spin state interconversion observed in the S 2 state. Subsequent XFEL structural studies show the incorporation of a sixth oxygen O (6) in the cleft between Mn(1) and Mn(4), a possible site for O−O bond formation ( Figure 1). ...
... [17,24,41] Structural changes to the OEC through either oxo exchange or (de)protonation would be accompanied by concomitant changes in the nature and magnitude of the magnetic exchange coupling J, which in turn affect not only the S G of the cluster but also other spectroscopic properties such as the sign and magnitude of the projected 55 Mn hyperfine coupling constants. [15,39,44] In a related computational study, protonation of the bridging oxo O(4) (Figure 1) in the S 2 state is proposed to lead to a high spin state, while maintaining the open-cubane structure. [24] XAS studies performed on the high-spin form of the S 2 state indeed show structural differences to the low-spin form, but extracted Mn-Mn distances do not appear consistent with the closed-cubane structure. ...
We report the single crystal XRD and MicroED structure, magnetic susceptibility, and EPR data of a series of CaMn3IVO4 and YMn3IVO4 complexes as structural and spectroscopic models of the cuboidal subunit of the oxygen‐evolving complex (OEC). The effect of changes in heterometal identity, cluster geometry, and bridging oxo protonation on the spin‐state structure was investigated. In contrast to previous computational models, we show that the spin ground state of CaMn3IVO4 complexes and variants with protonated oxo moieties need not be S=9/2. Desymmetrization of the pseudo‐C3‐symmetric Ca(Y)Mn3IVO4 core leads to a lower S=5/2 spin ground state. The magnitude of the magnetic exchange coupling is attenuated upon oxo protonation, and an S=3/2 spin ground state is observed in CaMn3IVO3(OH). Our studies complement the observation that the interconversion between the low‐spin and high‐spin forms of the S2 state is pH‐dependent, suggesting that the (de)protonation of bridging or terminal oxygen atoms in the OEC may be connected to spin‐state changes.
... After the discovery of the high-resolution XRD structure ( Umena et al. 2011), our theoretical group ( Isobe et al. 2014) investigated formations of left-and right-opened Mn-oxo intermediates in the S 3 state by the QM(HDFT) calculations. Large-scale QM UB3LYP calculations ( Isobe et al. 2016) were applied for full geometry optimizations of possible nine intermediates in the S 3 state. ...
... Large-scale QM UB3LYP calculations ( Isobe et al. 2016) were applied for full geometry optimizations of possible nine intermediates in the S 3 state. Full geometry optimizations of the nine possible intermediates by large-scale quantum mechanics/molecular mechanics (QM/MM) methods (Shoji et al. 2019a(Shoji et al. , 2019b were also performed to refine our previous optimized structures ( Isobe et al. 2014Isobe et al. , 2016 in the S 3 state. Judging from the optimized O (5) -O (6) distances for the CaMn 4 O 6 cluster, the Mn-peroxide intermediate is a possible candidate for the SFX structure with the short (about 1.5 Å) O (5) -O (6) distance, whereas the Mn-oxo intermediate is a plausible candidate for the SFX structure with the moderate (about 2.1 Å) O (5) -O (6) distance. ...
The optimized geometries of the CaMn4OX (X=5, 6) cluster in the oxygen evolving complex (OEC) of photosystem II (PSII) by large‐scale quantum mechanics (QM) and molecular mechanics (MM) calculations are compared with recent serial femtosecond crystallography (SFX) results for the Si (i=0‐3) states. The valence states of four Mn ions by the QM/MM calculations are also examined in relation to the experimental results by the X‐ray emission spectroscopy (XES) for the Si intermediates. Geometrical and valence structures of right‐opened Mn‐hydroxide, Mn‐oxo and Mn‐peroxide intermediates in the S3 state are investigated in detail in relation to recent SFX and XES experiments for the S3 state. Interplay between theory and experiment indicates that the Mn‐oxo intermediate is a new possible candidate for the S3 state. Implications of the computational results are discussed in relation to possible mechanisms of the oxygen‐oxygen (OO) bond formation for water oxidation in OEC of PSII.
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... Six different spin structures (namely one HS, four IS and three LS configurations) of the four-site spin Hamiltonian model [32,87] were constructed at the UB3LYP level to determine the J ab values in Equation (7) from total energy differences of these structures. Judg- ing from the calculated J ab values, the Mn ions of the CaMn 4 O 5 cluster were cooperative to provide total septet (S = 3) ground state in the S 1 state; note that the refine- ment of the XRD structure [22] by the full geometry optimisation was necessary to obtain the singlet (S = 0) ground state [99]. The LS BS DFT (UB3LYP) calcula- tions were also performed for the S 3 state with the formal illustrated in Scheme 5. We thus have obtained sixth basic concept (BC VI) on the basis of the high-resolution XRD structure [22,32,33]. ...
... The possibility of O-O (or O-OH) bond formation in the S 3 state has been a classic problem extensively investigated by Renger [104] since electron-transfer (ET) dynamics experiments by his group [103] have indicated the maximum activation barrier in the S 3 state (see sup- porting section SIV) [107]. Our previous QM computa- tions [99,105,106] also indicated that several interme- diates with different ground spin states are feasible in the S 3 state. The EPR results for the S 3 state by Boussac et al. ...
Possible mechanisms for water cleavage in oxygen evolving complex (OEC) of photosystem II (PSII) have been investigated based on broken-symmetry (BS) hybrid DFT (HDFT)/def2 TZVP calculations in combination with available XRD, XFEL, EXAFS, XES and EPR results. The BS HDFT and the experimental results have provided basic concepts for understanding of chemical bonds of the CaMn4O5 cluster in the catalytic site of OEC of PSII for elucidation of the mechanism of photosynthetic water cleavage. Scope and applicability of the hybrid DFT (HDFT) methods have been examined in relation to relative stabilities of possible nine intermediates such as Mn-hydroxide, Mn-oxo, Mn-peroxo, Mn-superoxo, etc., in order to understand the O–O (O–OH) bond formation in the S3 and/or S4 states of OEC of PSII. The relative stabilities among these intermediates are variable, depending on the weight of the Hartree–Fock exchange term of HDFT. The Mn-hydroxide, Mn-oxo and Mn-superoxo intermediates are found to be preferable in the weak, intermediate and strong electron correlation regimes, respectively. Recent different serial femtosecond X-ray (SFX) results in the S3 state are investigated based on the proposed basic concepts under the assumption of different water-insertion steps for water cleavage in the Kok cycle. The observation of water insertion in the S3 state is compatible with previous large-scale QM/MM results and previous theoretical proposal for the chemical equilibrium mechanism in the S3 state . On the other hand, the no detection of water insertion in the S3 state based on other SFX results is consistent with previous proposal of the O–OH (or O–O) bond formation in the S4 state . Radical coupling and non-adiabatic one-electron transfer (NA-OET) mechanisms for the OO-bond formation are examined using the energy diagrams by QM calculations and by QM(UB3LYP)/MM calculations . Possible reaction pathways for the O–O and O–OH bond formations are also investigated based on two water-inlet pathways for oxygen evolution in OEC of PSII. Future perspectives are discussed in relation to post HDFT calculations of the energy diagrams for elucidation of the mechanism of water oxidation in OEC of PSII.
... The near degeneracy of the spin states in the monomeric and Ru-O 2 forms thus suggests that spin crossing may be involved in the nal steps of the watersplitting process with an interesting connection to the Mn 4 O 5 Ca of PSII, which also has near degenerate high and low spin states in key steps of its reaction cycle. [56][57][58][59][60] Moreover, similar to PSII, the O 2 species is likely to form via a radical coupling mechanism, 59,61,62 as indicated by a unit spin density on the oxygenous-ligand along the O-O bond formation process (Fig. 1, ESI-Fig. 3, ESI- Table 1 ...
Rational design of artificial water-splitting catalysts is central for developing new sustainable energy technology. However, the catalytic efficiency of the natural light-driven water-splitting enzyme, photosystem II, has been remarkably difficult to achieve artificially. Here we study the molecular mechanism of ruthenium-based molecular catalysts by integrating quantum chemical calculations with inorganic synthesis and functional studies. By employing correlated ab initio calculations, we show that the thermodynamic driving force for the catalysis is obtained by modulation of π-stacking dispersion interactions within the catalytically active dimer core, supporting recently suggested mechanistic principles of Ru-based water-splitting catalysts. The dioxygen bond forms in a semi-concerted radical coupling mechanism, similar to the suggested water-splitting mechanism in photosystem II. By rationally tuning the dispersion effects, we design a new catalyst with a low activation barrier for the water-splitting. The catalytic principles are probed by synthesis, structural, and electrochemical characterization of the new catalyst, supporting enhanced water-splitting activity under the examined conditions. Our combined findings show that modulation of dispersive interactions provides a rational catalyst design principle for controlling challenging chemistries.
... 5,39−41 Two structural isomers S 3 A (dimer-of-dimers) and S 3 B (trimer−monomer), both with S = 3 spin ground states, have been invoked for the S 3 state (Figure 1a). 5,42 A similar structural isomerism has been proposed for the S 2 state. 24,43 Such proposed structural changes may lead to differences in the sign and magnitude of the magnetic exchange interactions (J ij ) between adjacent Mn centers, which in turn affect not only the spin ground state of the cluster but also the observed sign and magnitude of the projected 55 Mn hyperfine interactions (A i ). ...
The S3 state is currently the last observable intermediate prior to O−O bond formation at the oxygen evolving complex (OEC) of Photosystem II, and its electronic structure has been assigned to a homovalent MnIV4 core with an S = 3 ground state. While structural interpretations based on the EPR spectroscopic features of the S3 state provide valuable mechanistic insight, corresponding synthetic and spectroscopic studies on tetranuclear complexes mirroring the Mn oxidation states of the S3 state remain rare. Herein, we report the synthesis and characterization by XAS and multifrequency EPR spectroscopy of a MnIV4O4 cuboidal complex as a spectroscopic model of the S3 state. Results show that this MnIV4O4 complex has an S = 3 ground state with isotropic 55Mn hyperfine coupling constants of −75, −88, −91, and 66 MHz. These parameters are consistent with an αααβ spin topology approaching the trimer-monomer magnetic coupling model of pseudo-octahedral MnIV centers. Importantly, the spin ground state changes from S = 1/2 to S = 3 as the OEC is oxidized from the S2 state to the S3 state. This same spin state change is observed following the oxidation of the previously reported MnIIIMnIV3O4 cuboidal complex to the MnIV4O4 complex described here. This sets a synthetic precedent for the observed low-spin to high-spin conversion in the OEC.
This paper reviews our historical developments of broken-symmetry (BS) and beyond BS methods that are applicable for theoretical investigations of metalloenzymes such as OEC in PSII. The BS hybrid DFT (HDFT) calculations starting from high-resolution (HR) XRD structure in the most stable S1 state have been performed to elucidate structure and bonding of whole possible intermediates of the CaMn4Ox cluster (1) in the Si (i = 0 ~ 4) states of the Kok cycle. The large-scale HDFT/MM computations starting from HR XRD have been performed to elucidate biomolecular system structures which are crucial for examination of possible water inlet and proton release pathways for water oxidation in OEC of PSII. DLPNO CCSD(T0) computations have been performed for elucidation of scope and reliability of relative energies among the intermediates by HDFT. These computations combined with EXAFS, XRD, XFEL, and EPR experimental results have elucidated the structure, bonding, and reactivity of the key intermediates, which are indispensable for understanding and explanation of the mechanism of water oxidation in OEC of PSII. Interplay between theory and experiments have elucidated important roles of four degrees of freedom, spin, charge, orbital, and nuclear motion for understanding and explanation of the chemical reactivity of 1 embedded in protein matrix, indicating the participations of the Ca(H2O)n ion and tyrosine(Yz)-O radical as a one-electron acceptor for the O–O bond formation. The Ca-assisted Yz-coupled O–O bond formation mechanisms for water oxidation are consistent with recent XES and very recent time-resolved SFX XFEL and FTIR results.
Water splitting is catalyzed by photosystem II, which comprises an inorganic core (CaMn4O5) and protein ligands. To understand the evolution of CaMn4O5 after attaching water molecules, an isolated CaMn4O5+ cluster was investigated using vibrational spectroscopy and density functional theory calculations. Computational findings suggest that when a water molecule adsorbs on the Ca atom through the O atom of water, one of the OH bonds forms a hydrogen bond with a μ-oxo bridge, which dissociates into two OH groups. This is consistent with the fact that no isomers with molecularly adsorbed water were experimentally observed.
Among many processes occurring in oxygenic photosynthesis, the water oxidation reaction catalyzed by the Mn4Ca cluster provides various types of insights into the field of the metal coordination chemistry. The water oxidation reaction in nature is carried out by Photosystem II (PS II), a multi subunit membrane protein complex. This light-driven reaction is made possible by a spatially separated, yet temporally connected series of cofactors along the electron transfer chain of PS II over 40 Å, through the donor—the Mn4CaO5 catalytic center, the reaction center chlorophylls, to the mobile quinone electron acceptors. Such chemical architecture provides an ideal platform to investigate how to control multi-electron/proton chemistry, using the flexibility of metal redox states, in coordination with the protein and the water network. Understanding the insights of nature's design gives inspiration of how to build artificial photosynthetic devices, where the controlled accumulation of charge and high-selectivity of products is currently challenging. The electronic and geometric structure of this catalyst have been extensively investigated, but its step-wise water oxidation mechanism is not yet completely understood. In this chapter, we summarize our current understanding of the water oxidation reaction in nature.
This review aims to summarize fundamental concepts and principles of isolobal and isospin analogy between organic and inorganic molecules with local spins. The isolobal analogy based on the extended Hückel (EH) molecular orbital (MO) model has been successfully applied for organic and organometallic compounds with closed-shell eight and eighteen electron rules. The EHMO with spatial symmetry has been employed for confirmation and elucidation of the orbital symmetry conservation rules for concerted reactions. On the other hand, the isospin analogy based on the Heisenberg spin Hamiltonian (HSH) model has been proposed for conceptual bridges between organic and inorganic open-shell molecules and clusters with the magnetic symmetry given by the spin rotation and time-reversal (spin inversion) symmetries. The spin-correlation diagrams by the HSH model are available for elucidation of exchange-allowed and -forbidden radical reactions. The broken-symmetry (BS) MO and density functional theory (DFT) models are constructed with spatial, spin rotation and time-reversal symmetries for open-shell species with one-dimensional (1D), 2D and 3D spin orbital structures. Both isolobal and isospin analogy based on the BS MO and DFT models have been applied for elucidation of electronic mechanisms of oxygenation reactions by active oxygen, oxyradicals and high-valent transition-metal oxo species with the oxyl-radical character. The isolobal and isospin analogy are also applicable for examination and investigation of possible mechanisms of the oxygen-oxygen (OO) bond formations for water oxidations catalyzed with the native CaMn4Ox cluster and artificial 3d transition-metal complexes. To this end, BS DFT methods have been applied to elucidate geometrical, electronic and spin structures of the CaMn4Ox (X = 5, 6) clusters in the Si (i = 1 ~ 4) states of the Kok cycle for water oxidation on the basis of the geometrical structures by the X-ray diffraction (XRD and SFX XFEL) methods. The computational results have been compared with spectroscopic (EXAFS, XES, EPR) results for elucidation of scope and reliability of the BS hybrid DFT followed by DLPNO-CCSD(T) level of theory for strongly correlated electron systems (SCES) such as the Mn and Fe-oxide complexes. Interplay between theory and experiment is effective and powerful for unraveling secrets of the water oxidation in OEC of PSII and related artificial systems. Fundamental concepts revealed by the interplay are applied to design of bio-inspired artificial Z-schemes for conversion of solar energy to chemical energy.
To better describe the Sn-state intermediates of Photosystem II, a ferromagnetically coupled CaMn3IVO4 subunit with an S=9/2 ground state has been proposed. This assignment has played a key role in the mechanism of water oxidation, but electronic-structure studies of CaMn3IVO4 complexes remain rare. Through cluster desymmetrization or oxo protonation, lower spin ground states are found to be accessible, challenging prior models.
Abstract
We report the single crystal XRD and MicroED structure, magnetic susceptibility, and EPR data of a series of CaMn3IVO4 and YMn3IVO4 complexes as structural and spectroscopic models of the cuboidal subunit of the oxygen-evolving complex (OEC). The effect of changes in heterometal identity, cluster geometry, and bridging oxo protonation on the spin-state structure was investigated. In contrast to previous computational models, we show that the spin ground state of CaMn3IVO4 complexes and variants with protonated oxo moieties need not be S=9/2. Desymmetrization of the pseudo-C3-symmetric Ca(Y)Mn3IVO4 core leads to a lower S=5/2 spin ground state. The magnitude of the magnetic exchange coupling is attenuated upon oxo protonation, and an S=3/2 spin ground state is observed in CaMn3IVO3(OH). Our studies complement the observation that the interconversion between the low-spin and high-spin forms of the S2 state is pH-dependent, suggesting that the (de)protonation of bridging or terminal oxygen atoms in the OEC may be connected to spin-state changes.
Full geometry optimization of all S2 intermediates in OEC (oxygen-evolving complex) of PSII (photosystem II) were carried out by using UB3LYP-D3/Def2-TZVP with COSMO solvation effects. Our detail calculations yielded meta-stable structures of six (=3 × 2 (HS (high-spin), IS (intermediate-spin)) intermediates for W1 = W2 = H2O and eight (=4 × 2 (HS, IS)) intermediates for W1 = OH⁻ or W2 = OH⁻, and were named to H2O and OH models, respectively. In the next step, relative stability among these intermediate structures were investigated by hybrid-DFT and DLPNO-CC methods. UB3LYP methods show that right (R)-opened structures (open-cubane) are more stable than left (L)-opened structures (closed-cubane) by about 3.5 kcal/mol, though decreasing of DFT-weights suppresses such energy gaps. DLPNO-CCSD(T0) methods promote stabilization of (L)-structures and finally reproduce near degeneration or more stable (L)-structure. All pattern of spin configurations in four Mn(III) and Mn(IV) ions were assumed and BS (broken-symmetry) solutions were successfully obtained to find the most stable spin structures. This complete sets of all spin conformations enabled us evaluate sets of effective exchange integrals J as magnetic coupling parameters. The calculated J values for the spin Hamiltonian elucidated one g2 (S = 1/2) and two g4 (S = 5/2) molecular structures in the S2 state in accord with the recent EXAFS results.
Fundamental concepts and basic theories for the broken-symmetry (BS) methods have been reviewed in relation to theoretical elucidation and understanding of the mechanism for water oxidation in the oxygen evolving complex (OEC) of photosystem II (PSII). The HOMO-LUMO mixings by the BS method have provided the BS orbitals which are mainly localized on the metal and oxygen sites of the high-valent transition-metal oxo (MO) bonds, respectively. The oxyl-radical character (M–O) is responsible for radical reactivity such as the radical coupling in accord with various experimental results. The Lewis acids play important roles for reduction of the oxyl-radical character, indicating the participation of the water-coordinated Ca(II) ion of the CaMn3O4 cubane to stabilization of the Mn(V)=O…Ca(II) bond for essentially non-radical reactions. Several chemical indices have been calculated to elucidate the radical character for quantitative purpose. Implications of the computational results are discussed in relation to possible mechanisms of water oxidation in OEC of PSII.
It is well known that unrestricted density functional theory (UDFT) calculations include spin contamination errors. While errors in UDFT/plane-wave calculations have not been clarified thus far, some effects of these errors are investigated. Recently, our group estimated spin contamination errors in UDFT/plane-wave calculation results by developing and applying the approximate spin projection (AP) scheme [Chem. Phys. Lett., 701: 103 (2018), Mol. Phys., 117: 2251 (2019), Molecules, 24: 505 (2019), Appl. Phys. Express, 12: 115506 (2019)]. In this study, a systematic theoretical investigation of the surface effects on the spin contamination error was performed. For this purpose, we selected model systems such as Au dimers, chains, and film adsorptions onto MgO and BaO (001) surfaces. The calculation results showed the dependence on the dimensions of the supported materials and lattice constants of the supports. In general, the effects of spin contamination errors are decreased by interaction with the surface. The effects of the errors increased by increasing dimension; i.e. the increasing order of spin contamination errors is film > chain > dimer. In addition, the spin-polarised states are stabilised because of the interaction with the surfaces, and spin contamination errors occur in some cases where the Au–Au distances are small.
The oxidation states of the Mn4CaO5 cluster of the photosynthetic oxygen-evolving complex remain controversial. New quantum chemical models for the dark-stable S1 state suggest that a low-valent Mn(III-IV-III-II) form, opposed to the commonly accepted high-valent Mn(III-IV-IV-III) assignment, agrees with available structural data. We examine the magnetic properties of the models and the consequences for electronic structure and catalytic progression of assuming a neutral second-sphere residue D1-His337. The low-valent model reproduces the experimental diamagnetic ground spin-state. However, the protonation assignment introduces a critical flaw because neutral His337 becomes itself the locus of subsequent oxidation, in contradiction to physiological catalytic progression.
Molecular quantum mechanics (MQM) investigations have been performed for elucidation of fundamental principles of the photo-induced water oxidation in oxygen evolving complex (OEC) of photosystem II (PSII). To this end, as a first theoretical step, broken symmetry (BS) quantum mechanics (QM) and QM(BS)/molecular mechanics (MM) calculations have been conducted for elucidation of geometrical, electronic and spin structures of the CaMn4Ox (X = 5, 6) cluster in the five steps Si (i = 0∼4) of the Kok cycle for water oxidation. The QM and QM/MM calculations have provided full optimised geometries of short-lived key intermediates and transition state structure for the O-O bond formation in the native solar-energy conversion. The interplay between theory and experiment have clearly indicated that the CaMn4O5 cluster in OEC of PSII exhibits typical physicochemical properties of strong correlation electron system (SCES) confined with effective protein field. Our QM and QM/MM computational results for key intermediates and transition structure for the O-O bond formation in the Kok cycle are now plentiful for derivation of fundamental principles (FP) for understanding of photo-induced water oxidation in OEC of PSII.
We summarize twenty nine fundamental principles (FPs) in systematic manner by QM and QM/MM calculations for understanding of water oxidation in Oxygen Evolving Complex(OEC) of Photosystem II(PSII). One of our final aims is theoretical design of the next-generation artificial photosystem materials composed of abundant metal ions.
Photosynthetic water oxidation takes place at the Mn cluster in photosystem II. During this process, several water molecules including four water ligands form a hydrogen bond network around the Mn cluster. To better elucidate the role of this network in the mechanisms underlying water oxidation, we examined the vibrational structure of the water molecules coupled with the Mn cluster using quantum mechanics/molecular mechanics (QM/MM) calculations. The OH vibrations of these water molecules in the hydrogen-bonding network between YZ and D1-D61 were simulated by the QM/MM simulations. The normal mode analysis showed that a broad positive feature at 2500–3200 cm⁻¹ in the experimental S2-minus-S1 difference spectrum was attributed to the OH stretching vibrations with the strong hydrogen bond interaction of water molecules around the Mn cluster, including those of water ligands coordinating with Mn and the in-phase coupled vibration among water molecules in the hydrogen bond network around the Mn cluster. In contrast, the bands in higher frequency (3500–3700 cm⁻¹) region were assigned to the OH stretching vibrations with weaker hydrogen bond interaction of water molecules in the network. These assignments strongly suggested that the in-phase mode among several water molecules may have a function to facilitate rapid proton transfer along the vibration direction using the Grotthuss mechanism. Thus, we proposed that the hydrogen bond network formed by several water molecules around the Mn cluster plays a key role in proton transfer during the water oxidation process.
The spin structure in the S2 state and the crystal structure of the manganese cluster of the oxygen evolving complex of plant photosystem II was combined by the quantitative evaluation of the magnetic anisotropy of the g = 4 signal. The g -values of 3.93 and 4.13 were obtained for the g = 4 signal in the directions parallel and perpendicular to the membrane normal, respectively. The peak-to-peak separations were 270 and 420 G for the parallel and perpendicular orientations to the membrane, respectively. By comparison with the crystal structure, the z-axis of the zero-field splitting was ascribed to the direction of the dangling Mn connecting water oxygen, Mn4-O(W1), in the manganese cluster. The results give the first experimental evidence that the valence of the dangling Mn is Mn(III) in the S2 high spin state. We showed the strong exchange coupling of Mn4 to Mn3 was required for g =4.1 spin state in the four spin couplings, estimated as > ~|-30 cm⁻¹|, indicating that the present closed cubane model in QM/MM calculation cannot explain the g = 4.1 spin structure. The onsite zero-field splitting of the dangling Mn was evaluated as –2.3 cm⁻¹ under the strong antiferromagnetic couplings (-50 cm⁻¹) with the dangling Mn to the cubane frame in the four coupled spin state. From the viewpoint of the arrangement of the Mn valences in the cluster, a closed cubane model is effective, but no large structural deviation from the S1 state crystal structure.
Domain-based local pair natural orbital (DLPNO) coupled cluster single and double (CCSD) methods with perturbative triples (T) correction with NormalPNO were used to compute energies for twelve different S1 structures of the CaMn4O5 cluster in the oxygen evolving complex (OEC) of photosystem II (PSII). The DLPNO-CCSD(T0) calculations with TightPNO for the important six structures among them revealed that the right (R)-opened S1XYZW structures were more stable than the corresponding left (L)-opened structures (X = O(5), Y = W2, Z = W1, and W = O(4)) of CaMn4O5. The three different S1 structures belonging to the R-opened type (S1acca, S1bbca, and S1abcb, where O2- = a, OH- = b and H2O = c) were found nearly degenerated in energy, indicating the possibility of the coexistence of different structures in the S1 state. The DLPNO-CCSD(T0) calculations with TightPNO supported the proposal of a dynamic equilibrium model based on the multi-intermediate structures for the S1 state, which is also in agreement with EPR and other experimental and hybrid DFT computational results. Implications of the computational results are discussed in relation to scope and applicability of NormalPNO and TightPNO for the CCSD(T0) calculations of strongly correlated electron systems such as 3d transition-metal complexes.
The fully optimized geometrical structures of the CaMn4Ox (x = 5, 6) clusters in the Si (i = 0–3) states of the Kok cycle of photosynthetic water oxidation by the large-scale quantum mechanics/molecular mechanics (QM/MM) calculations were compared to recent experimental results based on serial femtosecond crystallography (SFX). The MnMn and CaMn distances obtained by the QM/MM calculations were found to be totally comparable to the SFX experiments, elucidating the entire Kok cycle involving the S4 transition state during the OO bond formation for water oxidation in the oxygen evolving complex (OEC) of photosystem II (PSII).
Photosynthetic water oxidation is catalyzed by a Mn 4 CaO 5 -cluster in photosystem II through an S-state cycle. Understanding the roles of heterogeneity in each S-state, as identified recently by the EPR spectroscopy, is very important to gain a complete description of the catalytic mechanism. We performed herein hybrid DFT calculations within the broken-symmetry formalism and associated analyses of Heisenberg spin models to study the electronic and spin structures of various isomeric structural motifs (hydroxo-oxo, oxyl-oxo, peroxo, and superoxo species) in the S 3 state. Our extensive study reveals several factors that affect the spin ground state: (1) (formal) Mn oxidation state; (2) metal-ligand covalency; (3) coordination geometry; and (4) structural change of the Mn cluster induced by alternations in Mn···Mn distances. Some combination of these effects could selectively stabilize/destabilize some spin states. We found that the high spin state (S total = 6) of the oxyl-oxo species can be causative for catalytic function, which manifests through mixing of the metal-ligand character in magnetic orbitals at relatively short O5···O6 distances (<2.0 Å) and long Mn A ···O5 distances (>2.0 Å). These results will serve as a basis to conceptually identify and rationalize the physicochemical synergisms that can be evoked by the unique "distorted chair" topology of the cluster through cooperative Jahn-Teller effects on multimetallic centers.
QM(UB3LYP)/MM(AMBER) calculations were performed for the locations of the transition structure (TS) of the oxygen–oxygen (O–O) bond formation in the S4 state of the oxygen-evolving complex (OEC) of photosystem II (PSII). The natural orbital (NO) analysis of the broken-symmetry (BS) solutions was also performed to elucidate the nature of the chemical bonds at TS on the basis of several chemical indices defined by the occupation numbers of NO. The computational results revealed a concerted bond switching (CBS) mechanism for the oxygen–oxygen bond formation coupled with the one-electron transfer (OET) for water oxidation in OEC of PSII. The orbital interaction between the σ-HOMO of the Mn(IV)4–O(5) bond and the π*-LUMO of the Mn(V)1=O(6) bond plays an important role for the concerted O–O bond formation for water oxidation in the CaMn4O6 cluster of OEC of PSII. One electron transfer (OET) from the π-HOMO of the Mn(V)1=O(6) bond to the σ*-LUMO of the Mn(IV)4–O(5) bond occurs for the formation of electron transfer diradical, where the generated anion radical [Mn(IV)4–O(5)]⁻• part is relaxed to the •Mn(III)4 … O(5)⁻ structure and the cation radical [O(6)=Mn(V)1]⁺ • part is relaxed to the ⁺O(6)–Mn(IV)1• structure because of the charge-spin separation for the electron-and hole-doped Mn–oxo bonds. Therefore, the local spins are responsible for the one-electron reductions of Mn(IV)4->Mn(III)4 and Mn(V)1->Mn(IV)1. On the other hand, the O(5)⁻ and O(6)⁺ sites generated undergo the O–O bond formation in the CaMn4O6 cluster. The Ca(II) ion in the cubane- skeleton of the CaMn4O6 cluster assists the above orbital interactions by the lowering of the orbital energy levels of π*-LUMO of Mn(V)1=O(6) and σ*-LUMO of Mn(IV)4–O(5), indicating an important role of its Lewis acidity. Present CBS mechanism for the O–O bond formation coupled with one electron reductions of the high-valent Mn ions is different from the conventional radical coupling (RC) and acid-base (AB) mechanisms for water oxidation in artificial and native photosynthesis systems. The proton-coupled electron transfer (PC-OET) mechanism for the O–O bond formation is also touched in relation to the CBS-OET mechanism.
The effects of spin contamination errors on the activation barriers of catalytic NO reduction by TiO2/Ag and ZrO2/Cu core-shell catalyst models were investigated using an approximate spin projection method and an unrestricted density functional theory calculation with the plane-wave basis set. The estimated barrier of the TiO2/Ag system increased (0.03 eV), whereas that of the ZrO2/Cu system decreased (0.04 eV) after the correction of the spin contamination error. This difference in the estimated barriers of the two systems can be attributed to the difference in their surface structures. The error obtained for the TiO2/Ag system was larger than that obtained for the gas phase, i.e. the spin contamination error was induced by the molecule/surface interaction. Moreover, the error correction also changed the rate-determining step of ZrO2/Cu. These results demonstrate the importance of the correction of spin contamination errors for the detailed investigation of catalytic reactions.
Photosystem II (PSII) is a multisubunit membrane protein that plays a central role in oxygenic photosynthesis in plants, algae, and cyanobacteria. Ever since the structure of cyanobacterial PSII was solved at close to atomic resolution in 2011, with the details of the Mn4CaO5 cluster (WOC, water‐oxidation complex, or OEC, oxygen‐evolving complex), more detailed structural and spectroscopic studies together with the theoretical interpretations are emerging slowly. Yet, there are outstanding questions of its functions, which include its water‐oxidation mechanism catalyzed by the Mn4CaO5 cluster and the assembly mechanism of PSII. In this article, we give an update of the current knowledge of PSII, mainly regarding its structure, channels, and repair mechanism, and other related details.
The sunlight-powered oxidation of water by photosystem II (PSII) of algae, plants, and cyanobacteria underpins the energy conversion processes that sustain most of life on our planet. Understanding the structure and function of the “engine of life”, the oxygen-evolving complex (OEC) in the active site of PSII, has been one of the great and persistent challenges of modern science. Immense progress has been achieved in recent years through combined contributions of diverse disciplines and research approaches, yet the challenge remains. The improved understanding of the tetramanganese-calcium cluster of the OEC for the experimentally accessible catalytic states often creates a more complex picture of the system than previously imagined, while the various strands of evidence cannot always be unified into a coherent model. This review focuses on selected current problems that relate to structural–electronic features of the OEC, emphasizing conceptual aspects and highlighting topics of structure and function that remain uncertain or controversial. The Mn4CaOx cluster of the OEC cycles through five redox states (S0–S4) to store the oxidizing equivalents required for the final step of dioxygen evolution in the spontaneously decaying S4 state. Remarkably, even the dark-stable state of the OEC, the S1 state, is still incompletely understood because the available structural models do not fully explain the complexity revealed by spectroscopic investigations. In addition to the nature of the dioxygen-evolving S4 state and the precise mechanism of O–O bond formation, major current open questions include the type and role of structural heterogeneity in various intermediate states of the OEC, the sequence of events in the highly complex S2–S3 transition, the heterogeneous nature of the S3 state, the accessibility of substrate or substrate analogues, the identification of substrate oxygen atoms, and the role of the protein matrix in mediating proton removal and substrate delivery. These open questions and their implications for understanding the principles of catalytic control in the OEC must be convincingly addressed before biological water oxidation can be understood in its full complexity on both the atomic and the systemic levels.
Atmospheric oxygenation and evolution of aerobic life on our earth are a result of water oxidation by oxygenic photosynthesis in photosystem II (PSII) of plants, algae, and cyanobacteria. The water oxidation in the oxygen-evolving complex (OEC) of PSII is expected to proceed through five oxidation states, known as the Si (i = 0, 1, 2, 3, and 4) states in the Kok cycle, with the S1 being the most stable state in the dark. The OEC in PSII involves the active catalytic site made of four Mn ions and one Ca ion, namely the CaMn4O5 cluster. Past decades, molecular structures of the CaMn4O5 cluster in OEC of PSII have been investigated by the extended X-ray absorption fine structure (EXAFS). The magnetostructural correlations were extensively investigated by EPR spectroscopy. Recently, Kamiya and Shen groups made a great breakthrough for determination of the S1 structure of OEC of PSII by the X-ray diffraction (XRD) and X-ray free electron laser (XFEL) experiments, providing structural foundations that are crucial for theoretical investigations of structure and reactivity of the CaMn4O5 cluster. Large-scale QM/MM calculations starting from the XRD structures elucidated geometrical, electronic, and spin structures of the CaMn4O5 cluster, indicating an important role of the Jahn–Teller (JT) effect of Mn(III) ions. This review fully examines our theoretical formulae for estimation of the Jahn–Teller deformations of the CaMn4O5 cluster in OEC of PSII. Scope and applicability of the JT deformation formulae are elucidated in relation to several different structures of the CaMn4O5 cluster proposed by XRD, XFEL, EXAFS, and other experiments. Subtle differences among XRD, XFEL, and EXAFS structures in the S1 state are examined in relation to environmental effects for the CaMn4O5 cluster in OEC of PSII. The X-ray damage of the serial femtosecond crystallography (SFX) by XFEL is also examined in relation to the damage-free low-dose (LD) XRD structure. The JT deformation formulae are also applied to theoretical analysis of the S3 structures by SFX. Implications of the computational results are discussed for further refinements of geometrical parameters of the CaMn4O5 cluster in OEC of PSII and possible mechanisms of water oxidation in OEC of PSII.
Spin contamination error in the total energy of the Au2/MgO system was estimated using the density functional theory/plane-wave scheme and approximate spin projection methods. This is the first investigation in which the errors in chemical phenomena on a periodic surface are estimated. The spin contamination error of the system was 0.06 eV. This value is smaller than that of the dissociation of Au2 in the gas phase (0.10 eV). This is because of the destabilization of the singlet spin state due to the weakening of the Au-Au interaction caused by the Au-MgO interaction.
In Photosystem II (PSII), the Mn4CaO5-cluster of the active site advances through five sequential oxidation states (S0to S4) before water is oxidized and O2is generated. Here, we have studied the transition between the low spin (LS) and high spin (HS) configurations of S2using EPR spectroscopy, quantum chemical calculations using Density Functional Theory (DFT), and time-resolved UV-visible absorption spectroscopy. The EPR experiments show that the equilibrium between S2LSand S2HSis pH dependent, with a pKa ≈ 8.3 (n ≈ 4) for the native Mn4CaO5and pKa ≈ 7.5 (n ≈ 1) for Mn4SrO5. The DFT results suggest that exchanging Ca with Sr modifies the electronic structure of several titratable groups within the active site, including groups that are not direct ligands to Ca/Sr, e.g., W1/W2, Asp61, His332 and His337. This is consistent with the complex modification of the pKaupon the Ca/Sr exchange. EPR also showed that NH3addition reversed the effect of high pH, NH3-S2LSbeing present at all pH values studied. Absorption spectroscopy indicates that NH3is no longer bound in the S3TyrZstate, consistent with EPR data showing minor or no NH3-induced modification of S3and S0. In both Ca-PSII and Sr-PSII, S2HSwas capable of advancing to S3at low temperature (198 K). This is an experimental demonstration that the S2LSis formed first and advances to S3via the S2HSstate without detectable intermediates. We discuss the nature of the changes occurring in the S2LSto S2HStransition which allow the S2HSto S3transition to occur below 200 K. This work also provides a protocol for generating S3in concentrated samples without the need for saturating flashes.
This account describes a current summary of our computational studies intended to elucidate the mechanism underlying water oxidation by the tetranuclear Mn cluster in the oxygen-evolving complex of photosystem II, the most fundamental bioenergetic process required for the maintenance of life. We focus herein on several important findings about the relatively high oxidation (S2 and S3) states of the cluster that involve three or four MnIV and one or no MnIII ions. The presentation is designed to highlight how the cluster stores the oxidizing power, binds substrate water molecules, and activates them. We discuss the fundamental importance of the cooperative effects of multiple Jahn–Teller axes on MnIII ions, which inevitably deform the cluster structure in such a direction as to promote substrate binding during S2 → S3 transition and O–O bond formation in the S3 state. Our interpretation is that the “distorted chair” topology of the cluster is the heart of efficient catalysis for oxygen evolution, and the presentation attempts to reflect this view.
The accurate description of magnetic level energetics in oligonuclear exchange-coupled transition metal complexes remains a formidable challenge for quantum chemistry. The density matrix renormalization group (DMRG) brings such systems for the first time easily within reach of multireference wave function methods by enabling the use of unprecedentedly large active spaces. But does this guarantee systematic improvement in predictive ability, and if so, under which conditions? We identify operational parameters in the use of DMRG using as a test system an experimentally characterized mixed valence bis-μ-oxo/μ-acetato Mn(III,IV) dimer, a model for the oxygen-evolving complex of photosystem II. A complete active space of all metal 3d and bridge 2p orbitals proved to be the smallest meaningful starting point; this is readily accessible with DMRG and greatly improves on the unrealistic metal-only configuration interaction or complete active space self-consistent field (CASSCF) values. Orbital optimization is critical for stabilizing the antiferromagnetic state, while a state-averaged approach over all spin states involved is required to avoid artificial deviations from isotropic behavior that are associated with state-specific calculations. Selective inclusion of localized orbital subspaces enables probing the relative contributions of different ligands and distinct superexchange pathways. Overall, however, full-valence DMRG-CASSCF calculations fall short from providing a quantitative description of the exchange coupling owing to insufficient recovery of dynamic correlation. Quantitatively accurate results can be achieved through a DMRG implementation of second order N-electron valence perturbation theory (NEVPT2) in conjunction with a full-valence metal and ligand active space. Perspectives for future applications of DMRG-CASSCF/NEVPT2 to exchange coupling in oligonuclear clusters are discussed.
Dioxygen formation mechanism of biological water oxidation in nature has long been the focus of arguments, where great diversities of mechanistic hypotheses have appeared. Based on the recent breakthrough in resolution of electronic and structural properties of the oxygen-evolving complex in the S3 state, our density functional theory (DFT) calculations reveal that the open-cubane oxo-oxyl coupling mechanism, whose substrates are preferably originated from W2 and O5 in the S2 state, emerges as the best candidate for O-O bond formation in the S4 state. This is justified by its overwhelming energetic superiority over alternative mechanisms in both isomeric open and closed-cubane forms of the Mn4CaO5 cluster, with spin-dependent reactivity rooted in variable magnetic couplings found to play an essential role. Importantly, this oxygen evolution style is supported by the new femtosecond X-ray free electron lasers (XFEL) discovery, and the origin of reported structural changes from the S1 to S3 state are analyzed. In this view, we corroborate the proposed water binding mechanism during S2-S3 transition and correlate the theoretical models with experimental findings from aspects of substrate selectivity according to the water exchange kinetics. This theoretical consequence on the native metalloenzyme may serve as a significant guidance for improvement of design and synthesis of biomimetic materials in the field of photocatalytic water splitting.
The O2-producing Mn4CaO5 catalyst in Photosystem II oxidizes two water molecules (substrate) to produce one O2 molecule. Considerable evidence supports identifying one of the two substrate waters as the Mn4CaO5 cluster's oxo bridge known as O5. The identity of the second substrate water molecule is less clear. In one set of models, the second substrate is the Mn-bound water molecule known as W2. In another set of models, the second substrate is the Ca2+-bound water molecule known as W3. In all of these models, a deprotonated form of the second substrate moves to a position next to O5 during the catalytic step immediately prior to O-O bond formation. In this study, FTIR difference spectroscopy was employed to identify the vibrational modes of hydrogen-bonded water molecules that are altered by the substituting Sr2+ for Ca2+. Our data show that the substitution substantially altered the vibrational modes of only a single water molecule: the water molecule whose D-O-D bending mode is eliminated during the catalytic step immediately prior to O-O bond formation. These data are most consistent with identifying the Ca2+-bound W3 as the second substrate involved in O-O bond formation.
Atmospheric oxygenation and evolution of aerobic life on our earth are a result of water oxidation by oxygenic photosynthesis in photosystem II (PSII) of plants, algae and cyanobacteria. The water oxidation in the oxygen-evolving complex (OEC) in PSII is expected to proceed through five oxidation states, known as the Si (i = 0, 1, 2, 3 and 4) states in the Kok cycle, with the S1 being the most stable state in the dark. The OEC in PSII involves the active catalytic site made of four Mn ions and one Ca ion, namely the CaMn4O5 cluster. Past decades, molecular structures of the CaMn4O5 cluster in OEC in PSII have been investigated by the extended X-ray absorption fine structure (EXAFS). The magneto-structural correlations were extensively investigated by electron paramagnetic resonance (EPR) spectroscopy. Recently, Kamiya and Shen groups made great breakthrough for determination of the S1 structure of OEC of PSII by the X-ray diffraction (XRD) and X-ray free-electron laser (XFEL) experiments, providing structural foundations that are crucial for theoretical investigations of the CaMn4O5 cluster. Large-scale quantum mechanics/molecular mechanics calculations starting from the XRD structures elucidated geometrical, electronic and spin structures of the CaMn4O5 cluster, indicating an important role of the Jahn–Teller (JT) effect of Mn(III) ions. This paper presents theoretical formulas for estimation of the JT deformations of the CaMn4O5 cluster in OEC of PSII. Scope and applicability of the formulas are examined in relation to several different structures of the CaMn4O5 cluster proposed by XRD, XFEL, EXAFS and other experiments. Implications of the computational results are discussed for further refinements of geometrical parameters of the CaMn4O5 cluster.
Large-scale QM/MM calculations were performed to elucidate an optimized geometrical structure of a CaMn4O5 cluster with and without water insertion in the S3 state of the oxygen evolving complex (OEC) of photosystem II (PSII). The left (L)-opened structure was found to be stable under the assumption of no hydroxide anion insertion in the S3 state, whereas the right (R)-opened structure became more stable if one water molecule is inserted to the Mn4Ca cluster. The optimized Mna(4)-Mnd(1) distance determined by QM/MM was about 5.0 Å for the S3 structure without an inserted hydroxide anion, but this is elongated by 0.2-0.3 Å after insertion. These computational results are discussed in relation to the possible mechanisms of O-O bond formation in water oxidation by the OEC of PSII.
Large-scale QM/MM calculations including hydrogen-bonding networks in the oxygen evolving complex (OEC) of photosystem II (PSII) were performed to elucidate the geometric structures of the CaMn4O5 cluster in the key catalytic states (Si (i=0-3)). The optimized Mn-Mn, Ca-Mn and Mn-O distances by the large-scale QM/MM starting from the high-resolution XRD structure were consistent with those of the EXAFS experiments in the dark stable S1 state by the Berkeley and Berlin groups. The optimized geometrical parameters for other Si (i=0, 2, 3) states were also consistent with those of EXAFS, indicating the importance of the large-scale QM/MM calculations for the PSII-OEC.
Water oxidation by photosystem II (PSII) converts light energy into chemical energy with the concomitant production of molecular oxygen, both of which are indispensable for sustaining life on Earth. This reaction is catalyzed by an oxygen-evolving complex (OEC) embedded in the huge PSII complex, and its mechanism remains elusive in spite of the extensive studies of the geometric and electronic structures. In order to elucidate the water-splitting mechanism, synthetic approaches have been extensively employed to mimic the native OEC. Very recently, a synthetic complex [Mn4CaO4(Bu(t)COO)8(py)(Bu(t)COOH)2] () closely mimicking the structure of the native OEC was obtained. In this study, we extensively examined the geometric, electronic and spin structures of using the density functional theory method. Our results showed that the geometric structure of can be accurately reproduced by theoretical calculations, and revealed many similarities in the ground valence and spin states between and the native OEC. We also revealed two different valence states in the one-electron oxidized state of (corresponding to the S2 state), which lie in the lower and higher ground spin states (S = 1/2 and S = 5/2), respectively. One remarkable difference between and the native OEC is the presence of a non-negligible antiferromagnetic interaction between the Mn1 and Mn4 sites, which slightly influenced their ground spin structures (spin alignments). The major reason causing the difference can be attributed to the short Mn1-O5 and Mn1-Mn4 distances in . The introduction of the missing O4 atom and the reorientation of the Ca coordinating ligands improved the Mn1-O5 and Mn1-Mn4 distances comparable to the native OEC. These modifications will therefore be important for the synthesis of further advanced model complexes more closely mimicking the native OEC beyond .
Photosynthetic water oxidation takes place at the Mn4CaO5 cluster in photosystem II. Around the Mn4CaO5 cluster, a hydrogen bond network is formed by several water molecules including four water ligands. To clarify the role of this water network in the mechanism of water oxidation, we investigated the effects of the removal of Ca2+ and substitution to metal ions on the vibrations of water molecules coupled to the Mn4CaO5 cluster by means of Fourier transform infrared (FTIR) difference spectroscopy and quantum mechanics/molecular mechanics (QM/MM) calculations. The OH stretching vibrations of nine water molecules forming a network between D1-Glu61 and YZ were calculated using the QM/MM method. Based on the calculated normal modes, a broad positive feature at 3200-2500 cm-1 in an S2-minus-S1 FTIR spectrum was attributed to the vibrations of strongly hydrogen-bonded OH bonds of water involving the vibrations of water ligands to a Mn ion and the in-phase coupled vibration of a water network connected to YZ, while bands in the 3700-3500 cm-1 region were assigned to the coupled vibrations of weakly hydrogen-bonded OH bonds of water. All the water bands were lost upon Ca2+ depletion and Ba2+ substitution, which inhibit the S2→S3 transition, indicating that a solid water network was broken by these treatments. By contrast, Sr2+ substitution slightly altered the water bands around 3600 cm-1, reflecting minor modification in water interactions, consistent with the retention of water oxidation activity with a decreased efficiency. These results suggest that the water network around the Mn4CaO5 cluster plays an essential role in the water oxidation mechanism particularly in a concerted process of proton transfer and water insertion during the S2→S3 transition.
Magneto-structural correlations in oxygen-evolving complex (OEC) of photosystem II (PSII) have been elucidated on the basis of theoretical and computational results in combination with available electron paramagnetic resonance (EPR) experimental results, and extended x-ray absorption fine structure (EXAFS) and x-ray diffraction (XRD) results. To this end, the computational methods based on broken-symmetry (BS) UB3LYP solutions have been developed to elucidate magnetic interactions in the active manganese catalyst for water oxidation by sunlight. The effective exchange interactions J for the CaMn(III)Mn(IV)3O5(H2O)3Y(Y = H2O or OH−) cluster (1) model of OEC of PSII have been calculated by the generalised approximate spin projection (GAP) method that eliminates the spin contamination errors of the BS UB3LYP solution. Full geometry optimisations followed by the zero-point energy (ZPE) correction have been performed for all the spin configurations of 1 to improve the J values that are compared with accumulated EPR in the S2 state of Kok cycle and magnetic susceptibility results of Christou model complex Ca2Mn(IV)3O4 (2). Using the calculated J values, exact diagonalisation of the spin Hamiltonian matrix has been carried out to obtain excitation energies and spin densities of the ground and lower excited states of 1. The calculated excitation energies are consistent with the available experimental results. The calculated spin densities (projection factors) are also compatible with those of the EPR results. The calculated spin densities have been used to calculate the isotropic hyperfine (Aiso) constants of 55Mn ions revealed by the EPR experiments. Implications of the computational results are discussed in relation to the structural symmetry breaking (SSB) in the S1, S2 and S3 states, spin crossover phenomenon induced by the near-infrared excitation and the right- and left-handed scenarios for the O–O bond formation for water oxidation.
In order to confirm theoretical system models of photosystem II (PSII), quantum mechanics (QM)/molecular mechanics (MM) calculations using a large-scale QM model (QM Model V) have been performed to elucidate hydrogen bonding networks and proton wires for proton release pathways (PRPs) of water oxidation reaction in the oxygen-evolving complex (OEC) of PSII. Full geometry optimizations of PRP by the QM/MM model have been carried out starting from the geometry of heavy atoms determined by the recent high-resolution X-ray diffraction (XRD) experiment on PSII refined to 1.9Å resolution. The optimized MnMn and CaMn distances by large-scale QM/MM are consistent with the EXAFS results, removing out the discrepancy between the refined XRD and EXAFS. Computational results from QM/MM calculations have demonstrated the labile nature of the MnaO(5)Mnd bond of the CaMn4O5 cluster in the OEC of PSII which allows left (L)-opened, quasi-central (CQ)-, and right (R)-opened structures. This confirms the feasibility of the left- and right-hand scenarios for water oxidation in the OEC of PSII that are dependent on the hydrogen bonding networks. The QM/MM computations have elucidated the networks structures: hydrogen bonding O. . .O(N) and O. . .H distances and O(N)H. . .O angles in PRP, together with the ClO(N) and Cl. . .H distances and O(N)H. . .Cl angles for chloride anions. The obtained hydrogen bonding networks are fully consistent with the results from XRD and available experiments such as EXAFS, showing the reliability of our theoretical system model that is crucial for investigations of functions of PSII such as water oxidation. The QM/MM computations have elucidated possible roles of chloride anions in OEC of PSII for proton transfers. The QM/MM computational results have provided useful information for the understanding and explanation of several experimental results obtained with mutants of the OEC of PSII. The possible implications of the present results are discussed in relation to our theoretical system models of PSII, strong or weak perturbations of the system structures by mutations, damage-free X-ray free-electron laser structure of PSII, and bioinspired working hypotheses for the development of artificial water oxidation systems which use 3d transition metal complexes.
Several key concepts and geometrical rules for the Mn–Mn and Mn–O distances of the CaMn4O5 cluster in the oxygen evolving complex (OEC) of photosystem II (PSII) by previous and present theoretical calculations were examined for a clear understanding of the damage-free S1 structure revealed by X-ray free electron laser (XFEL). A simple equation to estimate the Mna–Mnb distance in relation to the Mna–O(5) distance was derived taking into consideration the Jahn–Teller (JT) effects for Mn centers, indicating that the XFEL structure is regarded as a slightly right-elongated quasi-central structure in contradiction to a right-opened structure proposed by the EXAFS measurements.
The site for water oxidation in Photosystem II (PSII) goes through five sequential oxidation states (S0 to S4) before O2 is evolved. It consists of a Mn4CaO5-cluster close to a redox-active tyrosine residue (YZ). Cl(-) is also required for enzyme activity. By using EPR spectroscopy it has been shown that both Ca(2+)/Sr(2+) exchange and Cl(-)/I(-) exchange perturb the proportions of centres showing high (S=5/2) and low spin (S=1/2) forms of the S2-state. The S3-state was also found to be heterogeneous with: i) a S=3 form that is detectable by EPR and not sensitive to near-infrared light; and ii) a form that is not EPR visible but in which Mn photochemistry occurs resulting in the formation of a (S2YZ(•))' split EPR signal upon near-infrared illumination. In Sr/Cl-PSII, the high spin (S=5/2) form of S2 shows a marked heterogeneity with a g=4.3 form generated at low temperature that converts to a relaxed form at g=4.9 at higher temperatures. The high spin g=4.9 form can then progress to the EPR detectable form of S3 at temperatures as low as 180K whereas the low spin (S=1/2) S2-state can only advance to the S3 state at temperatures≥235K. Both of the two S2 configurations and the two S3 configurations are each shown to be in equilibrium at≥235K but not at 198K. Since both S2 configurations are formed at 198K, they likely arise from two specific populations of S1. The existence of heterogeneous populations in S1, S2 and S3 states may be related to the structural flexibility associated with the positioning of the oxygen O5 within the cluster highlighted in computational approaches and which has been linked to substrate exchange. These data are discussed in the context of recent in silico studies of the electron transfer pathways between the S2-state(s) and the S3-state(s).
Copyright © 2015. Published by Elsevier B.V.
Quantum mechanical (QM)/molecular mechanics (MM) calculations by the use of a large-scale QM model (QM Model V) have been performed to elucidate hydrogen-bonding networks and proton wires for proton release pathways (PRP) of water oxidation reaction in the oxygen evolving complex (OEC) of photosystem II (PSII). Full geometry optimisations of PRP by the QM/MM model have been carried out starting from the geometry of heavy atoms determined by the recent high-resolution X-ray diffraction (XRD) experiment of PSII refined to 1.9 Å resolution. Computational results by the QM/MM calculations have elucidated the hydrogen-bonding O···O(N) and O···H distances and O(N)–H···O angles in PRP, together with the Cl–O(N) and Cl···H distances and O(N)–H···Cl angles for chloride anions. The optimised hydrogen-bonding networks are well consistent with the XRD results and available experiments such as extended X-ray absorption fine structure, showing the reliability of channel structures of OEC of PSII revealed by the XRD experiment. The QM/MM computations have elucidated possible roles of chloride anions in the OEC of PSII. The QM/MM computational results have provided useful information for understanding and explanation of accumulated mutation experiments of key amino acid residues in the OEC of PSII. Implications of the present results are discussed in relation to three steps for theoretical modelling of water oxidation in the OEC of PSII and bio-inspired working hypotheses for developments of artificial water oxidation systems by use of 3d transition-metal complexes.
The structure of the oxygen evolving complex (OEC) of photosystem II (PSII) was recently analyzed by crystallography at 1.95 Å resolution using X-ray free electron laser (XFEL), but the positions of hydrogen atoms were not determined. We have examined the XFEL structure theoretically under the assumption of four protonation cases. The spin densities obtained by the high-spin UB3LYP revealed that a partial internal reduction of the high-valent Mn ions in the CaMn4O4X(H2O)3Y cluster occurs for the O(5)(=X) = O2− case, entailing its protonation (X = OH−) in the XFEL structure.
Cytb559 in Photosystem II is a heterodimeric b-type cytochrome. The subunits, PsbE and PsbF, consist each in a membrane α-helix. Roles for Cytb559 remain elusive. In Thermosynechococcus elongatus, taking advantage of the robustness of the PSII variant with PsbA3 as the D1 subunit (WT*3), 4 mutants were designed hoping to get mutants nevertheless the obligatory phototrophy of this cyanobacterium. In two of them, an axial histidine ligand of the haem-iron was substituted for either a methionine, PsbE/H23M, which could be potentially a ligand or for an alanine, PsbE/H23A, which cannot. In the other mutants, PsbE/Y19F and PsbE/T26P, the environment around PsbE/H23 was expected to be modified. From EPR, MALDI-TOF and O2 evolution activity measurements, the following results were obtained: Whereas the PsbE/H23M and PsbE/H23A mutants assemble only an apo-Cytb559 the steady-state level of active PSII was comparable to that in WT*3. The lack of the haem or, in PsbE/T26P, conversion of the high-potential into a lower potential form, slowed-down the recovery rate of the O2 activity after high-light illumination but did not affect the photoinhibition rate. This resulted in the following order for the steady-state level of active PSII centers under high-light conditions: PsbE/H23M≈PsbE/H23A< PsbE/Y19F≤PsbE/T26P≤WT*3. These data show i) that the haem has no structural role provided that PsbE and PsbF are present, ii) a lack of correlation between the rate of photoinhibition and the Em of the haem and iii) that the holo-Cytb559 favors the recovery of a functional enzyme upon photoinhibition.
Copyright © 2014. Published by Elsevier B.V.
The oxygen-evolving complex (OEC) in the membrane-bound protein complex photosystem II (PSII) catalyzes the water oxidation reaction that takes place in oxygenic photosynthetic organisms. We investigated the structural changes of the Mn4CaO5 cluster in the OEC during the S state transitions using x-ray absorption spectroscopy (XAS). Overall structural changes of the Mn4CaO5 cluster, based on the manganese ligand and Mn-Mn distances obtained from this study, were incorporated into the geometry of the Mn4CaO5 cluster in the OEC obtained from a polarized XAS model and the 1.9-Å high resolution crystal structure. Additionally, we compared the S1 state XAS of the dimeric and monomeric form of PSII from Thermosynechococcus elongatus and spinach PSII. Although the basic structures of the OEC are the same for T. elongatus PSII and spinach PSII, minor electronic structural differences that affect the manganese K-edge XAS between T. elongatus PSII and spinach PSII are found and may originate from differences in the second sphere ligand atom geometry.
Background: Mn4CaO5 cluster catalyzes water oxidation in photosystem II.
Results: Mn-Mn/Ca/ligand distances and changes in the structure of the Mn4CaO5 cluster are determined for the intermediate states in the reaction using x-ray spectroscopy.
Conclusion: Position of one bridging oxygen and related geometric changes may be critical during catalysis.
Significance: Knowledge about structural changes during catalysis is crucial for understanding the O–O bond formation mechanism in PSII.
Oxygen-evolving complex of photosystem II (PSII) is a tetra-manganese calcium penta-oxygenic cluster (MnCaO) catalyzing light-induced water oxidation through several intermediate states (S-states) by a mechanism that is not fully understood. To elucidate the roles of Ca in this cluster and the possible location of water substrates in this process, we crystallized Sr-substituted PSII from Thermosynechococcus vulcanus, analyzed its crystal structure at a resolution of 2.1 Å, and compared it with the 1.9 Å structure of native PSII. Our analysis showed that the position of Sr was moved toward the outside of the cubane structure of the MnCaO-cluster relative to that of Ca, resulting in a general elongation of the bond distances between Sr and its surrounding atoms compared with the corresponding distances in the Ca-containing cluster. In particular, we identified an apparent elongation in the bond distance between Sr and one of the two terminal water ligands of Ca, W3, whereas that of the Sr-W4 distance was not much changed. This result may contribute to the decrease of oxygen evolution upon Sr-substitution, and suggests a weak binding and rather mobile nature of this particular water molecule (W3), which in turn implies the possible involvement of this water molecule as a substrate in the O-O bond formation. In addition, the PsbY subunit, which was absent in the 1.9 Å structure of native PSII, was found in the Sr-PSII structure.
Multi-core oxomanganese complexes can adopt different oxidation states and protonation patterns depending on ligands and external conditions (for example, solvent, pH, and redox potential). An archetypical example of such complexes is the Mn(4)Ca cluster in the oxygen-evolving complex (OEC) of photosystem II (PSII). Despite the recent high-resolution crystal structure of PSII, some uncertainty about the oxidation state of the Mn centers and the protonation pattern of the oxygen atoms bridging the metals still exists. In this work, we construct a quantum-chemically based tool to "recognize'' the oxidation state and the protonation pattern of oxomanganese complexes from their experimental structure. Combined with simple structural information, our tool can be employed as an empirical guideline to recognize the oxidation state and/or the protonation pattern of those oxomanganese complexes for which this information is not experimentally available.
The laboratory synthesis of the oxygen-evolving complex (OEC) of photosystem II has been the objective of synthetic chemists since the early 1970s. However, the absence of structural information on the OEC has hampered these efforts. Crystallographic reports on photosystem II that have been appearing at ever-improving resolution over the past ten years have finally provided invaluable structural information on the OEC and show that it comprises a [Mn(3)CaO(4)] distorted cubane, to which is attached a fourth, external Mn atom, and the whole unit attached to polypeptides primarily by aspartate and glutamate carboxylate groups. Such a heterometallic Mn/Ca cubane with an additional metal attached to it has been unknown in the literature. This paper reports the laboratory synthesis of such an asymmetric cubane-containing compound with a bound external metal atom, [(1)]. All peripheral ligands are carboxylate or carboxylic acid groups. Variable-temperature magnetic susceptibility data have established 1 to possess an S = 9/2 ground state. EPR spectroscopy confirms this, and the Davies electron nuclear double resonance data reveal similar hyperfine couplings to those of other Mn(IV) species, including the OEC S(2) state. Comparison of the X-ray absorption data with those for the OEC reveal 1 to possess structural parameters that make it a close structural model of the asymmetric-cubane OEC unit. This geometric and electronic structural correspondence opens up a new front in the multidisciplinary study of the properties and function of this important biological unit.
UB3LYP calculations have been performed to elucidate electronic and spin states of the CaMn(III)4 − mMn(IV)mX(H2O)4 cluster (X = O5 (1) and O4(OH)) (2) as active catalytic site for water-splitting reaction in oxygen-evolving complex of PSII refined to 1.9 Å X-ray resolution. Both charge- and spin-fluctuated structures have been considered for the mixed-valence (MV) states of 1 and 2. Total energies obtained by these calculations have elucidated quasi-degenerated electronic and spin states that are characterized by charge and spin density populations. The energy levels revealed by UB3LYP are analyzed on the basis of the Heisenberg spin Hamiltonian model, providing the effective exchange integrals between manganese ions at an MV structure. The charge-fluctuation model is also introduced to analyze relative stabilities between MV structures of 1 and 2. The natural orbital (NO) analysis of the UB3LYP solutions has also been performed to elucidate the nature of chemical bonds of 1 and 2: classification of localized d-electrons, labile chemical bonds, and closed-shell orbitals based on their occupation numbers. The localized d-electrons characterized by the NO analysis are responsible for redox reactions, and the origins for the Heisenberg model, namely valence-bond (VB) description of the chemical bonds. On the other hand, labile d–p bonds in 1 and 2 are grasped with the molecular orbital (MO) model: occupation numbers of the NO are used for computations of effective bond order (b), diradical character (y), and spin density indices (Q). Thus, the universal MO–VB model based on the broken-symmetry (BS) calculations followed by the NO analysis is a practical and handy procedure for theoretical approaches to multinuclear transition metal complexes that are hardly investigated by the symmetry-adapted (SA) multireference approaches such as complete active space (CAS) DFT, CASPT2, and CASCC: these SA calculations for related small clusters are performed for examination of scope and applicability of UB3LYP and related DFT functions for target large systems such as 1 and 2.
Electronic and spin structures of manganese clusters, Mn4O4 (1), CaMn3O4 (2), Mn3O4 (3), MnX (4), and CaMn4O4 (5), in the photosynthesis II system are investigated using the classical and quantum Heisenberg models. The molecular orbital calculations by the use of general spin orbitals (GSO) are performed for cubane-type calcium manganese cluster 2 with noncollinear spin alignment, which has also been concluded in our previous studies of 1 and 3. The calculated results, together with available experiments, enable us to propose possible electronic states (from S0 to S4) of tetranuclear manganese cluster 5, which is the active site of oxygen evolution center (OEC). The low-spin (LS) ground states of 2–5 are consistent with the ESR and other magnetic observations. A new reaction scheme for oxygen evolution from water is resulted from both theoretical and experimental results for manganese clusters 1–5 in OEC on the basis of the newly determined X-ray structure by Ferreira et al. [Science 303 (2004) 1831]. In this mechanism, both calcium and manganese ions play important roles for formation of peroxide anion bridge, which is the precursor of molecular oxygen. Implications of computational results are discussed in relation to a key role of the high-valent manganese oxo (Mn(V)O) species in OEC for oxygen evolution from water. Our previous and present computations conclude that Mn(V)O plays a crucial role in both native and artificial OEC systems.
Very recently Umena et al. have determined the X-ray diffraction (XRD) structure of the CaMn4O5 cluster in the oxygen evolution complex (OEC) of photosystem II (PSII) refined to 1.9 Å resolution. We have performed theoretical attempts to elucidate possible electronic and spin states of their new XRD structure of the CaMn4O5 cluster. For the purpose, hybrid density functional theory (UB3LYP and UBHandHLYP) calculations have been performed for the mixed-valence (MV) CaMn(III)4-ω(IV)ωO5(H2O)4 (1) and CaMn(III)4-ω(IV)ωO4(OH)(H2O)4 (2) clusters as active catalytic site for water splitting reaction in OEC of PSII. Full geometry optimizations of 1a (ω = 2) and 2a (ω = 2) have been performed to elucidate scope and limitation of the cluster models. Both charge and spin fluctuated structures (48 UB3LYP solutions) have been considered for the MV 1a (ω = 2). Total energies obtained by these calculations have elucidated quasi-degenerated electronic and spin states that are characterized by charge and spin density populations. The energy levels revealed by hybrid DFT are analyzed on the basis of the Heisenberg spin Hamiltonian model, providing the effective exchange integrals between manganese ions at a uniform or MV structure. The spin projections for hybrid DFT solutions are performed using the effective exchange integrals. The charge fluctuation model is introduced to analyze relative stabilities among MV structures of 1a and 2a. These computational results for 1a and 2a have explored several characteristic electronic properties of the species that are used for theoretical elucidation of possible mechanisms of water splitting reaction. Orbital and spin correlation diagrams are derived for the OO bond formation and oxygen evolution in the reaction. Implications of the computational results are also discussed in relation to available experiments and theoretical results by other groups. © 2011 Wiley Periodicals, Inc. Int J Quantum Chem, 2012
Several hybrid DFT methods were applied to full geometry optimizations of the CaMn4O4X(H2O)4 (XOH1− (1) or O2− (2)) cluster in the oxygen evolving complex (OEC) of photosystem II (PSII) to elucidate Mn-Mn, Mn-Ca, and Mn-O distances on a theoretical ground. The computed Mn-Mn distances were compared with previous (London and Berlin) X-ray diffraction (XRD), and Berkeley and Berlin EXAFS results, together with the recent high-resolution XRD structure by Umena and coworkers. Present computational results by the hybrid DFT methods have elucidated several differences among these accumulated results. These DFT results led us to reassign the Mn-Mn and Mn-Ca distances by the EXAFS experiments, which became consistent with the results obtained by the high-resolution XRD structure. A characteristic feature revealed via the optimized Mn-O distances was that the degree of symmetry breaking of the Mn1-O(57)-Mn4 bond is not so remarkable under the UBHandHLYP approximation but it can be large by other hybrid DFT methods. The computational results for 2 indicated reduction of the Mn3-Mn4 distance with the deprotonation of the bridging oxo group. The hybrid DFT results for 1 are not inconsistent with an experimental proposal based on the new XRD structure, namely a protonated μ3-oxygen at the internal O(57) site of the cluster in the S1 state. On the other hand, the reduction of Mn ions (not degradation of whole cluster structure) by the X-ray irradiation still remains an important issue for refinements of the XRD structure. The computational results are discussed in relation to those of the electron spin echo envelope modulation (ESEEM) and possible pathways for water splitting reaction. Implications of the present DFT structures are discussed in relation to the previous DFT and related computational results, together with recent XRD results for cubane-like model clusters for OEC of PSII. © 2012 Wiley Periodicals, Inc.
Full geometry optimizations of mixed-valence (MV) cubane Mn(III)4-ωMn(IV)ωO4 cluster (ω = 0–4) by UB3LYP have been performed to elucidate Jahn-Teller (JT) effects for the Mn(III) ions. The optimized geometries have elucidated acute triangle for Mn(III)2 Mn(X) (X = III,IV) core in the cubane, indicating the JT effect. The JT effect is not remakable for Mn(IV)2Mn(III) cores, showing obtuse triangle and it diminishes in Mn(IV)3 core with equilateral triangle. The replacement of one of Mn ions with Ca (or Sr) ion in the cubane structure has also been examined to elucidate multiple roles of Ca(II) ion. The Ca-doping suppresses the JT effect even for Mn(III)2Mn(X) (X = III,IV) core because acute CaMnMn triangles with longer Ca-Mn distances than the Mn-Mn distance are newly formed. The suppression of the JT effect for Mn(IV)2 Mn(III) by Ca doping is also found because of the same reason. The Ca-doped cubane in the CaMn4O5 cluster (1) of oxygen evolving complex (OEC) of photosystem II (PSII) exhibits two acute CaMnMn triangles and one almost equilateral CaMnMn triangle because of the elongation of the Mn1(d)-Mn3(b) distance with the coordination of the extra Mn4(a) ion to the cubane. The Mn1(d)Mn2(c)Mn3(b) triangle becomes obtuse because of the suppression of the JT effect, indicating the Mn1(d)(III)Mn2(c)(IV)Mn3(b)(IV) valence state in the S1 state of 1. The JT distortion for Mn(III) ions modified by the Ca(or Sr) doping is coupled with the labile structural deformation for intracluster electron transfers via double exchange mechanism in 1. The structural anomalies of 1 revealed by the new XRD experiment are also crucial for derivation of several guiding principles for theoretical modeling of water splitting reaction at OEC of PSII. The hybrid DFT computational results for 1 have also supported these guiding principles that provide possible orbital and spin correlation diagrams for water splitting reactions. The Huckel-Hubbard-Hund (HHH) model has been used for qualitative understanding of these diagrams. Implications of the present computational results are discussed in relation to electronic and spin states of redox active Ca-doped Mott insulators constructed with magnetic transition metals such as Mn, Fe, Co, Ni, etc. Strongly correlated electron systems (SCES) modified by doping of Ca, Sr, Zn, etc. have been elucidated as possible candidates of bio-inspired artificial catalysts for water oxidation. © 2012 Wiley Periodicals, Inc.
Spin polarisation effects of labile manganese–oxygen bonds in the X-ray diffraction structure of the oxygen-evolving complex (OEC) of photosystem II (PSII) at 1.9 Å resolution have been investigated by the UB3LYP computations on the basis of three different theoretical models with and without hydrogen bonds: quantum-mechanical (QM) Model I, QM(Model II)/MM and QM Model III. The spin densities on the manganese and oxygen atoms of the CaMn4O5 cluster revealed by these computations have elucidated internal, semi-internal and external reductions of high-valent manganese ions in the CaMn4O5 cluster in OEC of PSII. The internal reduction of Mn(IV) ions by the back charge transfer from oxygen dianions is remarkable in the small QM Model I, whereas it is significantly reduced in the case of more realistic QM Model III including hydrogen bonding stabilisations of oxygen dianions. However, semi-internal reduction of the CaMn4O5 cluster with remote amino acid residues such as Asp61 anion occurs even in QM Model III, indicating the necessity of large QM parts for redox-active systems such as OEC of PSII. The computational results have clearly demonstrated important roles of confinement effects of the CaMn4O5 cluster with labile Mn–O bonds with protein. These computational results have been applied to molecular design of artificial robust catalysts for water oxidation by use of sunlight.
Recently, Umena et al. have revealed the X-ray diffraction structure of the CaMn4O5 cluster in the oxygen evolving complex (OEC) of photosystem II (PSII) refined to 1.9 Å resolution. Their X-ray structure has first elucidated hydrogen-bonding networks and proton release pathways at OEC of PSII. Here, several working hypotheses (heuristic principles) for water splitting reaction are derived from their X-ray structure for theoretical modeling. These hypotheses suggest how water can be oxidized at OEC of PSII: namely possible reaction mechanisms for the reaction. To confirm them, we have also performed broken-symmetry (BS) UB3LYP calculations for active site models based on their XRD structure. The bond lengths of formal Mn(V)O with labile dπ-pπ bonds are optimized to clarify possible roles of the species that are often introduced as a key intermediate in the catalytic (Kok) cycle for water splitting reaction at OEC of PSII. Location of the transition structure for the oxygen-oxygen (OO) bond formation is also performed by the energy optimization technique. The natural orbital (NO) analysis of the UB3LYP solutions has been performed to obtain the natural molecular orbitals and their occupation numbers that have been useful for classification of localized d-electrons, labile chemical bonds and closed-shell (valence) orbitals. The localized d-electrons characterized by the NO analysis are the origins for the magnetism revealed by ENDOR and other magnetic experiments. On the other hand, the nature of labile (soft) dπ-pπ bonds responsible for the OO bond formation has been investigated on the basis of chemical indices such as effective bond order (b), diradical character (y), and spin density (Q) indices that are calculated using the orbital overlap between broken-symmetry orbitals. These chemical indices have been calculated for the transition structure of the OO bond formation at OEC of PSII. Implications of present computational results are discussed in relation to the derived hypotheses and available accumulated experimental results. © 2011 Wiley Periodicals, Inc. Int J Quantum Chem, 2012
The authors report the detection of a new electron paramagnetic resonance (EPR) signal that demonstrates the presence of a paramagnetic intermediate in the resting (S{sub 1}) state of the photosynthetic oxygen-evolving complex. The signal was detected using the method of parallel polarization EPR, which is sensitive to {Delta}m = 0 transitions in high spin systems. The properties of the parallel polarization EPR signal in the S{sub 1} state are consistent with an S=1 spin state of and exchange-coupled manganese center that corresponds to the reduced form of the species giving rise to the multiline EPR signal in the light-induced S{sub 2} state. The implications for the electronic structure of the oxygen-evolving complex are discussed. 36 refs., 2 fig., 1 tab.
Quantum mechanical (QM) and QM/molecular mechanics (MM) calculations of three different cluster models have been performed to shed light on hydrogen bonding networks and proton wires for proton release pathways (PRP) of water oxidation reactions in the oxygen evolving complex (OEC) of photosystem II (PSII). Positions of all the hydrogen atoms in an extended QM Model III including the second coordination sphere for the active-site CaMn4O5 complex of OEC of PSII have been optimized assuming the geometry of heavy atoms determined by the recent high-resolution X-ray diffraction (XRD) experiment of PSII refined to 1.9 Å resolution. Full geometry optimizations of the first coordination sphere model (QM Model I) embedded in the Model III and QM (QM Model I plus seven water molecules, namely QM Model II)/MM models, together with full QM Model III, have also been conducted to elucidate confinement effects for geometrical parameters of the CaMn4O5 cluster by proteins. Computational results by these methods have elucidated the OO(N), OH distances and O(N)–HO angles for hydrogen bonds in proton release paths (PRP) I and II that construct a proton wire from Asp61 toward His190. The hydrogen-bonding structures revealed have also been examined in relation to the possibilities of protonation of bridge oxygen dianions within the CaMn4O5 cluster. The optimized inter-atomic distances by QM Models I and III, together with QM(Model II)/MM, have elucidated the elongation of the Mn–Mn distances with hydrogen bonds and variations of the Mnd–O(5) length with confinement effects by protein. Implications of the computational results are discussed in relation to the available EXAFS experiments, and internal, semi-internal and external reductions of Mn ions and long Mn–Mn distances of the high-resolution (SP8) XRD, and rational design of artificial catalysts for water oxidation that are current topics in the field of OEC of PSII.
In the crystal structure of photosystem II (PSII) from the cyanobacterium Thermosynechococcus elongatus at 3.2 Å resolution, several loop regions of the principal protein subunits are now defined that were not interpretable previously at 3.8 Å resolution. The head groups and side chains of the organic cofactors of the electron transfer chain and of antenna chlorophyll a
(Chl a) have been modeled, coordinating and hydrogen bonding amino acids identified and the nature of the binding pockets derived. The orientations of these cofactors resemble those of the reaction center from anoxygenic purple bacteria, but differences in hydrogen bonding and protein environment modulate their properties and provide the unique high redox potential (1.17 V) of the primary donor. Coordinating amino acids of manganese cluster, redox-active TyrZ and non-haem Fe2+ have been determined, and an all-trans
β-carotene connects cytochrome b-559, ChlZ and primary electron donor (coordinates are available under PDB-code 1W5C).
The process of water oxidation and dioxygen evolution by the photosystem II (PSII) component of plant photosynthesis is cyclic, with intermediate states of the oxygen-evolving complex (OEC) designated Sâ through Sâ. Two electron paramagnetic resonance (EPR) signals have been assigned to the Sâ state of the complex. A multiline' EPR signal centered at the g = 2 region of the spectrum shows 16 or more partially resolved Mn hyperfine transitions and arises from a cluster with a minimum of two exchange-coupled mixed-valence Mn atoms. The other Sâ EPR signal occurs in the g = 4.1 region of the spectrum. The lack of resolved Mn hyperfine couplings has prevented conclusive assignment of the g = 4.1 EPR signal to a Mn center. However, a shift of the Mn X-ray K edge to higher energies is correlated with the appearance of the g = 4.1 signal in PSII membranes illuminated at 140 K. A considerable body of experimental work, including measurements of the temperature dependence of the EPR signals and observations of the interconversion between the multiline and the g = 4.1 signals, has given rise to two different models involving S = 3/2 Mn origins for the g = 4.1 signal. In this communication, the authors present direct spectral evidence of a multinuclear Mn origin for the Sâ g = 4.1 signal.
Very recently Umena et al. have determined the X-ray diffraction (XRD) structure of the CaMn4O5 cluster (1) in the oxygen-evolving complex (OEC) of photosystem II (PSII) refined to 1.9Å resolution. UB3LYP calculations of 1 using this XRD structure were performed to elucidate possible mechanisms for the oxygen–oxygen (O–O) bond formation in oxygen evolution reaction of PSII. The solutions obtained were used for natural orbital (NO) analysis to obtain LUMOs of labile chemical bonds, which clearly indicated the possibilities of nucleophilic attack of hydroxide (or water molecule) to the electrophilic O(56) and/or O(57) sites of 1.
The Mn-4-cluster of photosystem II (PSII) from Synechococcus elongatus was studied by electron paramagnetic resonance (EPR) spectroscopy after a series of saturating laser flashes given in the presence of either methanol or ethanol. Results were compared to those obtained in similar experiments done on PSII isolated from plants. The flash-dependent changes in amplitude of the EPR multiline signals were virtually identical in all samples. In agreement with earlier work [Messinger, J., Nugent, J, H. A., and Evans, M. C. W. (1997) Biochemistry, 36, 11055-11060; Ahrling, K. A., Peterson, S., and Styring, S, (1997) Biochemistry 36, 13148-13152], detection of an EPR multiline signal from the So state in PSII from plants was only possible with methanol present. In PSII from S. elongatus, it is shown that the S-0 state exhibits an EPR multiline signal in the absence of methanol (however, ethanol was present as a solvent for the artificial electron acceptor). The hyperfine lines are better resolved when methanol is present. The S-0 multiline signals detected in plant PSII and in S, elongatus were similar but not identical. Unlike the situation seen in plant PSII, the S-2 state in S. elongatus is not affected by the addition of methanol in that (i) the S-2 multiline EPR signal is not modified by methanol and (ii) the spin state of the S-2 state is affected by infrared light when methanol is present. It is also shown that the magnetic relaxation properties of an oxidized low-spin heme, attributed to cytochrome c(550), vary with the S states. This heme then is in the magnetic environment of the Mn-4 cluster.
In Photosystem II preparations at low temperature we were able to generate and trap an intermediate state between the S1 and S2 states of the Kok scheme for photosynthetic oxygen evolution. Illumination of dark-adapted, oxygen-evolving Photosystem II preparations at 140 K produces a 320-G-wide EPR signal centered near g = 4.1 when observed at 10 K. This signal is superimposed on a 5-fold larger and somewhat narrower background signal; hence, it is best observed in difference spectra. Warming of illuminated samples to 190 K in the dark results in the disappearance of the light-induced g = 4.1 feature and the appearance of the multiline EPR signal associated with the S2 state. Low-temperature illumination of samples prepared in the S2 state does not produce the g = 4.1 signal. Inhibition of oxygen evolution by incubation of PS II preparations in 0.8 M NaCl buffer or by the addition of 400 μM NH2OH prevents the formation of the g = 4.1 signal. Samples in which oxygen evolution is inhibited by replacement of Cl− with F− exhibit the g = 4.1 signal when illuminated at 140 K, but subsequent warming to 190 K neither depletes the amplitude of this signal nor produces the multiline signal. The broad signal at g = 4.1 is typical for a spin system in a rhombic environment, suggesting the involvement of non-heme Fe in photosynthetic oxygen evolution.
In this contribution, the authors provide a more complete interpretation of earlier EPR data and include new experimental data on the magnetic properties of the g = 4.1 Sâ state EPR signal and the Sâ state multiline EPR signal produced by 245 K illumination in active state samples. An interpretation of the temperature-dependence data of the Sâ state EPR signal from NHâCl-treated PSII membranes was presented. These data can be best explained by a model of the Sâ state which consists of a mixed-valence manganese tetramer.
Strong influences of bridging ligands L on the magnetism of two Ni9 complexes, Ni9L2(O2CMe)8 {(2-py)2CO2}4 (L=OH−1 and N3-2) are demonstrated by magnetic interactions. Effective exchange integrals J for 1 and 2 are determined non-empirically using UB3LYP and UBLYP. The calculated magnetic susceptibility for 1 is wholly consistent with the experimental values. Although the ground spin state of 2 obtained using the calculated J values agrees with the experimental S=9 state, fitting of the J values to the experimental magnetic susceptibility curve indicates weak antiferromagnetic interactions via the azido ligands.
The electronic and spin structures of the [8Fe-7S] inorganic model complex (1) have been investigated using the density functional theory (DFT) UB3LYP and UBLYP methods. The experimental geometry of 1 was used to calculate the sets of exchange interactions (J values) between Fe-spin centers within spin Hamiltonian models. The experimental temperature-dependent paramagnetism is well reproduced on the basis of the calculated J values. The calculated low-lying energy levels are also consistent with those of the experiments. This indicates that the ground spin state of 1 is singlet (S = 0) for the weak antiferromagnetic coupling between two [4Fe-3S] cubane units, which take the Fe(III)Fe(II)3 formal charge and S = 7/2 spin states. The first-order density matrix of the most stable broken-symmetry (BS) solution has been diagonalized to elucidate the natural molecular orbitals (MOs) and their occupation number of 1, which are hardly obtained by the symmetry-adapted (SA) CASSCF approach. Several chemical indices such as the effective bond orders before and after spin projection are also calculated by using the occupation numbers to provide the SA MO picture of labile chemical bonds of 1. It is found that the BS MO calculation followed by spin-projected SA analysis is an effective and practical alternative to the CASSCF MO approach for the multinuclear transition metal clusters.
Freezing of spinach or barley chloroplasts during continuous illumination results in the trapping of a paramagnetic state or a mixture of such states characterized by a multiline EPR spectrum. Added Photosystem II electron acceptor enhances the signal intensity considerably. Treatments which abolish the ability of the chloroplasts to evolve oxygen, by extraction of the bound manganese, prevent the formation of the paramagnetic species. Restoration of Photosystem II electron transport in inhibited chloroplasts with an artificial electron donor (1,5-diphenylcarbazide) does not restore the multiline EPR spectrum. The presence of 3-(3,4-dichlorophenyl)-1, 1-dimethylurea (DCMU) results in a modified signal which may represent a second paramagnetic state. The paramagnetic forms appear to originate on the donor side in Photosystem II and are dependent on a functional oxygenevolving site and bound, intact manganese. It is suggested that magnetically interacting manganese ions in the oxygen-evolving site may be responsible for the EPR signals. This suggestion is supported by calculations.
Balancing act: DFT calculations show that the structures of the water-oxidizing complex in the two most recent single crystal XRD studies of photosystem II at 2.9 Å and 1.9 Å resolution are tautomers related by a single proton transfer. The anomalous oxygen species, O(5), weakly bound to four metal centers in the 1.9 Å structure is identified as a substrate water molecule balanced between the Jahn-Teller axes of Mn(1), Mn(3), and Mn(4).
Full geometry optimizations of several inorganic model clusters, CaMn(4)O(4)XYZ(H(2)O)(2) (X, Y, Z = H(2)O, OH(-) or O(2-)), by the use of the B3LYP hybrid density functional theory (DFT) have been performed to illuminate plausible molecular structures of the catalytic site for water oxidation in the S(0), S(1), S(2) and S(3) states of the Kok cycle for the oxygen-evolving complex (OEC) of photosystem II (PSII). Optimized geometries obtained by the energy gradient method have revealed the degree of symmetry breaking of the unstable three-center Mn(a)-X-Mn(d) bond in CaMn(4)O(4)XYZ(H(2)O)(2). The right-elongated (R) Mn(a)-XMn(d) and left-elongated (L) Mn(a)X-Mn(d) structures appear to occupy local minima on a double-well potential for several key intermediates in these states. The effects of insertion of one extra water molecule to the vacant coordination site, Mn(d) (Mn(a)), for R (L) structures have also been examined in detail. The greater stability of the L-type structure over the R-type has been concluded for key intermediates in the S(2) and S(3) states. Implications of the present DFT structures are discussed in relation to previous DFT and related results, together with recent X-ray diffraction results for model compounds of cubane-like OEC cluster of PSII.
An ESEEM (electron spin−echo envelope modulation) spectroscopic study employing a series of 2H-labeled alcohols provides direct evidence that small alcohols (methanol and ethanol) ligate to the Mn cluster of the oxygen evolving complex (OEC) of Photosystem II in the S2-state of the Kok cycle. A numerical method for calculating the through-space hyperfine interactions for exchange-coupled tetranuclear Mn clusters is described. This method is used to calculate hyperfine interaction tensors for protons [deuterons] in the vicinity of two different arrangements of Mn ions in a tetranuclear cluster: a symmetric cubane model and the EXAFS-based Berkeley “dimer-of-dimers” model. The Mn−H distances derived from the spectroscopically observed coupling constants for methanol and ethanol protons [deuterons] and interpreted with these cluster models are consistent with the direct ligation of these small alcohols to the OEC Mn cluster. Specifically, for methanol we can simulate the three-pulse ESEEM time domain pattern with three dipolar hyperfine interactions of 2.92, 1.33, and 1.15 MHz, corresponding to a range of maximal Mn−H distances in the models of 3.7−5.6 Å (dimer-of-dimers) and 3.6−4.9 Å (symmetric cubane). We also find evidence for limited access of n-propanol, but no evidence for 2-propanol or DMSO access. Implications for substrate accessibility to the OEC are discussed.
The two forms of the g ≈ 4.1 signal recently identified in photosystem II (Smith, P. J.; Pace, R. J. Biochim. Biophys. Acta 1996, 1275, 213) have been simulated at several frequencies as near-axial spin 3/2 centers. In both cases, an explicit spin coupling model is assumed, involving two magnetically isolated Mn pairs, one for each signal type. For that pair assumed to give rise to the spin 1/2 multiline signal as the ground state, the modeling of the first-excited-state 4.1 signal gives estimates of the fine structure parameters for the individual Mn centers and the exchange coupling constant for the pair. The fine structure terms suggest that one Mn ion is a conventional MnIII ion in a highly axially distorted environment. The other Mn center, which is formally spin 3/2, is unlikely to be a conventional MnIV ion, but rather a MnIII−radical ligand pair, strongly antiferromagnetically coupled to give a net spin 3/2 state. The coupling between this Mn−radical center and the other MnIII is weak (J = −2.3 cm-1) in the absence of alcohol in the buffer medium, as determined earlier (Smith and Pace). The model is shown to be quantitatively consistent with the behavior of other signals proposed to arise from this coupled dimer. Comparison of our own data with those of others (Haddy, A.; et al. Biochim. Biophys. Acta 1992, 1099, 25−34) on one-dimensionally ordered photosystem II samples shows a generally consistent orientation of the molecular axis system for the dimer in the membrane plane. The second 4.1 signal, which exhibits ground-state behavior, may be simulated at X- and Q-band frequencies as an isolated system with D = +1.1 cm-1 and E/D = 0.037. The spin center is suggested to arise from a radical-bridged Mn homodimer, and the modeling parameters have been interpreted within this framework. The resulting proposal, involving two isolated dimers for the Mn organization within the oxygen evolving center, is critically examined in the light of recent work from other groups.
Binding of NH3 to the S2 state of the O2-evolving complex of photosystem II (PSII) causes a structural change in the Mn site that is detectable with low-temperature electron paramagnetic resonance (EPR) spectroscopy. Untreated spinach PSII membranes at pH 7.5 produce a S2 state multiline EPR spectrum when illuminated at either 210 K or at 0°C in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) having an average hyperfine line spacing of 87.5 G. The temperature dependence of the S2 state multiline EPR signal observed from untreated samples deviates from the Curie law above 5 K, with a maximum signal intensity at 6.9 K as has been previously observed. In contrast, 100 mM NH4Cl-treated PSII membranes at pH 7.5 exhibit a new S2 state EPR spectrum when illuminated at 0°C in the presence of DCMU. The novel S2 state EPR spectrum from NH4Cl-treated PSII membranes has an average hyperfine line spacing of 67.5 G and a temperature dependence obeying the Curie law except for small deviations at low temperature. We assign the new S2 state EPR signal from NH4Cl-treated PSII membranes to a form of the S2 state having one or more NH3 molecules directly coordinated to the Mn site. NH3 does not bind to Mn in the dark-stable S1 state present before illumination, since generation of the S2 state in NH4Cl-treated PSII membranes by illumination at 210 K does not yield the new S2 state EPR spectrum. Since inhibition of O2 evolution activity in the presence of NH4Cl probably occurs through binding of NH3 to the O2-evolving complex in competition with substrate H2O molecules, these results indicate that the EPR-detectable Mn site functions as the substrate-binding site of the O2-evolving complex.
We have performed continuous-wave electron paramagnetic resonance (CW-EPR) and electron spin echo electron nuclear double resonance (ESE-ENDOR) experiments on the multiline form of the S2-state of untreated, MeOH-treated, and ammonia-treated spinach photosystem II (PS II) centers. Through simultaneously constrained simulations of the CW-EPR and ESE-ENDOR data, we conclude that four effective 55Mn hyperfine tensors (AX, AY, AZ) are required to properly simulate the experimental data [untreated and MeOH-treated PS II centers (MHz): −232, −232, −270; 200, 200, 250; −311, −311, −270; 180, 180, 240; ammonia-treated PS II centers (MHz): 208, 208, 158; −150, −150, −112; 222, 222, 172; −295, −315, −390]. We further show that these effective hyperfine tensors are best supported by a trimer/monomer arrangement of three Mn(IV) ions and one Mn(III) ion. In this topology, MnA, MnB, and MnC form a strongly exchange coupled core (JAB and JBC < −100 cm-1) while MnD is weakly exchange coupled (JCD) to one end of the trinuclear core. For untreated and MeOH-treated PS II centers, the Mn(III) ion is either MnA or MnC, with a zero-field-splitting of D = −1.25 to −2.25 cm-1. For ammonia-treated PS II centers, the Mn(III) ion is MnD, with a zero-field-splitting of D = +0.75 to +1.75 cm-1. The binding of the ammonia ligand results in a shift of the Mn(III) ion from the trinuclear core to the monomer Mn ion. This structural model can also account for the higher spin of the g = 4.1 signal and the magnetic properties of the S0-state.
The process of water oxidation and dioxygen evolution by the photosystem II (PSII) component of plant photosynthesis is cyclic, with intermediate states of the oxygen-evolving complex (OEC) designated S{sub 0} through S{sub 4}. Two electron paramagnetic resonance (EPR) signals have been assigned to the S{sub 2} state of the complex. A multiline' EPR signal centered at the g = 2 region of the spectrum shows 16 or more partially resolved Mn hyperfine transitions and arises from a cluster with a minimum of two exchange-coupled mixed-valence Mn atoms. The other S{sub 2} EPR signal occurs in the g = 4.1 region of the spectrum. The lack of resolved Mn hyperfine couplings has prevented conclusive assignment of the g = 4.1 EPR signal to a Mn center. However, a shift of the Mn X-ray K edge to higher energies is correlated with the appearance of the g = 4.1 signal in PSII membranes illuminated at 140 K. A considerable body of experimental work, including measurements of the temperature dependence of the EPR signals and observations of the interconversion between the multiline and the g = 4.1 signals, has given rise to two different models involving S = 3/2 Mn origins for themore » g = 4.1 signal. In this communication, the authors present direct spectral evidence of a multinuclear Mn origin for the S{sub 2} g = 4.1 signal.« less
Water binding to the Mn(4)O(5)Ca cluster of the oxygen-evolving complex (OEC) of Photosystem II (PSII) poised in the S(2) state was studied via H(2)(17)O- and (2)H(2)O-labeling and high-field electron paramagnetic resonance (EPR) spectroscopy. Hyperfine couplings of coordinating (17)O (I = (5)/(2)) nuclei were detected using W-band (94 GHz) electron-electron double resonance (ELDOR) detected NMR and Davies/Mims electron-nuclear double resonance (ENDOR) techniques. Universal (15)N (I = (1)/(2)) labeling was employed to clearly discriminate the (17)O hyperfine couplings that overlap with (14)N (I = 1) signals from the D1-His332 ligand of the OEC ( Stich Biochemistry 2011 , 50 ( 34 ), 7390 - 7404 ). Three classes of (17)O nuclei were identified: (i) one μ-oxo bridge; (ii) a terminal Mn-OH/OH(2) ligand; and (iii) Mn/Ca-H(2)O ligand(s). These assignments are based on (17)O model complex data, on comparison to the recent 1.9 Å resolution PSII crystal structure ( Umena Nature 2011 , 473 , 55 - 60 ), on NH(3) perturbation of the (17)O signal envelope and density functional theory calculations. The relative orientation of the putative (17)O μ-oxo bridge hyperfine tensor to the (14)N((15)N) hyperfine tensor of the D1-His332 ligand suggests that the exchangeable μ-oxo bridge links the outer Mn to the Mn(3)O(3)Ca open-cuboidal unit (O4 and O5 in the Umena et al. structure). Comparison to literature data favors the Ca-linked O5 oxygen over the alternative assignment to O4. All (17)O signals were seen even after very short (≤15 s) incubations in H(2)(17)O suggesting that all exchange sites identified could represent bound substrate in the S(1) state including the μ-oxo bridge. (1)H/(2)H (I = (1)/(2), 1) ENDOR data performed at Q- (34 GHz) and W-bands complement the above findings. The relatively small (1)H/(2)H couplings observed require that all the μ-oxo bridges of the Mn(4)O(5)Ca cluster are deprotonated in the S(2) state. Together, these results further limit the possible substrate water-binding sites and modes within the OEC. This information restricts the number of possible reaction pathways for O-O bond formation, supporting an oxo/oxyl coupling mechanism in S(4).
Using models derived from the X-ray structure of photosystem II, it is shown that the oxygen evolving complex in the S(2) state exists in two energetically similar and interconvertible forms. A longstanding question regarding the spectroscopy of the catalyst is thus answered: one form corresponds to the multiline g=2.0 EPR signal (see picture, right; O red, Mn purple, Ca yellow), and the other to the g≥4.1 signals (left).
Reaction mechanisms of oxygen evolution in native and artificial photosynthesis II (PSII) systems have been investigated on the theoretical grounds, together with experimental results. First of all, our previous broken-symmetry (BS) molecular orbitals (MO) calculations are reviewed to elucidate the instability of the dπ-pπ bond in high-valent (HV) Mn(X)O systems and the dπ-pπ-dπ bond in HV MnOMn systems. The triplet instability of these bonds entails strong or intermediate diradical characters: •Mn(IV)O• and •MnOMn•; the BS MO resulted from strong electron correlation, leading to the concept of electron localizations and local spins. The BS computations have furthermore revealed guiding principles for derivation of selection rules for radical reactions of local spins. As a continuation of these theoretical results, the BS MO interaction diagrams for oxygen-radical coupling reactions in the oxygen evolution complex (OEC) in the PSII have been depicted to reveal scope and applicability of local singlet diradical (LSD) and local triplet diradical (LTD) mechanisms that have been successfully utilized for theoretical understanding of oxygenation reactions mechanisms by p450 and methane monooxygenase (MMO). The manganese-oxide cluster models examined are London, Berlin, and Berkeley models of CaMn4O4 and related clusters Mn4O4 and Mn3Ca. The BS MO interaction diagrams have revealed the LSD and/or LTD mechanisms for generation of molecular oxygen in the total low-, intermediate and high-spin states of these clusters. The spin alignments are found directly corresponding to the spin-coupling mechanisms of oxygen-radical sites in these clusters. The BS UB3LYP calculations of the clusters have been performed to confirm the comprehensive guiding principles for oxygen evolution; charge and spin densities by BS UB3LYP are utilized for elucidation and confirmation of the LSD and LTD mechanisms. Applicability of the proposed selection rules are examined in comparison with a lot of accumulated experimental and theoretical results for oxygen evolution reactions in native and artificial PSII systems. © 2010 Wiley Periodicals, Inc. Int J Quantum Chem, 2010
UB3LYP calculations were first performed to elucidate electronic and spin structures of the CaMn4O5 cluster in the oxygen-evolving-complex of the PSII system refined to the 1.9 Å X-ray resolution by Kamiya, Shen, and their collaborators. Eight different UB3LYP solutions with axial spin structures were constructed to obtain the energy levels of the cluster on the basis of their X-ray structure. The energy diagrams were analyzed in terms of the Heisenberg model that involves six effective-exchange integrals between manganese ions. Several characteristic features of the electronic states of the cluster are revealed from these theoretical investigations based on the UB3LYP calculations.Graphical abstractView high quality image (66K)Research highlights► A first ab initio study of the manganese cluster with the 1.9 Å X-ray resolution. ► We examined all possible axial spin structures using B3LYP method of Mn(IV)4 and Mn(III)4 cases. ► We analyzed the energy spectra of spin states using Heisenberg 6 J model. ► Energy gaps are quite small, which is related to the labile character of the cluster.
Density functional theory (DFT) calculations are reported for a set of model compounds intended to represent the structure of the Photosystem II (PSII) water oxidising complex (WOC) as determined by the recent 1.9 Å resolution single crystal X-ray diffraction (XRD) study of Umena et al. In contrast with several other theoretical studies addressing this structure, we find that it is not necessary to invoke photoreduction of the crystalline sample below the S(1)'resting state' in order to rationalise the observed WOC geometry. Our results are consistent with crystallised PSII in the S(1) state, with S(1) corresponding to either (Mn(III))(4) or (Mn(III))(2)(Mn(IV))(2) as required by the two competing paradigms for the WOC oxidation state pattern. Of these two paradigms, the 'low-oxidation-state' paradigm provides a better match for the crystal structure, with the comparatively long Mn(2)-Mn(3) distance in particular proving difficult to reconcile with the 'high-oxidation-state' model. Best agreement with the set of metal-metal distances is obtained with a S(1) model featuring μ-O, μ-OH bridging between Mn(3) and Mn(4) and deprotonation of one water ligand on Mn(4). Theoretical modelling of the 1.9 Å structure is an important step in assessing the validity of this recent crystal structure, with implications for our understanding of the mechanism of water oxidation by PSII.
Oxo- or hydroxo-bridged diiron centers are ubiquitous in metalloenzymes such as hemerythrin (Hr), ribonucleotide reductase, methane monooxygenase, and rubrerythrin. In each enzyme the diiron core plays a central role in the highly specific reaction. To elucidate mechanisms of these reactions, many experimental studies have been carried out, and bioinorganic model compounds have also been synthesized for the purpose. In this study electronic structures of diiron centers for Hr model compounds are investigated from the viewpoint of magnetic interactions. To this end, the Hubbard model for the three-center four-electron bond is analytically solved to elucidate an important role of electron correlation and the resulting superexchange interaction between localized spins. The hybrid density functional theory (DFT) calculations also are performed for Hr model compounds to provide the natural orbitals and their occupation numbers, which are crucial for computations of several chemical indices, such as effective bond order, information entropy, and unpaired electron density. These indices are useful for characterization and understanding of chemical bonds in FeOFe cores. The calculated effective exchange integrals (Jab) are wholly consistent with the available experiments. The orbital interactions in the FeOFe cores are reconsidered in relation to recent work by other groups. It is found that magnetic interactions are sensitive to the hydrogen bonds in the systems and are related to effective regulation of the activity. Implications of the calculated results are discussed in relation to the nature of chemical bonds in the FeOFe cores of several biological systems. © 2004 Wiley Periodicals, Inc. Int J Quantum Chem, 2004
Extensive quantum chemical DFT calculations were performed on the high-resolution (1.9 Å) crystal structure of photosystem II in order to determine the protonation pattern and the oxidation states of the oxygen-evolving Mn cluster. First, our data suggest that the experimental structure is not in the S(1)-state. Second, a rather complete set of possible protonation patterns is studied, resulting in very few alternative protonation patterns whose relevance is discussed. Finally, we show that the experimental structure is a mixture of states containing highly reduced forms, with the largest contribution (almost 60%) from the S(-3)-state, Mn(II,II,III,III).
The oxygen-evolving complex (OEC) of Photosystem II (PSII) is an oxomanganese complex that catalyzes water-splitting into O2, protons and electrons. Recent breakthroughs in X-ray crystallography have resolved the cuboidal OEC structure at 1.9 Å resolution, stimulating significant interest in studies of structure/function relations. This article summarizes recent advances on studies of the OEC along with studies of synthetic oxomanganese complexes for artificial photosynthesis. Quantum mechanics/molecular mechanics hybrid methods have enabled modeling the S1 state of the OEC, including the ligation proposed by the most recent X-ray data where D170 is bridging Ca and the Mn center outside the CaMn3 core. Molecular dynamics and Monte Carlo simulations have explored the structural/functional roles of chloride, suggesting that it regulates the electrostatic interactions between D61 and K317 that might be critical for proton abstraction. Furthermore, structural studies of synthetic oxomanganese complexes, including the [H2O(terpy)MnIII(μ-O)2MnIV(terpy)OH2]3+ (1, terpy=2,2':6',2″-terpyridine) complex, provided valuable insights on the mechanistic influence of carboxylate moieties in close contact with the Mn catalyst during oxygen evolution. Covalent attachment of 1 to TiO2 has been achieved via direct deposition and by using organic chromophoric linkers. The (III,IV) oxidation state of 1 attached to TiO2 can be advanced to (IV,IV) by visible-light photoexcitation, leading to photoinduced interfacial electron transfer. These studies are particularly relevant to the development of artificial photosynthetic devices based on inexpensive materials.
The light-induced EPR multiline signal is studied in O2-evolving PS II membranes. The following results are reported: (1) Its amplitude is shown to oscillate with a period of 4, with respect to the number of flashes given at room temperature (maxima on the first and fifth flashes). (2) Glycerol enhances the signal intensity. This effect is shown to come from changes in relaxation properties rather than an increase in spin concentration. (3) Deactivation experiments clearly indicate an association with the S2 state of the water-oxidizing enzyme. A signal at g = 4.1 with a linewidth of 360 G is also reported and it is suggested that this arises from an intermediate donor between the S states and the reaction centre. This suggestion is based on the following observations: (1) The g = 4.1 signal is formed by illumination at 200 K and not by flash excitation at room temperature, suggesting that it arises from an intermediate unstable under physiological conditions. (2) The formation of the g = 4.1 signal at 200 K does not occur in the presence of DCMU, indicating that more than one turnover is required for its maximum formation. (3) The g = 4.1 signal decreases in the dark at 220 K probably by recombination with Q−AFe. This recombination occurs before the multiline signal decreases, indicating that the g = 4.1 species is less stable than S2. (4) At short times, the decay of the g = 4.1 signal corresponds with a slight increase in the multiline S2 signal, suggesting that the loss of the g = 4.1 signal results in the disappearance of a magnetic interaction which diminishes the multiline signal intensity. (5) Tris-washed PS II membranes illuminated at 200 K do not exhibit the signal.
Possible spin-exchange structures of the Mn(III,IV,IV,IV) cluster in an S2 state of plant photosystem II were computer-searched, within the range compatible with X-ray absorption data, by diagonalizing each Heisenberg spin-exchange Hamiltonian and then by checking whether it can take the S=1/2 ground state capable of explaining the effective hyperfine constants determined from oriented multiline spectra and the first excited state with excitation energy around 20–50 cm−1, or not. The possible spin-exchange structures were found to be distributed in those that contain only one strong-antiferromagnetic coupling and at most two intermediate coupling(s). The most probable structures are discussed in detail.
Ab initio calculations of effective exchange interactions between spins are performed for H–H, H–He–H and a simplified model of binuclear manganese oxide, Mn2O2, by using the spin-unrestricted Hartree–Fock (UHF), spin-polarized density functional (DFT) and UHF + DFT hybrid methods. The scopes and limitations of these broken-symmetry approaches are discussed in relation to several computational schemes of effective exchange integrals (Jab). The natural orbitals (UNO or DNO) of the UHF, DFT and hybrid DFT solutions for magnetic clusters are used for interpretation of the superexchange interactions in Mn2O2 complexes.
The most recent XRD studies of Photosystem II (PS II) reveal that the His337 residue is sufficiently close to the Mn(4)Ca core of the Water Oxidising Complex (WOC) to engage in H-bonding interactions with the μ(3)-oxo bridge connecting Mn(1), Mn(2) and Mn(3). Such interactions may account for the lengthening of the Mn-Mn distances observed in the most recent and highest resolution (1.9 Å) crystal structure of PS II compared to earlier, lower-resolution (2.9 Å or greater) XRD structures and EXAFS studies on functional PS II. Density functional theory is used to examine the influence on Mn-Mn distances of H-bonding interactions, mediated by the proximate His337 residue, which may lead to either partial or complete protonation of the μ(3)-oxo bridge on models of the WOC. Calculations were performed on a set of minimal-complexity models (in which WOC-ligating amino acid residues are represented as formate and imidazole ligands), and also on extended models in which a 13-peptide sequence (from His332 to Ala344) is treated explicitly. These calculations demonstrate that while the 2.9 Å structure is best described by models in which the μ(3)-oxo bridge is neither protonated nor involved in significant H-bonding, the 1.9 Å XRD structure is better reproduced by models in which the μ(3)-oxo bridge undergoes H-bonding interactions with the His337 residue leading to expansion of the 'close' Mn-Mn distances well known from EXAFS studies at ∼ 2.7 Å. Furthermore, full μ(3)-oxo-bridge protonation remains a distinct possibility during the process of water oxidation, as evidenced by the lengthening of the Mn-Mn vectors observed in EXAFS studies of the higher oxidation states of PS II. In this context, the Mn-Mn distances calculated in the protonated μ(3)-oxo bridge structures, particularly for the peptide extended models, are in close agreement with the EXAFS data.
The new high-resolution X-ray structure of photosystem II has allowed more detailed studies than before of water oxidation at the oxygen evolving complex (OEC). In the present study the two final S-transitions of water oxidation are studied. The electron coupled proton transfers are followed from the center of the OEC to Asp61, which is considered as the start of the transfer chain through the protein to the lumenal side. It is found that the proton transfers occur in multiple steps. Structures of intermediates and energy diagrams are derived and compared to experimental observations. Since the new experimental structure of the OEC is very similar to the one suggested earlier by density functional calculations, the O-O bond formation step remains essentially the same as the one suggested five years ago. An interesting new result is that the barrier for proton transfer within the OEC actually competes with the O-O bond formation step of being rate-limiting.
The recently-published 3.5 Å resolution X-ray crystal structure of a cyanobacterial photosystem II (PDB entry 1S5L) provides a detailed architecture of the oxygen-evolving complex (OEC) and the surrounding amino-acids [K. N. Ferreira, T. M. Iverson, K. Maghlaoui, J. Barber and S. Iwata, Science, 2004, 203, 1831–1838]. The revealed geometry of the OEC lends weight to certain hypothesized mechanisms for water-splitting, including the one propounded by this group, in which a calcium-bound water acts as a nucleophile to attack the oxygen of a MnVO group in the crucial O–O bond-forming step [J. S. Vrettos, J. Limburg and G. W. Brudvig, Biochim. Biophys. Acta, 2001, 1503, 229–245]. Here we re-examine this mechanism in the light of the new crystallographic information and make detailed suggestions concerning the mechanistic functions (especially the redox and proton-transfer roles) of calcium, chloride and certain amino-acid residues in and around the OEC. In particular, we propose an important role for an arginine residue, CP43–Arg357, in abstracting protons from a substrate water molecule during the water-splitting reaction.
Despite the remarkable thermochemical accuracy of Kohn–Sham density-functional theories with gradient corrections for exchange-correlation [see, for example, A. D. Becke, J. Chem. Phys. 96, 2155 (1992)], we believe that further improvements are unlikely unless exact-exchange information is considered. Arguments to support this view are presented, and a semiempirical exchange-correlation functional containing local-spin-density, gradient, and exact-exchange terms is tested on 56 atomization energies, 42 ionization potentials, 8 proton affinities, and 10 total atomic energies of first- and second-row systems. This functional performs significantly better than previous functionals with gradient corrections only, and fits experimental atomization energies with an impressively small average absolute deviation of 2.4 kcal/mol.
Protonation states of water ligands and oxo bridges are intimately involved in tuning the electronic structures and oxidation potentials of the oxygen evolving complex (OEC) in Photosystem II, steering the mechanistic pathway, which involves at least five redox state intermediates S(n) (n = 0-4) resulting in the oxidation of water to molecular oxygen. Although protons are practically invisible in protein crystallography, their effects on the electronic structure and magnetic properties of metal active sites can be probed using spectroscopy. With the twin purpose of aiding the interpretation of the complex electron paramagnetic resonance (EPR) spectroscopic data of the OEC and of improving the view of the cluster at the atomic level, a complete set of protonation configurations for the S(2) state of the OEC were investigated, and their distinctive effects on magnetic properties of the cluster were evaluated. The most recent X-ray structure of Photosystem II at 1.9 Å resolution was used and refined to obtain the optimum structure for the Mn(4)O(5)Ca core within the protein pocket. Employing this model, a set of 26 structures was constructed that tested various protonation scenarios of the water ligands and oxo bridges. Our results suggest that one of the two water molecules that are proposed to coordinate the outer Mn ion (Mn(A)) of the cluster is deprotonated in the S(2) state, as this leads to optimal experimental agreement, reproducing the correct ground state spin multiplicity (S = 1/2), spin expectation values, and EXAFS-derived metal-metal distances. Deprotonation of Ca(2+)-bound water molecules is strongly disfavored in the S(2) state, but dissociation of one of the two water ligands appears to be facile. The computed isotropic hyperfine couplings presented here allow distinctions between models to be made and call into question the assumption that the largest coupling is always attributable to Mn(III). The present results impose limits for the total charge and the proton configuration of the OEC in the S(2) state, with implications for the cascade of events in the Kok cycle and for the water splitting mechanism.
The procedure for fixing atoms of amino acid residues in cluster model calculations on enzymes is reviewed. Examples from recent calculations on photosystem II (PSII) and Mo,Cu-dependent CO dehydrogenase are given. In this context, the cluster model work on finding a mechanism for O-O bond formation and a structure of the oxygen-evolving complex in PSII is also reviewed. In that work, fixing certain atoms played an important role. The main part of the present study concerns the mechanism in PSII using models based on the new high-resolution (1.9 Å) X-ray structure, which is compared to that using the old, theoretically suggested, structure. It is concluded that the mechanism remains the same, with a similar barrier height. Finally, a connection between the OEC structure and Mn,Ca-containing minerals is also briefly discussed.
Multifrequency electron spin-echo envelope modulation (ESEEM) spectroscopy is used to ascertain the nature of the bonding interactions of various active site amino acids with the Mn ions that compose the oxygen-evolving cluster (OEC) in photosystem II (PSII) from the cyanobacterium Synechocystis sp. PCC 6803 poised in the S(2) state. Spectra of natural isotopic abundance PSII ((14)N-PSII), uniformly (15)N-labeled PSII ((15)N-PSII), and (15)N-PSII containing (14)N-histidine ((14)N-His/(15)N-PSII) are compared. These complementary data sets allow for a precise determination of the spin Hamiltonian parameters of the postulated histidine nitrogen interaction with the Mn ions of the OEC. These results are compared to those from a similar study on PSII isolated from spinach. Upon mutation of His332 of the D1 polypeptide to a glutamate residue, all isotopically sensitive spectral features vanish. Additional K(a)- and Q-band ESEEM experiments on the D1-D170H site-directed mutant give no indication of new (14)N-based interactions.