New Reaction Model for O–O Bond Formation and O2 Evolution

Article pubs.acs.org/JPCA

New Reaction Model for O−O Bond Formation and O2 Evolution Catalyzed by Dinuclear Manganese Complex Makoto Hatakeyama,† Hiroya Nakata,† Masamitsu Wakabayashi,§ Satoshi Yokojima,‡,§ and Shinichiro Nakamura*,†,§ †

Department of Biomolecular Engineering, Tokyo Institute of Technology, B-70, 4259 Nagatsuta, Midori-ku, Yokohama 226-8503, Japan ‡ School of Pharmacy, Tokyo University of Pharmacy and Life Sciences, 1432-1 Horinouchi, Hachioji, Tokyo 192-392, Japan § Nakamura Laboratory, RIKEN Research Cluster for Innovation, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan S Supporting Information *

ABSTRACT: A new mechanism of the oxygen evolving reaction catalyzed by [H2O(terpy)Mn(μ-O)2Mn(terpy)OH2]3+ is proposed by using density functional theory. This proton coupled electron transfer (PCET) model shows reasonable barriers. Because in experiments excess oxidants (OCl− or HSO5−) are required to evolve oxygen from water, we considered the Mn2 complex neutralized by three counterions. Structure optimization made the coordinated OCl− withdraw a H+ from the water ligand and produces the reaction space for H2O2 formation with the deprotonated OH− ligand. The reaction barrier for the H2O2 formation from OH− and protonated OCl− depends significantly on the system charge and is 14.0 kcal/mol when the system is neutralized. The H2O2 decomposes to O2 during two PCET processes to the Mn2 complex, both with barriers lower than 12.0 kcal/mol. In both PCET processes the spin moment of transferred electrons prefers to be parallel to that of Mn 3d electrons because of the exchange interaction. This model thus explains how the triplet O2 molecule is produced.

1. INTRODUCTION Photosystem II contains an oxygen evolving complex, catalyzing the oxidation of water to molecular oxygen, that consists of a tetranuclear Mn cluster and has a double-bridged dinuclear Mn structure (Mn(μ-O)2Mn).1−3 A remarkable highresolution X-ray analysis of its crystal structure has recently been reported by J.-R. Shen and his colleagues,4,5 providing a splendid opportunity to advance research in this field. Some experimentally synthesized multinuclear Mn complexes with similar double-bridged (Mn(μ-O)2Mn) structures catalyze reactions producing molecular oxygen,6−12 and the complex [H2O(terpy)Mn(μ-O)2Mn(terpy)OH2]3+ (terpy denoting 2,2′:6′,2″-terpyridine) (shown in Figure 1 and hereafter denoted 1) has been reported to catalyze oxygen evolution from an oxidant (OCl− or HSO5−) in aqueous solution.6−8 The mechanism of the oxygen evolving reaction catalyzed by this complex has been analyzed experimentally and found from the relationship between oxidant concentration and the rate of O2 evolution to be a Michaelis−Menten type reaction.7 The reaction mechanism proposed by Limburg and his colleagues, hereafter denoted the Limburg model, is shown in Scheme 1. The rate-limiting step in their model is assumed to be the oxidant desorption ((c) to (d) in Scheme 1), and the rate constant for the evolution of oxygen from HSO5− was estimated to be 2420 mol O2 h−1 mol−1. According to the © 2012 American Chemical Society

Figure 1. [H2O(terpy)Mn(μ-O)2Mn(terpy)OH2]3+ (terpy = 2,2′:6− 2″-terpyridine). This complex is referred to in the text as 1.

transition state theory for the oxidant desorption step, the corresponding reaction barrier has been estimated as 18 kcal/ mol.13 The structural details of the O−O bond formation in the oxygen evolving reaction are still unknown, but an already reported theoretical analysis has resulted in what we call the Received: January 6, 2012 Revised: June 2, 2012 Published: June 7, 2012 7089

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Both of these alternatives are interpreted as Mn(IV)−O·, where ↑ and ↓ indicate a localized spin. In this Lundberg model, the reaction barrier for O−O bond formation is 23 kcal/ mol in the lowest energy electronic spin-state. This barrier is higher than the value estimated from the experimental kinetic data (18 kcal/mol) and is not consistent with the experimental Limburg-model, which supposes the rate-limiting step as the oxidant-desorption. Here, we point out two arguments to the Limburg model. The first is in what extent does the Mn(V)O intermediate take part in the O2 evolution? In experimental studies, the Mn(V)O intermediate is considered in order to explain the (18O)2 formation with H218O and the nonlabeled oxidant.15 When the Mn(V)O is formed by the oxidant as shown in Scheme 1, 16O,18O-atom exchange through the Mn(V)O satisfies the (18O)2 formation through the Limburg model.7,8 The presence of such an extremely high oxidation state of Mn(V)O in the reaction has, however, been established neither by evidence obtained in studies of crystal structures nor by other spectroscopic evidence. The (18O)2 accounts of only 12% of the total amount of O2 when the HSO5− oxidant is used. When the OCl− oxidant is used, the 16OCl− intrinsically exchanges the O-atom with H218O in the absence of the Mn2 catalyst.7 Thus, it is worth considering that a part of the O2 evolution may proceed aside from the Mn(V)O intermediate. The second argument concerns the role of oxidants. One sees in Scheme 1 that, in the Limburg model, the contribution of the oxidant (OCl− or HSO5−) is only to generate Mn(V) O for which stoichiometric amounts of oxidants is required. In experiments, however, excess oxidants are necessary, suggesting that oxidants play other important roles. In this study, we consider the possibility that the oxidants ensure electroneutrality at the catalyst and in the reaction field.16 The Mn(III)(μ-O)2Mn(IV) complex 1 has a positive charge (+3.0), while oxidants existing in excess (OCl− or HSO5−) are strong electrolytes having a negative charge (−1.0). Therefore, it is natural that the 1 will be neutralized by the oxidants and that the actual oxygen evolving reaction will be catalyzed by the neutralized 1. Taking these arguments into account, we investigated an alternative mechanism of the O2 evolution catalyzed by the neutralized 1, aside from the Mn(V)O intermediate. We obtained the optimized structure of [H2O(terpy)Mn(μO)2Mn(terpy)OH2](OCl)3 complex with OCl− as an oxidant. From the optimized structure (referred to as 1(OCl)3), we figured out a new mechanism for the O−O bond formation and the consequent O2 evolution through proton-coupled electron transfer (PCET) processes. Here, we also present the transition state (TS) geometries and energies.

Scheme 1. Limburg Model: Mechanism of Oxygen Evolving Reaction Proposed by J. Limburg et al.7,8a

XO indicates an oxidant (OCl− or HSO5−). Only the oxidation numbers are shown in state (d) because the structure of the Mn2 complex after evolving O2 has not been identified. a

Lundberg model (Scheme 2).13,14 According to the calculated spin population, the structures (c)′ and (c)″ in Scheme 2 have Mn(IV)−O· but not the high-valent Mn(V)O. That is, due to the existence of unpaired localized spins on Mn and O· atoms, the state is characterized as follows: Mn( ↑ ↑ ↑ )−O( ↓ ) or Mn( ↑ ↑ ↑ )−O( ↑ )

Scheme 2. Lundberg Model: Schematic Illustration of O−O Bond Formation Mechanism Proposed by M. Lundberg et al.;13,14 After Oxidant Desorption, an Oxyl Radical (O·) Is Formed in State (c)

2. COMPUTATIONAL DETAILS The structures studied in this work were optimized by unrestricted density functional theory (DFT), using the B3LYP exchange-correlation functional.17 The LanL2DZ basis set function was applied for manganese, and the 6-31G(d) basis set was applied for the other atoms. Optimization with a small basis set has already been investigated as sufficient since the final energy is rather insensitive to the quality of the geometry optimization.13,18 Energy differences between respective structures are investigated by using the Gibbs free-energies based on the ideal gas approximation. Thermal corrections due to the intramolecular vibrations are estimated with the Hessian 7090

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optimization, resulting in HO−···H−OCl structures. Only one of the two hydrogens of the water ligand bound to Mn(IV) was withdrawn by OCl−. The structure where one H+ near (μ-O)2− was withdrawn is shown in Figure 2(i, right from center), and the structure where another H+ was withdrawn is shown in Figure 2(ii, left from center). The Gibbs free energy of the structure in Figure 2(i) is 0.2 kcal/mol lower than that of the structure in Figure 2(ii). It is worth noting that no local minimum, which maintains Mn−(OH2)···OCl− structure, was obtained. In addition, the H withdrawing occurred only from waters bound to Mn. When OCl− was added to any other H atom of terpyridine ligands, that atom was not withdrawn by OCl− (Figure 2(iii)). Instead, the energy of those structures was 20−30 kcal/mol higher than that of the structures shown in Figure 2(i),(ii).30 Alternatively, when OCl− is bound to Mn (similar to the state (b) in Scheme 1) and a water ligand is coordinated to one of the oxygens in (μ-O)2− (similar to (c)′ in Scheme 2), the OCl− ligand does not withdraw the H atom of water (as shown in Figure 2-(iv)). These results indicate that, when the 1 is neutralized by excess OCl− oxidants in water solution, the OH− is consistently produced. The OH−, being a strong base, has an oxidation potential smaller than that of water.31 Therefore, the oxygen evolving mechanism driven by OH− is expected to have a reaction rate faster than that driven by H2O. In all the calculation processes, the solvent effect was taken into account by the PCM scheme. This solvent effect enables not only the H+ withdrawing by OCl− but also the prevention of an artificial electron transfer from OCl− to Mn ions. Notice that the B3LYP method is not impossible to show positive occupied-orbital energies in anion species such as OCl− and to invoke an artificial electron transfer from the anion to cation species such as MnIII/IV. When an isolated OCl− is calculated by using B3LYP/6-311+G(d,p) in the vacuum state, the anion actually showed the positive HOMO energy of +5.7 (kcal/ mol). However, the HOMO energy is corrected to be −126.2 (kcal/mol) by using the PCM scheme. 3.2. New Mechanism for Triplet O 2 Molecule Evolution. Structure optimization of 1(OCl)3 led to the OH− ligand formation on Mn as a result of the H atom withdrawing by OCl−. The O-atom in this OH− ligand has a chance to form an O−O bond since there is enough bonding space around oxygen atoms. This result motivated us to investigate the possibility of a new mechanism for the O−O bond formation and O2 evolution (Scheme 3). We call it the proton coupled electron transfer (PCET) model. 3.2.1. Mechanism of O−O Bond Formation. At state (a) in Scheme 3, an HO−···H−OCl structure is formed (Figure 2). From (a) to (b), HOCl transfers from the HO− ligand to one of the O-atoms in the bridged oxygens (μ-O)2−. This transfer produces sufficient space for O−O bond formation ((b) in Scheme 3). If orbitals on O-atoms overlap, the O−O bond formation eventually proceeds ((c) in Scheme 3). As shown in Scheme 4, the process from state (b) to state (c) consists of four concerted rearrangements: (i) fission of the O−Cl bond in HOCl, (ii) formation of an O−O between the OH− ligand and the HO of HOCl, (iii) transfer of an electron from the OH− ligand to the Cl atom of HOCl, and (iv) H+ withdrawing from the OH− ligand to the attached OCl−. The concerted process of O−Cl bond fission and O−O bond formation, satisfying energy balance of bond breakage and formation,32 results in an electron transfer from an OH− ligand to a Cl atom. The Cl atom becomes a Cl− anion bonding weakly to H2O2. In fact, the

calculated by using unrestricted B3LYP/(LanL2DZ+631G(d)). Following the geometry optimization, the electronic energy is refined by using the LanL2TZf19 basis set for Mn and 6-311+G(d,p) for others. Other basis sets (Ahlrichs TZVP20 and cc-pVTZ for all atoms) are also examined, in order to verify the reliability of the energies, which may depend on the size of basis sets. Electronic energies are also examined by using dispersion-corrected DFT functionals (B97D 21 and wB97XD22) and other functionals (wB97X23 and M0624). To take the solvent effect of water into account, the polarizable continuum model (PCM) was applied for all DFT calculations.25 All structural optimizations were accomplished in two steps, as in the flip-spin procedure:26 optimization for the high-spin state, and then optimization for the low-spin state. In the calculation of the high-spin state, the number of unpaired electrons with α-electron spin was set equal to the total number of d electrons in two manganese atoms. This procedure was based on an experimental finding that a mononuclear Mn complex is in a high-spin state.27 Still, we investigated the possibility of the low-spin state. In the calculation of the lowspin state, the initial guess for electron density was constructed in such a way as to divide a calculated model into fragments,28 and either α or β electron spin was assigned to each fragment. In the analysis for the oxidation number of the manganeses and the net-charge of atoms and coordinated ligands, Mulliken’s electron (spin) population analysis was used. All the calculations were performed using the Gaussian 09 program package.29

3. RESULTS AND DISCUSSION 3.1. Optimized Structure of [H2O(terpy)Mn(μ-O)2Mn(terpy)OH2](OCl)3, 1(OCl)3. Two representative optimized structures of 1(OCl)3 are shown in Figure 2, where H atoms in water ligands were withdrawn by OCl− during the structural

Figure 2. Optimized structure of 1(OCl)3. Mn(III) and Mn(IV) are assigned by considering the Mulliken’s spin population. The colors for atoms are purple for manganese, green for chlorine, red for oxygen, blue for nitrogen, gray for carbon, and white for hydrogen. Structure (iv), where OCl− is coordinated to Mn(IV) directly, is analogous to the state (b) in Scheme 1. 7091

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Scheme 3. PCET Model: Schematic Illustration of New Mechanism for the O−O Bond Formation Catalyzed by 1a

a Net charge on OH− ligand and Cl− is indicated to show an electron transfer during the reaction. The process from state (d)′ to (a) represents the regeneration of 1; i.e., oxidation of 1 from Mn(II)/Mn(III) to Mn(IV)/Mn(III), deprotonation of (μ−OH)− and rearrangement of Cl−, OCl−, HOCl, and H2O. Jahn−Teller axes around the Mn(III) and Mn(II) are represented in the red lines.

Scheme 4. Schematic Illustration of the O−O Bond Formation Mechanism in the PCET Model for the Neutralized 1(OCl)3a

a

For clarity, terpyridine ligands are omitted. Dashed arrows represent the nuclear motion.

produced H2O2 is partially polarized as HOOδ−···H δ+ by the Hδ+ withdrawing of the attached OCl− (see also Table S1, Supporting Information, where Mn2−O6 in state (c) corresponds to the (H2O2)−Mn(IV) distance). 3.2.2. Mechanism of O2 Evolution after O−O Bond Formation. In the PCET model, once the O−O bond and

HOOH structure are formed ((c) in Scheme 3), O2 evolution can occur, if two PCETs from O−O to Mn are assumed.35 At the onset of the first PCET, a Cl− ion dissociates from one H atom of H2O2 to an H atom of a terpyridine ligand.36 The first PCET (from O−O to Mn) is followed by a proton transfer 7092

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mechanism by HSO5− may have to be distinguished from the reaction by OCl− and the PCET model because of pKa. The HSO5− shows the pKa < 0.0 in the protonated-form (H2SO5),37 while the OCl− shows the pKa of about 7.5 in the protonated form.38 These pKa values are critical to determine the details of the mechanism since the PCET model starts with the deprotonation of the Mn(IV)-coordinated H2O ligand. 3.3. Free-Energy Diagram of PCET Model. A Gibbs free energy diagram of PCET model is shown in Figure 3, where only the low-spin state results are shown because the energies of all the high-spin states were higher than those of low-spin states (see Figure S1 of Supporting Information). To confirm the effect of electroneutrality, the energy diagram for the nonneutralized [1(OCl)]2+ complex was also calculated and is shown as (ii) in Figure 3. The [1(OCl)]2+ was constructed by omitting two OCl− from 1(OCl)3, one OCl− from the vicinity of Mn(III) and the other from the vicinity of Mn(IV) (being away from (μ-O)2−). One OCl− remains near Mn(IV) and (μO)2− so as to accomplish O−O bond formation ((b) to (c) in Scheme 3) and HOCl transfer ((a) to (b) in Scheme 3). In addition, Mulliken’s atomic spin densities and Mn ligand distances are calculated as a function of reaction step, as shown in Table S1 and S2, Supporting Information. 3.3.1. O−O Bond Formation. In the (ii) results, one sees a large barrier, 24.0 kcal/mol, between (b) and (c) (TS-2). This value is more or less comparable to the value calculated using the Lundberg model for O−O bond formation (23−28 kcal/ mol).13 In contrast, the addition of counterions (i.e., electroneutrality) lowered the reaction barrier of TS-2 to 14.0 kcal/ mol (see results (i) in Figure 3). There are two viewpoints to explain the lowering of the barrier of O−O bond formation (24.0 to 14.0 kcal/mol) by neutralization; (i) total charge and (ii) local arrangement for bond formation. The first one (i) is explained as follows. In Scheme 1, the O− O bond formation in the PCET model proceeds together with the transfer of one electron from OH− to a Cl atom. Because of

from HOOH to one of the oxygens of the bridge (μ-O)2 (from (c)′ to (c)″ in Scheme 3 and in Scheme 5). Scheme 5. Schematic Illustration of the First PCET Step for the Neutralized 1(OCl)3a

a

For clarity, terpyridine ligands are omitted. Dashed arrows represent the nuclear motion.

The second PCET occurs together with the deprotonation from HOO· to form O·−O· HOCl ((c)‴ in Scheme 3). In each PCET, an electron transfers from a πy* or πz* orbital of the O− O bond to an Mn-centered orbital (the x axis is the O−O bonding line). The spin moment of transferred electrons can be parallel to the spin moment of the 3d electrons of the Mnatom, thereby stabilizing the system because of the exchange interactions (see section 3.3). 3.2.3. Mechanism of (18O)2 Evolution in H218O Solution. The evolution of (18O)2 has been shown experimentally by using the isotope-labeled H218O solvent.7 Although the amount of (18O)2 is only 12% of the total amount of O2, we examined this mechanism. The PCET model shown in Scheme 3 is still consistent with the mechanism of (18O)2 evolution, when we take into account the following fact. The isotope analysis for the O2 evolution has also reported that the OCl− oxidants exchange the O-atom with H218O solvents.7 Therefore, the exchanged 18OCl− oxidants can form (18O)2 with the Mn(IV)coordinated H218O ligand, along with the PCET model. Notice that the other oxidant (HSO5−) has shown no Oatom exchange with H218O. However, the O2 evolution

Figure 3. Calculated Gibbs free energy diagram of PCET model for the O−O bond formation and O2 evolution. Notations along with horizontal axis are the same as in Scheme 3. Compounds shown below the energy levels represent the schematic illustration of 1 in each reaction step. Results shown in blue (i) are for neutral 1(OCl)3, and results shown in red (ii) are for [1(OCl)]2+. 7093

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this dissociation of Cl− ion from 1, the O−O bond formation results in charge separation between Cl− and [(H2O2)(terpy)Mn(μ-O)2Mn(terpy)(OH2)](OCl)x (x = 2 in (i), and 0 in (ii)). In the process, the charge on the Mn2 complex depends on the charge of the total system. When the system is neutralized ((i) in Figure 3), the Mn2 complex is coordinated by two OCl− ions at the charge separation, and the charge becomes 1+. However, when the system charge is 2+ ((ii) in Figure 3), the system charge amounts to 3+ at the charge separation. Naturally, the neutralized state can shift more easily to the charge-separated state (from 0 to 1+) than the 2+ state can shift to the 3+ state. The discussion is also valid in the case from 1+ to 2+ (see Figures S2 and S3, Supporting Information).39 The second viewpoint (ii) to explain the low barrier of O−O bond formation is the following. As shown at the TS-2 in Scheme 4, in a concerted way, the OCl−, which attaches to the OH−, withdraws the Hδ+ of OH−, during the O−O bond formation. In fact, the barrier of the TS-2 is different with OCl− and without OCl− on the OH− shown at the left in Scheme 4, respectively. The detailed features are shown in Figure S3, Supporting Information. Thus, the lower barrier for O−O bond formation is understood. In order to examine more of the effect of the counterions, the free-energy diagram of 1(OCl)(NO3)2 is also analyzed, as shown in Figures S4 and S5, Supporting Information. The NO3− has been known to coordinate to the crystal structure of 1,6 and HNO3 shows the negative pKa different from the pKa = 7.5 of HOCl. The reaction barrier of O−O bond formation is increased to 19.8 (kcal/mol), compared to the 14.0 (kcal/mol) of 1(OCl)3. Still, the low barrier of O−O bond formation for 1(OCl)3 is not changed significantly when an extra two H2O solvent molecules are explicitly coordinated to 1(OCl)3, as shown in Figures S6 and S7, Supporting Information. It is noteworthy that, in the transition from (a) to (b) through TS-1, the barrier without the counterions (ii) is lower than that with them (i). Although unexpected, this is rationalized as follows. Because the transition (a) to (b) is an HOCl transfer from OH− to (μ-O)2−, its reaction barrier depends on the strength of the HO−···HOCl hydrogen bond. The optimized bond lengths are 1.46 for (i) and 1.58 Å for (ii). In fact, the addition of two counterions increases the polarization (more negative charge on the O-atom in HO−), with the result that Hδ+Oδ−···HOCl hydrogen bonding becomes strong.40 3.3.2. Triplet O2 Evolution. After the O−O bond formation, three transition states (TS-3, TS-4, and TS-5) are involved in the charge-neutral compounds ((i) in Figure 3), while, in the case of the dication compound ((ii) in Figure 3), there is an additional barrier between TS-3 and TS-4 (there are four transition states between (c) and (d)). As shown in the energy diagram for O2 evolution ((c)′ to (d) in Figure 3), the electron transfers from the O−O bond to a Mn-atom. It may be preferred that the spin moment of transferring electrons are in parallel to that of the Mn-atom 3d electrons. In order to confirm this, two spin configurations (parallel and antiparallel shown in Scheme 6) of the product of the first PCET ((c)″ in Scheme 3) are compared. Without counterions (results (ii) in Figure 3), the parallel configuration (state (i) in Scheme 6) has an energy 14.5 kcal/mol lower than that of the antiparallel configuration ((ii) in Scheme 6). With OCl− counterions (results (i) in Figure 3), the energy of the parallel configuration is 16.1 kcal/mol lower than that of the

Scheme 6. Schematic Illustration of Spin-Configuration in the Product of the First PCETa

a

For clarity, terpyridine ligands are omitted. Solid (dashed) arrows represent the remaining (transferring) electron-spins after the PCET. Dashed arrows with unfilled arrowheads represent the electron motion.

antiparallel configuration. Thus, an electron transferred to a Mn-atom prefers to have its spin parallel to that of the Mnatom electrons. Notice that, if the entropy is not taken into account, the barrier height for TS-5 is more than 17.0 kcal/mol (see Figure S10, Supporting Information, in details), indicating the importance of the entropy in determining the reaction barrier of the O2 desorption process. 3.3.3. Dependence on the Basis Sets and DFT Functional. The dependence of the free-energy diagram on the basis sets is analyzed by changing the (LanL2TZf+6-311+G(d,p)) basis sets to Ahlrichs TZVP and cc-pVTZ, as shown in Figure S8, Supporting Information. B3LYP calculation with all-electron large basis sets increase those reaction barriers only by about 1.0−3.0 kcal/mol, along with the structures optimized by B3LYP/(LanL2DZ+6-31G(d)) calculation. The dependence of the free-energy diagrams on the DFT-functional (B97D, wB97XD, wB97X, and M06) is analyzed with (LanL2TZf+6311+G(d,p)) and shown in Figure S9, Supporting Information. The M06 functional increases the barrier of the O−O bond formation to 20.2 kcal/mol. This barrier may seem to be consistent with the experimental maximum reaction rate 6.5 mol O2 h−1 mol−1 because the experimental rate is comparable to about 20 kcal/mol barrier within transition state theory. 3.4. Details of Transition States in PCET Model. Here, we will discuss the geometry and electronic structure of TSs in the PCET model. Figure 7 shows the transition state structure of 1(OCl)3 in O−O bond formation ((b) to (c) in Scheme 3 and TS-2 in Figure 3). Also shown in Figure 4 is the third highest occupied Kohn−Sham (KS) orbital (α-spin). The orbital shows that there is the σ* interaction between O···O and O···Cl pairs. In this transition state, the O−O bond formation and O−Cl bond fission are aligned in the same line. This linearity makes the shortest path for the electron transfer from the HO− ligand to the Cl atom (see Scheme 4). In this TS, the HOCl unit moves smoothly, with the H pivoting around a (μ-O) atom. The intrinsic reaction coordinate (IRC) shows that, just before the transition state, σ*O−O contributes more to the third highest occupied orbital than σ*O−Cl does. After the transition state, the contribution of σ*O−O decreases, and the contribution of σ*O−Cl increases. The O···O and O···Cl 7094

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Figure 6. Highest occupied β-spin orbital of 1(OCl)3 in TS-5 of the PCET model. Notations πy* and 3dxy* correspond to the orbital interaction explained in section 3.4.

highest KS orbital occupied by β-spin electrons. This is the late TS, which is very similar to the intermediate releasing molecular O2 ((c)‴ in Scheme 3). The O···Mn bond length is 3.6 Å (see Table S1(i), Supporting Information). The Mn− (μ-O)2− bond lengths are about 2.1 Å. They are longer than the ordinary Mn−(μ-O)2− bond lengths (1.7−1.9 Å). The KS orbital shows the characteristic of PCET, where the antibonding 3d(Mn) character exists. 3.5. Validation of Computational Accuracy. To verify the computational accuracy for the neutralization of catalytic Mn2 complex, we evaluated the oxidation potential of 1 (corresponding to the change from Mn(IV)/Mn(III) to Mn(IV)/Mn(IV)) and compared it with the value measured experimentally.35c,43 The data of cyclic-voltammetry in the various pH condition are available (from 2.0 to 6.0).35c We took the value at pH ≈ 6.0 (about 1.1 V vs NHE) for comparison with the calculations. Note that the O2 evolution reaction has been measured at pH ≈ 8.6, when OCl− oxidants are used.6−8 Two structures were analyzed; the non-neutralized 1 complex shown in Figure 1, and the neutralized 1(NO3)3 complex shown in Figure 7. The 1(NO3)3 complex was used because cyclic-voltammetry results are available for experiments with NO3− (but not OCl−) as the counterion for 1. In the neutralization, the NO3− counterions are also expected to withdraw H+ from the water ligands after the oxidation of 1(NO3)3 because the oxidation of 1 has been thought as to

Figure 4. Third highest occupied α-spin orbital of 1(OCl)3 in TS-2 of the PCET model. The σ* notation corresponds to the orbital interaction explained in section 3.4.

pairs also have π* interactions having almost the same weights.41 As the reaction passes through the TS, the weight of the π* interaction shifts from O···O to O···Cl. The increase of antibonding character in O···Cl reflects the electron transfer from OH− to Cl. The structure of 1(OCl)3 in the transition state of the first PCET from H2O2 to Mn(IV) ((c)′ to (c)″ in Scheme 3 and TS4 in Figure 3) is shown in Figure 5 together with the highest

Figure 5. Highest occupied β-spin orbital of 1(OCl)3 in TS-4 of the PCET model. Notations πz* and 3dz2* correspond to the orbital interactions explained in section 3.4.

occupied KS orbital by β-spin electrons.42 The orbital shows the interaction between a π* orbital of O−O and an antibonding 3d orbital of Mn, with the electron transferring from H2O2 to Mn(IV). As a result of the electron transfer, at the transition state the Mn (to which H2O2 is bound) has a spin population of −3.5 (the negative value representing an excess of β-spin electrons, see Table S2(i), Supporting Information). We note that, in the transition state shown in Figure 5, Cl− ions have hydrogen bonding with terpyridine ligands but not with H2O2. As long as the Cl− retains the hydrogen bonding with H2O2, the PCET cannot be accomplished. In other words, as long as the Cl− retains Cl−···H2O2 interaction, the reaction does not go through the transition state, and Mn shows a spin population of about −3.0 or −4.0. The structure of 1(OCl)3 at the transition state of the second PCET from HOO· to Mn(III) ((c)″ to (c)‴ in Scheme 3 and TS-5 in Figure 3) is shown in Figure 6 together with the

Figure 7. Optimized structure of 1(NO3)3. The colors for atoms are purple for manganese, red for oxygen, blue for nitrogen, gray for carbon, and white for hydrogen. 7095

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Computing Center at the Tokyo Institute of Technology and also thank the RIKEN Integrated Cluster of Clusters (RICC) for the computer resources used for the calculation. This work was partially supported by the KAITEKI Institute, Inc. (Mitsubishi Chemical Holdings).

couple with the deprotonation on the terminal water ligands. The procedure we used to calculate oxidation potential was based on that used by Fu et al.44 To calculate the change of solvation free energy during the oxidation, we used two different solvation models; the first is the PCM model that is already used in the calculation of the free-energy diagram for the PCET model, and the second is the SMD model that has been parametrized to show quantitatively correct solvation energy.45 The oxidation potential calculated for 1 (without counterions) was 1.90 V with PCM and 1.33 V with SMD, respectively. The latter value is also close to the already reported value (1.40 V), calculated by using cc-pVTZ(-f) basis sets and the Poisson−Boltzmann salvation model.46 Instead, the potential for 1(NO3)3 was 1.21 V with PCM, and 1.06 V with SMD, respectively, and the latter value is close to the experimental value (about 1.1 V) at pH ≈ 6.

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4. CONCLUSIONS We propose a new mechanism of the O−O bond formation and O2 evolution catalyzed by the [H2O(terpy)Mn(μ-O)2Mn(terpy)OH2](OCl)3 complex. Using the B3LYP functional to calculate the reaction barriers of this PCET model, we found that, when the Mn2 complex is neutralized by OCl− oxidants, all of the barriers are lower than 14.0 kcal/mol, which is accessible at room temperature, and are lower than the 23 kcal/mol barrier obatined in the previous Lundberg model. The present PCET model is an alternative mechanism to understand the Lundberg and Limberg models, which include an Mn(V)O intermediate. The PCET model for the case of the OCl− oxidant explains the results of the isotope study without including the Mn(V)O intermediate. The proposal of the PCET model is based on two important considerations: (i) including oxidants (OCl−) explicitly in the calculations and (ii) starting from the charge-neutralized reactants. The OCl− oxidant, which is in excess in experiments, enables HO− to form from Mn-bound water (OCl− acting as an activator) and an O−O bond to form by accepting an electron transferred from HO−. Barriers accessible at room temperature are achieved on the condition of electrostatic neutrality. The current study provides insight into the O2 evolution mechanism in photosystem II.

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ASSOCIATED CONTENT

S Supporting Information *

Free-energy diagram of PCET-model by S = 1/2 and S = 7/2 state, free-energy diagram calculated by using further large basis sets, free-energy diagram of 1+ system, the change of Mn− ligand distances, and Mulliken’s spin popuration during the O2 evolution in the PCET-model. This material is available free of charge via the Internet at http://pubs.acs.org.

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REFERENCES

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AUTHOR INFORMATION

Corresponding Author

*Phone: +81-048-467-9477. Fax: +81-048-467-8503. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank Professor Jian-Ren Shen for valuable discussion. We thank TSUBAME 2.0 at the Global Scientific Information and 7096

dx.doi.org/10.1021/jp300174n | J. Phys. Chem. A 2012, 116, 7089−7097

The Journal of Physical Chemistry A

Article

HO− away from the Mn. As a result, the O-atom in HO− becomes electron-rich and the HO−···HOCl hydrogen bonding is strengthened. (41) Frontier occupied orbitals of 1(OCl)3 in the TS-2 state are shown in Figures S10−15,Supporting Information. σ* interaction in the O···O···Cl structure appears in Figures S10 (highest occupied Kohn−Sham orbital) and S15, and this interaction is similar to that shown in Figure 4. π* interaction appears in other orbitals and is also mixed into orbitals having σ* character (shown in Figures 4, S10, and S15). (42) Since 3d electrons are localized at Mn(IV) with having β-spin moment, β-spin electrons prefer to transfer through exchange interaction. (43) Baffert, C.; Romain, S.; Richardot, A.; Lepretre, J.-C.; Lefebvre, B.; Dronzier, A.; Collmb, M.-N. J. Am. Chem. Soc. 2005, 127, 13694− 13704. (44) Fu, Y.; Liu, L.; Yu, H.-Z.; Wang, Y.-M.; Guo, Q.-X. J. Am. Chem. Soc. 2005, 127, 7227−7234. (45) Marenich, A. V.; Cramer, C. J.; Truhlar, D. G. J. Phys. Chem. B 2009, 113, 6378−6396. (46) Wang, T.; Brudvig, G. W.; Batista, V. S. J. Chem. Theory Comput. 2010, 6, 2395−2401.

(26) Pantazis, D. A.; Orio, M.; Petrenko, T.; Zein, S.; Lubitz, W.; Messinger, J.; Neese, F. Phys. Chem. Chem. Phys. 2009, 11, 6788−6798. (27) (a) Manchanda, R.; Grudvig, G. W.; Crabtree, R. H. Coord. Chem. Rev. 1995, 144, 1−38. (b) Libby, E.; Folting, K.; Huffman, C. J.; Huffman, J. C.; Christou, G. Inorg. Chem. 1993, 32, 2549−2556. (28) Vacek, G.; Perry, J. K.; Langlois, J.-M. Chem. Phys. Lett. 1999, 310, 189−194. (29) Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Nakatsuji, H.; Caricato, M.; Li, X.; Hratchian, H. P.; Izmaylov, A. F.; Bloino, J.; Zheng, G.; Sonnenberg, J. L.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T.; Montgomery, J. A., Jr.; Peralta, J. E.; Ogliaro, F.; Bearpark, M.; Heyd, J. J.; Brothers, E.; Kudin, K. N.; Staroverov, V. N.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A.; Burant, J. C.; Iyengar, S. S.; Tomasi, J.; Cossi, M.; Rega, N.; Millam, J. M.; Klene, M.; Knox, J. E.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Martin, R. L.; Morokuma, K.; Zakrzewski, V. G.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Dapprich, S.; Daniels, A. D.; Farkas, O.; Foresman, J. B.; Ortiz, J. V.; Cioslowski, J.; Fox, D. J. Gaussian 09, revision A.02; Gaussian, Inc.: Wallingford, CT, 2009. (30) This result is consistent with the calculated Mulliken atomic charges in 1. In 1 having no oxidant, the atomic charge of H atoms in water ligands is about 0.50 on the average and is much larger than the 0.21 of H atoms in terpyridine ligands. (31) (a) Sawyer, D. T. Acc. Chem. Res. 1988, 21, 469−476. (b) Pearson, R. G. J. Am. Chem. Soc. 1986, 108, 6109−6114. (32) This can be expected when the energies of the breaking and forming bonds are of the same order of magnitude. The energy of the O−Cl in CH3OCl is 51 kcal/mol,33 and the energy of the O−O in H2O2 is 45 kcal/mol.34 (33) He, T.-J.; Chen, D.-M.; Liu, F.-C.; Sheng, L.-S. Chem. Phys. Lett. 2000, 332, 545−552. (34) Bach, R. D.; Ayala, P. Y.; Schlegel, H. B. J. Am. Chem. Soc. 1998, 118, 12758−12765. (35) When an O2 molecule is produced from H2O2, two e− and two H+ should be eliminated from H2O2. In modeling this e− and H+ extraction, we followed previous studies of photosystem II that have emphasized the importance of PCET for the water oxidation and O2 evolution: (a) Huynh, M. H. V.; Meyer, T. J. Chem. Rev. 2007, 107, 5004−5064. (b) Tommos, C.; Babcock, G. T. Biochim. Biophys. Acta 2000, 1458, 199−219. (c) Cady, C. W.; Shinopoulos, K. E.; Crabtree, R. H.; Brudvig, G. W. Dalton Trans. 2010, 39, 3985−3989. (36) The detailed mechanism of first PCET differs between the 1(OCl)3 and [1(OCl)]2+ systems. When the transition states were analyzed, [1(OCl)]2+ having Cl− coordination to terpyridine did not show the transition state. Instead, [1(OCl)]2+ having Cl− coordination to H2O2 (coordination produced by Cl− migration after H2O2 formation) showed the transition state. Because of this Cl− migration, the energy diagram of [1(OCl)]2+ shows an additional barrier before the first PCET ((c) to (c)′ in Figure 3). (37) Ball, D. L.; Edwards, J. O. J. Am. Chem. Soc. 1956, 78, 1125− 1129. (38) Morris, J. C. J. Phys. Chem. 1966, 70, 3798−3805. (39) The discussion is also valid in the case of 1+ systems. In the 1+ systems shown in Figure S2(i) of the Supporting Information (where two OCl− ions are coordinated to the water ligand bound to Mn(IV)), the barrier for O−O bond formation is 11.6 kcal/mol (the energy diagram shown in result (i) of Figure S3), and in the 1+ system shown in Figure S2(ii), where a OCl− ion is coordinated to each water ligand, the barrier for O−O bond formation is 16.5 kcal/mol (the diagram shown in result (ii) of Figure S3). (40) Another counterion is also added to a water ligand that is far away from the HO− ligand. It contributes to the reaction barrier for HOCl transfer. When H atoms in the water ligand are pulled by counterions, the water is polarized and located close to Mn. This structural change is brought by the (μ-O)2−−Mn bond and pushes the 7097

dx.doi.org/10.1021/jp300174n | J. Phys. Chem. A 2012, 116, 7089−7097