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Theory of chemical bonds in metalloenzymes VI: Manganese–oxo bonds in the photosynthesis II system
Polyhedron 26 (2007) 2216–2224 www.elsevier.com/locate/poly
Theory of chemical bonds in metalloenzymes VI: Manganese–oxo bonds in the photosynthesis II system K. Yamaguchi *, S. Yamanaka, H. Isobe, M. Shoji, K. Koizumi, Y. Kitagawa, T. Kawakami, M. Okumura Department of Chemistry, Graduate School of Science, Osaka University, Toyonaka, Osaka 560-0043, Japan Received 23 October 2006; accepted 24 October 2006 Available online 9 December 2006
Abstract Electronic and spin structures of high-valent manganese–oxo bonds in the photosynthesis II system (oxygen evolving center, OEC) are investigated by the use of spin polarized hybrid DFT (HDFT) method. Theoretical calculations of a high-valent manganese–oxo porphyrin complex are also performed to elucidate common characteristic of the active Mn@O bonds in both native OEC and artificial systems. The oxygen site of the high-valent Mn@O is found to be electrophilic in nature, in accord with our previous work, where the SE2, 1 O- and 3O-models have been presented for theoretical understanding of complex behaviors of oxygenation reactions by metal–oxo species. The 1O- and 3O-models are applicable to model complexes examined here, since the manganese–oxo bonds exhibit strong biradical character. Possibility of the SE2-like transition structure model for OEC is also discussed on both the theoretical and experimental grounds. Implications of present computational results are discussed in relation to hydroxylation reaction by MMO and P450. 2006 Elsevier Ltd. All rights reserved. Keywords: Manganese–oxo bond; Photosynthesis II; Oxygen evolution; SE2 reaction; B3LYP
1. Introduction Most of the oxygen in the atmosphere is generated by plants, algae and cyanobacteria by the photoinduced oxidation of water to dioxygen [1]: 2H2 O ! O2 þ 4Hþ þ 4e
ð1Þ
The oxygen-evolving center (OEC) of the photosynthesis (PS) II system, that catalyzes the reaction in Eq. (1), has been found to contain a cluster of four Mn atoms, calcium ion and chloride anions. Recently, Ferreira et al. [1] have reported the X-ray structure of OEC in PS II of cyanobac˚ resoluterium (Thermosynechococcus elongatus) at 3.5 A tion. Their X-ray data show that the OEC contains a cubane-like CaMn3O4 (1) cluster linked to a fourth Mn by a mono-l oxo bridge with the surrounding coordination *
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0277-5387/$ - see front matter 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.poly.2006.10.054
sphere as illustrated in Fig. 1. The currently accepted model of photosynthetic water oxidation involves five intermediate states from S0 through S1, S2 and S3 to S4 (the so-called Kok mechanism) [2]. The tetranuclear Mn complex in the OEC (1) is thought to couple the four-electron oxidation of water in Eq. (1) with the cyclic one-electron photochemistry (totally 4-electron transfers), namely S0 ! S1 ! S2 ! S3 ! S4 ! S0 (Kok cycle), in PS II. P680 and tyrosyl groups play important roles for these electron-transfer processes. A lot of experimental studies on the Mn OEC in PS II have been carried out to elucidate mechanisms of oxygen evolution from water [1,2]. Many review articles [3–11] have already been published to elucidate them on the basis of accumulated results. The experimental studies of several Mn model complexes have also been carried out extensively [12–16]. Several theoretical studies on the Mn complexes have been carried out to elucidate the electronic structures of Mn OEC [17,18]. The LCAO Xa calculation of the
K. Yamaguchi et al. / Polyhedron 26 (2007) 2216–2224
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Fig. 1. CaMn4O5 cluster (1) in the photosynthesis II and related cubane Mn4O4 (2), triangular Mn3O4 (3), and cubane CaMn3 (4) clusters. 2 and 3 exhibit the tetrahedral and triangular (antiferromagnetic) spin alignments, respectively, at the low-spin state.
tetranuclear manganese complex Mn(IV)Mn(III)3Cl7(O2CCCH3)3]3, a cubane complex, has been carried out to elucidate its electronic and spin states [16]. Belinskii [18] has carried out the theoretical studies on the mixed-valence Mn(III)3Mn(IV) and Mn(IV)3Mn(III) clusters on the basis of the quantum Heisenberg models, assuming trapezoid, butterfly, bent, T-type and distorted tetrahedron structures. Possible ground spin states for these five structures have been elucidated, changing effective exchange interactions between manganese ions. We have examined possible spin structures of tetranuclear (2) [19] and trinuclear (3,4) [20] manganese clusters in Fig. 1 on the basis of the spin vector model [21]. The strong spin frustration [15] in 3 and 4 [20] has provided non-collinear spin structures such as triangular spin structure in Fig. 1, on the assumption of the experimentally determined effective exchange integrals (Jij). The Jij values for the binuclear manganese complexes [22,23] have been calculated using the hybrid DFT method to elucidate the mechanisms for effective exchange interactions between Mn ions [24] LS
J ij ¼
EðXÞ HS EðXÞ ; HS h b S 2 iðXÞ LS h b S 2 iðXÞ
ð2Þ
S 2 iðXÞ are the total energy and total where YE(X) and Y h b angular momentum for the state Y(= LS; the lowest spin state, HS; the highest spin state) by the method X (= UHF, UMPn, UDFT, etc.). It was shown that the sign of Jij is negative because of the greater stability of LS than HS, and the magnitude of Jij values is variable with the oxidation numbers of Mn ion. The calculated Jij values have been consistent with the experiments available. Very
recently, Yamanaka et al. [25] have performed the DFT calculation of cubane-type Mn(II)4 cluster (2) using the general spin orbitals (GSO), namely, two component spinor. The resulted spin structure of 2 was consistent with the tetrahedral type in Fig. 1. The variations of charge and spin populations of manganese oxo (MnO) bonds with the oxidation number of Mn ion were also examined by the unrestricted Hartree– Fock (UHF) method [24]. It was concluded that the nature of oxygen atom in the manganese oxo bond (X = O in 5) varies from nucleophilic to electrophilic with the change of formal charge of Mn ion from low (II) to high (V) valent as illustrated in Fig. 2. The oxygen atom in the Mn(V)O core exhibited the radical character responsible for the radical reactivity for water [24–28]. These results enabled us to propose three possible models of oxygenation reactions of substrates by metal–oxo species: (1) SE2 model, (2) 1Omodel and (3) 3O-model as shown in Fig. 3 [25,26]: note that singlet and triplet states of atomic oxygen undergoes, respectively, insertion and abstraction reactions with X–H bonds (X = CH3, OH, etc.). Similar situations are expected for low-spin (LS) and high-spin (HS) metal-oxo species. As a first step toward theoretical approaches to water oxidation in OEC, Isobe et al. [28] have performed the DFT calculation of the model compound XH3Mn(IV)O2Mn(IV)H3Y (X,Y = O, H) (6) for the Limburg compound [(terpy)(H2O)Mn(l-O) 2Mn(terpy)(H2O)]3+ (7) [29] as shown in Fig. 2. It was found that electron correlation plays a crucial role to determine the nature of manganese–oxygen bonds in 7. Diradical or nonradical mechanism is found to be feasible for the oxygen atom transfer from water to high-valent manganese–oxo bond Mn(V)@O
Fig. 2. Variations of electronic structures of the manganese–oxo bond (5), and Mn–oxo model complexes (6, 7, and 8) for oxygen evolution center (OEC).
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K. Yamaguchi et al. / Polyhedron 26 (2007) 2216–2224
Protein Data Bank (PDB code 1S5L) [1]. All calculations were performed with the Gaussian 98 program package [34]. To obtain the symmetry-adapted (SA) picture for the broken-symmetry (BS) UB3LYP calculations, we have used the natural orbitals, which are determined by diagonalizing their spin-traced first-order density matrices c [23–28] as X ni /i ðrÞ/i ðr0 Þ; ð3Þ cðr; r0 Þ ¼ i
Fig. 3. SE2, 1O- and 3O-models for oxygenation reactions of X–H (X = CH3, OH, etc.), bonds and expoxidation reactions of C–C double bonds in Refs. [24,28]. The discrete radicals are generated in the 3O-model, though such species are hardly detectable in the 1O-model because of rapid recombination (or insertion).
in 7. The environmental effects such as solvent are considered to play an important role for control of the mechanism. The electronic and spin structure of the CaMn3O4 cluster 4 in 1 have been elucidated on the basis of both classical (spin vector) and quantum Heisenberg models [30]. The GSO DFT calculations of the cluster 4 were also performed to elucidate charge and spin populations and noncollinear spin structure (see 4 in Fig. 1). Possible reaction mechanisms of 1 have been proposed on the theoretical and experimental grounds [30]. However, the detailed computations of the metal–oxo part in 1 have not been performed yet. As a continuation of previous work [24–28,30], we here perform theoretical studies on the high-valent Mn–O bonds in OEC and porphyrin model complexes 8. The electronic structures of these species are investigated from the viewpoint of charge and spin populations, and diradical character. The strong diradical character of the Mn(V)@O bonds in the model complexes is consistent with the 1Oand/or 3O-models for oxygenations of X–H bonds. The SE2 mechanism in Fig. 3 is also examined as a possible model of the transition state of the O–O bond formation process. Implications of the calculated results are discussed in relation to possible mechanisms of oxygen evolution in OEC. Our previous [22–28,30] and present calculations conclude that Mn(V)@O (5a) or Mn(IV)@O (5b) plays a crucial role in both native (1) and artificial (8) OEC systems.
where ni denotes the occupation number of a natural orbital /i, ranging from 0 to 2. The spin-polarized BS molecular orbitals ðw i Þ for the up-spin and down-spin states are derived by bonding (/i) and antibonding ð/i Þ natural orbitals as w i ¼ cos hi /i sin hi /i
ði ¼ 1; 2; . . . ; N Þ;
ð4Þ
where hi is the orbital mixing parameter and N is the number of bonding natural orbitals. The orbital overlap Ti between the up-spin and down-spin orbitals is defined as a measure of orbital splitting by T i ¼ hwþ i jwi i ¼ cos 2hi :
ð5Þ
Ti is unity for closed-shell systems (hi = 0) and 0 6 Ti < 1 for open-shell systems (0 < hi 6 p/4). The occupation numbers of the bonding and antibonding natural orbitals are expressed by the orbital overlap Ti as ni ¼ 1 þ T i ;
ni ¼ 1 T i :
ð6Þ
This means that contribution of doubly excited configura tion /i /i is significant because of small orbital-energy gap and strong electron repulsion (correlation). The diradical character y is defined with the weight (WD) of the contribution of doubly excited configuration [23–28] as 2T i y i ¼ 2W D ¼ 1 : ð7Þ 1 þ T 2i In the extreme case of BS solutions (hi = p/4, Ti = 0, and ni ¼ ni ¼ 1), the up- and down-spin orbitals are simply in- and out-of phase combinations of bonding and antibonding natural orbitals, respectively, as shown in Eq. (8), showing strong electron localizations at different fragments A and B 1 1 w ðwA wþ and wB w ð8Þ i ¼ pffiffiffi /i pffiffiffi /i i i Þ: 2 2 3. Results and discussion
2. Theoretical background and computational details 3.1. The nature of metal–oxo bonds in OEC Electronic structures of Mn–oxo model complexes of OEC and Mn–oxo porphyrine complex were investigated using the unrestricted B3LYP (UB3LYP) method [31,32] with the Huzinaga’s MIDI+F basis set (533(21)/53(21)/ (41)) [33] for Mn ion and the 6-31G* basis set [34] for other atoms [35]. The coordinates of model complexes of OEC were taken from the X-ray crystallographic structure in
The models 1, 2 and 3 with and without extra two waters are examined as the active site of 1 in OEC. As a continuation of previous work [30], we examine the high-valent Mn(V)@O cores with the ligand fields revealed by the X-ray diffraction method [1]. In the model 1, three waters and two CH3COO anions were employed as the ligands,
K. Yamaguchi et al. / Polyhedron 26 (2007) 2216–2224
Fig. 4. Computational model 1: [Mn(V)@O (CH3CO2)2 (H2O)3]+1 without (a) and with (b) extra 2H2O, model 2: [Mn(V)@O (CH3CO2)2(H2O)2(OHCa(OH)2)]0 without (c) and with (d) extra 2H2O, and model 3: [Mn(V)@O (CH3CO2)2(H2O)2(OHCa(OH)2)(H2O)]0 without (e) and with (f) extra 2H2O.
while one water in model 1 is replaced with the (OH)Ca(OH)2 anion in the model 2 as shown in Fig. 4. Further one water is added to the Ca(II) ion in model 3. As shown previously [24], the Mn(V)@O core has the socalled oxene structure (r)2(dpx–ppx)2(dpy–ppy)2 with one dr–pr and two dp–pp bonds. However, the dp–pp bonds are usually spin-polarized because of strong electron correlation, and the resulting magnetic orbitals (wi) in Eq. (4) are more or less localized on the Mn and O sites, respectively. Here, ligand field effects on the Mn–O bonding are examined by our methods described in Section 2. Table 1 summarizes spin densities (Mulliken charge) on Mn, O, and ligand obtained by the UB3LYP calculations. The negative spin densities are populated on the O-site, in accord with the diradical character (Æ›Mn–OÆfl) of the Mn@O bond. Interestingly, the negative spin densities also appear on the ligands, namely CH3COO ligands in model 1 and Ca(OH)2 part in models 2 and 3, respectively. This means that the charge transfer (CT) from ligands (L) to the dpy–ppy antibonding orbital is not negligible, showing a contribution of the [Æ›Mn(IV)@OL Æ+fl] structure. Thus, the situation in the Mn(V)@O bond is similar to that of the high-valent Fe(V)@O and Mn(V)@O cores in porphyrine complex: [Æ›Fe(IV)@OPor Æ+fl] and [Æ›Mn(IV)@OPor Æ+ fl].
2219
However, the CT from ligands to Mn(V)@O is a little suppressed by addition of two extra waters as shown in the model 1 with 2H2O. The diradical character of the dpx–ppx bond is also decreased with change of the ligand field. For example, coordination of water to the Ca(II) ion largely reduced the spin density on the O-atom of MnO. The CT diradical character is rather significant in the models 2 and 3 with extra 2H2O. This implies that the cubane unit CaMn3O4 (4) in 1 play important roles in regulation of the nature of chemical bonds of the Mn– oxo part in 1. The present results indicate that the electrophilic character of the high-valent Mn(V)@O bond should be enhanced with suppression of the CT biradical character with CaMn3O4 in 1. This entails a possibility of the SE2 mechanism instead of the 1O- and/or 3O-models for oxygen evolution from waters, though the latter(s) are rather conceivable from strong diradical character of the Mn@O bonds in models 1 and 2, which can be regarded as models for synthetic manganese–oxo complexes [12–16,29]. The natural orbital analysis of the broken-symmetry (BS) UB3LYP solutions for the six models in Fig. 4 have been performed to obtain the natural orbitals and their occupation numbers, which are also available by the symmetry-adapted (SA) CASSCF procedure. Table 2 summarizes the occupation numbers of bonding (antibonding) dr–pr and dpx–ppx orbitals, together with those of the ligand orbital (L) and dpy–ppy antibonding orbitals. The dr–pr orbitals are almost doubly occupied, showing the nonradical character. While, the occupation numbers of the antibonding dpx–ppx orbitals are 0.602 (model 1), 0.562 (model 1 + 2H2O), 0.831 (model 2), 0.423 (model 2 + 2H2O), 0.748 (model 3), and 0.336 (model 3 + 2H2O), respectively. This in turn means that the orbital overlaps (Ti) between the magnetic dpx–ppx orbitals ðw i Þ are 0.398, 0.438, 0.169, 0.577, 0.252, and 0.664, respectively. Thus the diradical character of the dpx–ppx bond is sensitive to the ligand fields. On the other hand, the orbital overlaps (Ti) between the magnetic CT (dpy–py) orbitals are 0.113, 0.324, 0.002, 0.171, 0.210, and 0.184, respectively, indicating the strong CT diradical character. This indicates that contribution of the [Mn(IV)@OL Æ+] structure is significant in the model complexes 1, 2, and 3. Judging from the occupation numbers in Table 2, the four active orbitals and four active electrons [4, 4] are at least crucial for the complete active space (CAS) for SA CASCI treatment of the models 1, 2, and 3. However, inclusion of the bonding and antibonding dr–pr orbitals
Table 1 Spin densities (Mulliken charge) of the model complexes 1, 2 and 3 by UB3LYP
Table 2 Occupation numbers of natural orbitals for models 1, 2 and 3 by UB3LYP
Models
Mn
Ligands
Models
r (r*)
p (p*)
Model Model Model Model Model Model
1.881 1.396 1.681 1.701 1.455 1.457
0.833 0.625 0.865 1.243 1.006 1.089
Model Model Model Model Model Model
1.986 1.984 1.971 1.928 1.977 1.920
1.398 1.438 1.121 1.577 1.252 1.664
1 1 (2H2O) 2 2 (2H2O) 3 3 (2H2O)
O (1.884) (1.942) (1.886) (1.878) (1.906) (1.900)
1.048 0.771 0.816 0.458 0.449 0.368
(0.509) (0.529) (0.665) (0.762) (0.751) (0.765)
(1.375) (1.413) (1.221) (1.116) (1.155) (1.135)
1 1 (2H2O) 2 2 (2H2O) 3 3 (2H2O)
(0.014) (0.016) (0.029) (0.072) (0.023) (0.080)
L (p^*) (0.602) (0.562) (0.831) (0.423) (0.748) (0.336)
1.183 1.324 1.002 1.171 1.210 1.184
(0.817) (0.676) (0.998) (0.829) (0.790) (0.816)
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as an example. These natural orbitals are utilized for successive SA computations of the complexes, 1, 2, and 3. The CASCI results will be published elsewhere. 3.2. Electronic structures of Mn–oxo porphyrine complex
Fig. 5. Graphic drawings of the bonding and antibonding pairs of dr– pr(r), dpx–ppx(p), and dpy–ppy(p) type natural orbitals of MnO in the model 1 with extra 2H2O (b in Fig. 4).
becomes essential for MO-theoretical tracing of the dissociation process of the Mn@O bond. The six natural orbitals for the model complex 1 with 2H2O are depicted in Fig. 5
Fig. 6. Potential curve of the Mn(V)@O porphyrine complex (7) with change of the Mn–O distance.
Here, a manganese–oxo porphyrin complex (8), [Mn(V)@OPor](H2O) is examined as an example of artificial high-valent manganese–oxo species. Fig. 6 shows variations of the potential curve of 8 with changing the Mn–O bond distance (R). At the dissociation limit (R = 1), 8 is regarded as the exchange-coupled low-spin (LS) state constructed of the triplet state of [Mn(III)Por](H2O) and triplet atomic oxygen (3O) as illustrated in Fig. 7. This characteristic property remains even at R 1. For example, the spin density (Mulliken charge) of Mn and porphy˚ , namely [Mn(III)Por](H2O) rine of 8 at R = 3.0 A fragment, are 2.57 (1.22) and 0.63 (0.38), respectively. Then the p-electron of porphyrine is spin-polarized because of the internal magnetic field of triplet Mn(III) ion. The net charge of Mn(III) is largely reduced by the coordination of porphyrine dianion. The oxygen site of 8 is regarded as triplet oxygen with negative spin density (1.94). These results are consistent with the triplet O (3O) model in Fig. 3. The Mn–O distance at the equilibrium geometry of 8 is ˚ and the binding energy is calculated to be 1.6 A 59.12 kcal/mol. The spin density (Mulliken charge) of Mn, O and porphyrine are 1.53 (1.42), 0.47 (0.43) and 1.06 (0.15), respectively. Judging from the orbital spin densities, the dpx–ppx covalent bond is considerably spin-polarized, namely [›dÆMn(0.47)–O(0.47)dÆfl] (where spin densities are given in parentheses), because of strong electron correlation. On the other hand, the charge transfer from the p-bonding closed-shell orbital of porphyrine to the dpy–ppy antibonding orbital of the MnO site occurs at the geometry, giving rise to the porphyrine p-cation radical, which is responsible for the CT biradical structure: [›ÆMn(IV)–O(1.06)PorÆ+(1.06)fl](H2O). This behavior is similar to that of the models 1, 2, and 3 for the Mn@O bond in OEC.
Fig. 7. (a) The exchange-coupled low-spin (singlet) state between triplet Mn(III) and triplet oxygen atom (3O) with the closed-shell porphyrine at a ˚ ) manganese–oxo porphyrine complex. (b) Schematic illustrations of the occupation numbers of natural orbitals for the charge dissociated (R = 3.0 A transfer (CT) diradical (singlet) state constructed of doublet Mn(IV)@O and doublet cation radical of porphyrine.
K. Yamaguchi et al. / Polyhedron 26 (2007) 2216–2224
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Fig. 8. Graphical drawings of the bonding (1 0 0) and antibonding (1 0 3) pairs of the dpy–ppy type natural orbital and those (1 0 1 and 1 0 2) of the CT type orbitals, which are constructed of the porphyrine p- and dpy–ppy antibonding orbitals. The CT diradical property is variable with Mn–O distance.
The natural orbital analysis of the broken-symmetry (BS) UB3LYP solution of 8 at the equilibrium geometry has been performed to elucidate symmetry-adapted (SA) CASSCF picture. Figs. 7 and 8 illustrate, respectively, populations of occupation numbers and shapes of natural orbitals. From Fig. 8, the natural orbitals (/i) 1 0 1 and 1 0 2 are delocalized over both Mn@O and porphyrine groups, and their occupation numbers are almost 1.0. Then the magnetic orbitals ðw i Þ given by the mixing of them are localized on the Mn@O group ðwþ i ¼ wA Þ and porphyrine group ðw ¼ w Þ, respectively, leading to the singlet biradB i ical configuration. On the other hand, the natural orbitals 1 0 0 and 1 0 3 are the bonding and antibonding dpx–ppx orbitals. The occupation number of the antibonding orbital is 0.23, indicating a homolytic diradical character. However, this small number does not suppress significantly the electron accepting property of this LUMO. This is compatible with the electrophilic property of MnO. Thus the high-valent Mn–O bond in porphyrine complex exhibits similar characteristic to that of the model complexes 1 and 2 for OEC in Fig. 4. 4. Possible mechanisms of oxygen evolution 4.1. Importance of the Mn(V)@O bond Past two decades [22–28], Yamaguchi et al. elucidated electronic structures and spin states of transition-metal oxides on the basis of ab initio broken-symmetry (BS) (UHF UDFT, GHF and GDFT) calculations followed by the approximate spin projection. It was found that the oxygen atom in the metal-oxo species MO (M = Cr, Mn, Fe) exhibits the nucleophilic character M+O in the case of the lower-valent stage of M+; M(II) and Mn(III). For example, the Mn(III) ion forms an ionic bond with hydroxide anion, [Mn(III)–OH]2+, as shown in Fig. 2. On the other hand, the oxygen atom in the high-valent metaloxo species such as Mn(V)@O may have singlet or triplet oxygen atom (O) character, showing an electrophilic property to many substrates as illustrated in Fig. 3, for example: MnðVÞ@O þ OH ! MnðIVÞAOOH
ð9aÞ
MnðVÞ@O þ HAOH ! MnðIVÞAOH þ OH MnðVÞ@O þ HAOH ! MnðIIIÞ þ HOOH
ð9bÞ ð9cÞ
The reaction (9a) may be operative in ion reactions to generate the O–O bond. The hydrogen abstraction from water by Mn(V)@O in (9b) is also conceivable for high-spin
states of manganese–oxo species, though the insertion (or very fast rebound mechanism) is more reasonable in the low-spin (LS) state of them (in Eq. (9c)). Isobe et al. [28] have performed the DFT calculations of the model compound (6) for the Limburg compound (7). They have found that the metal–oxo bonds (Mn(V)@O) in 6 show the diradical character ÆMn–OÆ (see Fig. 2), and therefore the oxygen atom in Mn(V)@O in 7 may undergo electrophilic reactions with substrates in Eq. (9): note that singlet biradical character of the low-spin (LS) Mn(V)@O bond decrease significantly in the case of insertion-type reaction in Fig. 3. Several evidence [29] suggests that chloride anion plays an important role for oxygen evolution in Limburg reaction systems (7) like native OEC (1) in Fig. 1. This implies that SE2-like mechanism is also conceivable as discussed later (see Fig. 10). Koizumi et al. [35] have carried out the DFT calculations of dimer of manganese–oxo (MnO) porphyrin (PO) synthesized and characterized by Naruta’s group [36]. They have investigated variations of the electronic structures of POMn(X)@O with the change of oxidation number (X) of the Mn ion. It was found that the Mn(V)@O bond in Naruta’s oxygen evolution system has the oxygen-diradical character, which may entail the oxygen-atom radical coupling as follows: ðPOMnðVÞ@OÞ2 ! POMnðIVÞAOAOAMnðIVÞPO ! ðPOMnðIIIÞÞ2 þ O2
ð9dÞ
However, more complex mechanisms involving ionic processes are conceivable even in this case. For example, Fig. 9a illustrates the radical coupling mechanism for the formation of molecular oxygen in Eq. (9d), which is theoretically feasible because of the biradical nature of the Mn@O bond as shown in Figs. 7 and 8. On the other hand, strong electrophilic nature of the high-valent [Mn(V)@O+ Por] and/or [Mn(IV)@O Por Æ+] bonds indicates a possibility of the ionic (SE2) process [24] in Fig. 9b, where electrophilic attack of the oxygen of MnO to the lone pair of water is a key step for the O–O bond formation in oxygen evolution. Thus our theoretical studies on native OEC and artificial OEC [28,30,35] systems have revealed the crucial role of the high-valent Mn(V)@O and/or Mn(IV)@O bonds. 4.2. SE2 mechanism of oxygen evolution The present computational results indicate that the insertion (or rapid rebound) mechanism, 1O-model [24], is
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K. Yamaguchi et al. / Polyhedron 26 (2007) 2216–2224
Fig. 9. (a) Radical coupling mechanism of the O–O bond formation in the artificial OEC system and (b) ionic (SE2) mechanism of the O–O bond formation. The latter mechanism is closely related to that of OEC in Fig. 10.
applicable to the oxygenation by high-valent Mn–oxo species examined here because of strong diradical characters. However, the diradical character of the Mn–O bond is found to be sensitive to environmental effects such as hydrogen bonding and clustering of waters (see Tables 1 and 2). This in turn indicates that the nature of Mn@O bonds in 1 is variable depending on the electronic states of the cubane unit CaMn3O4. Therefore, three mechanisms in Fig. 3 are conceivable theoretically. Present computational results indicate a possibility of our previous bimolecular electrophilic substitution (SE2) mechanism (see Fig. 3) for oxygen evolution reaction in OEC as illustrated in Fig. 10. From Fig. 10, the oxygen site of the high valent manganese–oxo bonds [Mn(V)@O+ 4] and/or [Mn(IV)@O 4 Æ+] in OEC undergoes the electrophilic attack of lone pair of water molecule, followed by the concerted proton migration with base (for example hydrogen-bonding networks involving protein side chains within local environment). This SE2 reaction produces the Mn(IV)–hydroperoxide anion complex, which undergoes second proton migration to afford the low-spin
Mn(IV)–superoxide anion complex. The regulation of charge on O2 fragment by CaMn3O4 (4)part is feasible in the case of 1. The back electron transfer from superoxide anion to Mn(IV) generates triplet molecular oxygen and triplet Mn(III) complex as follows: 1
1 3 3 3 3 ½MnðIVÞO 2 ! ½ MnðIIIÞ O2 ! MnðIIIÞ þ O2
ð9eÞ
3
It is noteworthy that O2 is generated without spin inversion via spin–orbit interaction. The key point of the SE2 mechanism is the electrophilic nature of oxygen site in the high-valent manganese–oxo bonds [24]. The SE2 mechanism in Fig. 10 is consistent with the proposal by Iwata and Barber on the experimental ground [37,38]. The reaction scheme in Fig. 10 is now under further investigation in our laboratory. 4.3. Implications to related oxygenation reactions Finally, implications of the previous [24–28] and present computational results are briefly discussed in relation to other oxygenation reactions by metal–oxo species. For
Fig. 10. Possibility of the bimolecular electrophic substitution (SE2) mechanism of oxygen evolution reaction from water in OEC of the photosynthesis II. The SE2 mechanism is a direct extension of that in Fig. 3 (see text). It does not entail the formation of hydroxyl radical as in the case of the 3O-model.
K. Yamaguchi et al. / Polyhedron 26 (2007) 2216–2224
example, the conversion of methane to methanol is catalyzed at the active site of a metalloenzyme known as methane monooxygenase (MMO) (Mn ions in 6 and 7 are replaced with Fe ions in MMO) CH4 þ NADH þ Hþ þ O2 ! CH3 OH þ NADþ þ H2 O
2223
Table 3 Classifications of the reaction mechanisms of methane monooxygenation by several theoretical groups Our proposalsa
Recent computational results
SE2 model O-model
Yoshizawa (concerted) modelb Friesner–Lippard (bound-radical) modelc Morokuma–Basch (hydrogen abstraction) modeld Siegbahn (hydrogen abstraction) modele
ð10Þ
1
Both cationic and radical intermediates (or transition structures) have been proposed for this reaction on the experimental grounds [39]. Past decade, several computations have been performed to elucidate the nature of the intermediate in MMO. According to our previous proposal [24], computational results on the iron–oxo (Fe(IV)@O) species in MMO are classified into three categories illustrated in Fig. 3. Yoshizawa et al. [40,41] have proposed a concerted (fourcentered) mechanism between Fe@O and H–CH3 fragments on the basis of the spin-restricted (RHF) calculations. Their mechanism is similar to the SE2 (concerted) mechanism in Fig. 3, though our SE2 mechanism is based on the high-spin configuration of the Fe(IV) center instead of their closedshell (RHF) configuration. On the other hand, Basch, Morokuma and co-workers [42,43] have been proposed a hydrogen-abstraction mechanism for hydroxylation reaction by MMO, assuming the four unpaired spins at each Fe(IV) center of Q (namely the high-spin 9A dimer) in the spin-unrestricted DFT (UDFT) calculations. The hydrogen-abstraction mechanism in the 9A dimer model is similar to the 3O (abstraction)-model in Fig. 3 since the reaction site is regarded as the 3O plus H–CH3 system. Siegbahn et al. [44,45] have proposed a hydrogen abstraction model in the high-spin mixed-valence (MV) state: Q = [Fe(II)(S = 5/2) Fe(IV)(S = 2/2)O-radical]. Siegbahn model is regarded as a high-spin (3O) model in our terminology (Fig. 3) [24]. Friesner, Lippard and their co-workers [46,47] proposed a bound-radical pair model, assuming the low-spin (antiferromagnetic) dimer state of the high-spin iron (Fe(IV)) centers. Friesner–Lippard model is similar to the 1O (insertion)model, where both insertion and rapid recombination between the singlet radical pair (ÆOH plus ÆCH3) are feasible, depending on the reaction conditions [24,26]. Table 3 summarizes the proposed reaction mechanisms of methane monooxygenation (MMO) by several theoretical groups. The conclusions are dependent on the assumed anti (AF) and ferro (F) magnetic spin couplings of the iron oxo cores (Fe2O2) in MMO. However, the low-spin (LS) AF broken-symmetry usually involves the high-spin (HS) component. Therefore use of an approximate spin projected (AP) BS solution [23–28] is desirable for location of transition structure on the pure LS surface. This situation clearly indicates necessity of further theoretical investigations based on more realistic reaction-site and spin-state models including protein environments. Both radical and ionic mechanisms are also proposed for hydroxylation reactions of P450 with the active site: [Fe(IV)@OÆPorÆ+] [48]. The situation is quite similar to those of MMO and OEC in the photosynthesis II system.
3
O-model
a b c d e
Refs. Refs. Refs. Refs. Refs.
Methods RHF UDFT
1
9
A by UDFT
high spin MV by UDFT
[24,26]. [40,41]. [46,47]. [42,43]. [44,45].
This in turn indicates that theoretical and computational efforts may provide a unified picture and key concepts for understanding of oxygenation reactions in general [24,26]. 5. Concluding remarks The nature of high-valent manganese–oxo (Mn(V)@O) bonds has been investigated on the basis of the hybrid DFT calculations of the model complexes 1, 2, and 3 for oxygen evolution center (OEC) and the Mn–oxo prophyrine complex (8). It is found that charge transfer from ligands to Mn(V)@O occur to indicate significant contribution of the [Mn(IV)@O L Æ+] configuration. Therefore the high-valent (HV) Mn–O bond is regarded as the superposed state of these two configurations in general, WðMnðHVÞ@OÞ ¼ C 1 W1 ðMnðVÞ@O LÞ þ C 2 W2 ðMnðIVÞ@O Lþ Þ;
ð11Þ
where Ci denotes the mixing coefficients, which are variable with ligands and environmental effects as shown in this paper. The dual character of the HV Mn–O bond would be a key factor for theoretical understanding of complex behaviors of chemical reactions by HV Mn–O compounds. Similar situations are also found in HV iron–oxo species in MMO and P450. The hybrid DFT (HDFT) followed by the natural orbital analysis is a useful and practical method for theoretical investigations of metalloenzymes as shown in this series of papers [49]. Acknowledgement This work has been supported by a Grant-in-Aid for Scientific Research on Priority Areas (Nos. 18350008 and 18205023) from Ministry of Education, Science, Sports and Culture, Japan. References [1] K.N. Ferreira, T.M. Iversion, K. Maghlaoui, J. Barber, S. Iwata, Science 303 (2004) 1831. [2] B. Kok, B. Forbush, M. McGloin, Photochem. Photobiol. 11 (1970) 457.
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[15]
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Theory of chemical bonds in metalloenzymes VI: Manganese–oxo bonds in the photosynthesis II system K. Yamaguchi *, S. Yamanaka, H. Isobe, M. Shoji, K. Koizumi, Y. Kitagawa, T. Kawakami, M. Okumura Department of Chemistry, Graduate School of Science, Osaka University, Toyonaka, Osaka 560-0043, Japan Received 23 October 2006; accepted 24 October 2006 Available online 9 December 2006
Abstract Electronic and spin structures of high-valent manganese–oxo bonds in the photosynthesis II system (oxygen evolving center, OEC) are investigated by the use of spin polarized hybrid DFT (HDFT) method. Theoretical calculations of a high-valent manganese–oxo porphyrin complex are also performed to elucidate common characteristic of the active Mn@O bonds in both native OEC and artificial systems. The oxygen site of the high-valent Mn@O is found to be electrophilic in nature, in accord with our previous work, where the SE2, 1 O- and 3O-models have been presented for theoretical understanding of complex behaviors of oxygenation reactions by metal–oxo species. The 1O- and 3O-models are applicable to model complexes examined here, since the manganese–oxo bonds exhibit strong biradical character. Possibility of the SE2-like transition structure model for OEC is also discussed on both the theoretical and experimental grounds. Implications of present computational results are discussed in relation to hydroxylation reaction by MMO and P450. 2006 Elsevier Ltd. All rights reserved. Keywords: Manganese–oxo bond; Photosynthesis II; Oxygen evolution; SE2 reaction; B3LYP
1. Introduction Most of the oxygen in the atmosphere is generated by plants, algae and cyanobacteria by the photoinduced oxidation of water to dioxygen [1]: 2H2 O ! O2 þ 4Hþ þ 4e
ð1Þ
The oxygen-evolving center (OEC) of the photosynthesis (PS) II system, that catalyzes the reaction in Eq. (1), has been found to contain a cluster of four Mn atoms, calcium ion and chloride anions. Recently, Ferreira et al. [1] have reported the X-ray structure of OEC in PS II of cyanobac˚ resoluterium (Thermosynechococcus elongatus) at 3.5 A tion. Their X-ray data show that the OEC contains a cubane-like CaMn3O4 (1) cluster linked to a fourth Mn by a mono-l oxo bridge with the surrounding coordination *
Corresponding author. Tel.: +81 6 68505404; fax: +81 6 68505550. E-mail address: [email protected] (K. Yamaguchi).
0277-5387/$ - see front matter 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.poly.2006.10.054
sphere as illustrated in Fig. 1. The currently accepted model of photosynthetic water oxidation involves five intermediate states from S0 through S1, S2 and S3 to S4 (the so-called Kok mechanism) [2]. The tetranuclear Mn complex in the OEC (1) is thought to couple the four-electron oxidation of water in Eq. (1) with the cyclic one-electron photochemistry (totally 4-electron transfers), namely S0 ! S1 ! S2 ! S3 ! S4 ! S0 (Kok cycle), in PS II. P680 and tyrosyl groups play important roles for these electron-transfer processes. A lot of experimental studies on the Mn OEC in PS II have been carried out to elucidate mechanisms of oxygen evolution from water [1,2]. Many review articles [3–11] have already been published to elucidate them on the basis of accumulated results. The experimental studies of several Mn model complexes have also been carried out extensively [12–16]. Several theoretical studies on the Mn complexes have been carried out to elucidate the electronic structures of Mn OEC [17,18]. The LCAO Xa calculation of the
K. Yamaguchi et al. / Polyhedron 26 (2007) 2216–2224
2217
Fig. 1. CaMn4O5 cluster (1) in the photosynthesis II and related cubane Mn4O4 (2), triangular Mn3O4 (3), and cubane CaMn3 (4) clusters. 2 and 3 exhibit the tetrahedral and triangular (antiferromagnetic) spin alignments, respectively, at the low-spin state.
tetranuclear manganese complex Mn(IV)Mn(III)3Cl7(O2CCCH3)3]3, a cubane complex, has been carried out to elucidate its electronic and spin states [16]. Belinskii [18] has carried out the theoretical studies on the mixed-valence Mn(III)3Mn(IV) and Mn(IV)3Mn(III) clusters on the basis of the quantum Heisenberg models, assuming trapezoid, butterfly, bent, T-type and distorted tetrahedron structures. Possible ground spin states for these five structures have been elucidated, changing effective exchange interactions between manganese ions. We have examined possible spin structures of tetranuclear (2) [19] and trinuclear (3,4) [20] manganese clusters in Fig. 1 on the basis of the spin vector model [21]. The strong spin frustration [15] in 3 and 4 [20] has provided non-collinear spin structures such as triangular spin structure in Fig. 1, on the assumption of the experimentally determined effective exchange integrals (Jij). The Jij values for the binuclear manganese complexes [22,23] have been calculated using the hybrid DFT method to elucidate the mechanisms for effective exchange interactions between Mn ions [24] LS
J ij ¼
EðXÞ HS EðXÞ ; HS h b S 2 iðXÞ LS h b S 2 iðXÞ
ð2Þ
S 2 iðXÞ are the total energy and total where YE(X) and Y h b angular momentum for the state Y(= LS; the lowest spin state, HS; the highest spin state) by the method X (= UHF, UMPn, UDFT, etc.). It was shown that the sign of Jij is negative because of the greater stability of LS than HS, and the magnitude of Jij values is variable with the oxidation numbers of Mn ion. The calculated Jij values have been consistent with the experiments available. Very
recently, Yamanaka et al. [25] have performed the DFT calculation of cubane-type Mn(II)4 cluster (2) using the general spin orbitals (GSO), namely, two component spinor. The resulted spin structure of 2 was consistent with the tetrahedral type in Fig. 1. The variations of charge and spin populations of manganese oxo (MnO) bonds with the oxidation number of Mn ion were also examined by the unrestricted Hartree– Fock (UHF) method [24]. It was concluded that the nature of oxygen atom in the manganese oxo bond (X = O in 5) varies from nucleophilic to electrophilic with the change of formal charge of Mn ion from low (II) to high (V) valent as illustrated in Fig. 2. The oxygen atom in the Mn(V)O core exhibited the radical character responsible for the radical reactivity for water [24–28]. These results enabled us to propose three possible models of oxygenation reactions of substrates by metal–oxo species: (1) SE2 model, (2) 1Omodel and (3) 3O-model as shown in Fig. 3 [25,26]: note that singlet and triplet states of atomic oxygen undergoes, respectively, insertion and abstraction reactions with X–H bonds (X = CH3, OH, etc.). Similar situations are expected for low-spin (LS) and high-spin (HS) metal-oxo species. As a first step toward theoretical approaches to water oxidation in OEC, Isobe et al. [28] have performed the DFT calculation of the model compound XH3Mn(IV)O2Mn(IV)H3Y (X,Y = O, H) (6) for the Limburg compound [(terpy)(H2O)Mn(l-O) 2Mn(terpy)(H2O)]3+ (7) [29] as shown in Fig. 2. It was found that electron correlation plays a crucial role to determine the nature of manganese–oxygen bonds in 7. Diradical or nonradical mechanism is found to be feasible for the oxygen atom transfer from water to high-valent manganese–oxo bond Mn(V)@O
Fig. 2. Variations of electronic structures of the manganese–oxo bond (5), and Mn–oxo model complexes (6, 7, and 8) for oxygen evolution center (OEC).
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K. Yamaguchi et al. / Polyhedron 26 (2007) 2216–2224
Protein Data Bank (PDB code 1S5L) [1]. All calculations were performed with the Gaussian 98 program package [34]. To obtain the symmetry-adapted (SA) picture for the broken-symmetry (BS) UB3LYP calculations, we have used the natural orbitals, which are determined by diagonalizing their spin-traced first-order density matrices c [23–28] as X ni /i ðrÞ/i ðr0 Þ; ð3Þ cðr; r0 Þ ¼ i
Fig. 3. SE2, 1O- and 3O-models for oxygenation reactions of X–H (X = CH3, OH, etc.), bonds and expoxidation reactions of C–C double bonds in Refs. [24,28]. The discrete radicals are generated in the 3O-model, though such species are hardly detectable in the 1O-model because of rapid recombination (or insertion).
in 7. The environmental effects such as solvent are considered to play an important role for control of the mechanism. The electronic and spin structure of the CaMn3O4 cluster 4 in 1 have been elucidated on the basis of both classical (spin vector) and quantum Heisenberg models [30]. The GSO DFT calculations of the cluster 4 were also performed to elucidate charge and spin populations and noncollinear spin structure (see 4 in Fig. 1). Possible reaction mechanisms of 1 have been proposed on the theoretical and experimental grounds [30]. However, the detailed computations of the metal–oxo part in 1 have not been performed yet. As a continuation of previous work [24–28,30], we here perform theoretical studies on the high-valent Mn–O bonds in OEC and porphyrin model complexes 8. The electronic structures of these species are investigated from the viewpoint of charge and spin populations, and diradical character. The strong diradical character of the Mn(V)@O bonds in the model complexes is consistent with the 1Oand/or 3O-models for oxygenations of X–H bonds. The SE2 mechanism in Fig. 3 is also examined as a possible model of the transition state of the O–O bond formation process. Implications of the calculated results are discussed in relation to possible mechanisms of oxygen evolution in OEC. Our previous [22–28,30] and present calculations conclude that Mn(V)@O (5a) or Mn(IV)@O (5b) plays a crucial role in both native (1) and artificial (8) OEC systems.
where ni denotes the occupation number of a natural orbital /i, ranging from 0 to 2. The spin-polarized BS molecular orbitals ðw i Þ for the up-spin and down-spin states are derived by bonding (/i) and antibonding ð/i Þ natural orbitals as w i ¼ cos hi /i sin hi /i
ði ¼ 1; 2; . . . ; N Þ;
ð4Þ
where hi is the orbital mixing parameter and N is the number of bonding natural orbitals. The orbital overlap Ti between the up-spin and down-spin orbitals is defined as a measure of orbital splitting by T i ¼ hwþ i jwi i ¼ cos 2hi :
ð5Þ
Ti is unity for closed-shell systems (hi = 0) and 0 6 Ti < 1 for open-shell systems (0 < hi 6 p/4). The occupation numbers of the bonding and antibonding natural orbitals are expressed by the orbital overlap Ti as ni ¼ 1 þ T i ;
ni ¼ 1 T i :
ð6Þ
This means that contribution of doubly excited configura tion /i /i is significant because of small orbital-energy gap and strong electron repulsion (correlation). The diradical character y is defined with the weight (WD) of the contribution of doubly excited configuration [23–28] as 2T i y i ¼ 2W D ¼ 1 : ð7Þ 1 þ T 2i In the extreme case of BS solutions (hi = p/4, Ti = 0, and ni ¼ ni ¼ 1), the up- and down-spin orbitals are simply in- and out-of phase combinations of bonding and antibonding natural orbitals, respectively, as shown in Eq. (8), showing strong electron localizations at different fragments A and B 1 1 w ðwA wþ and wB w ð8Þ i ¼ pffiffiffi /i pffiffiffi /i i i Þ: 2 2 3. Results and discussion
2. Theoretical background and computational details 3.1. The nature of metal–oxo bonds in OEC Electronic structures of Mn–oxo model complexes of OEC and Mn–oxo porphyrine complex were investigated using the unrestricted B3LYP (UB3LYP) method [31,32] with the Huzinaga’s MIDI+F basis set (533(21)/53(21)/ (41)) [33] for Mn ion and the 6-31G* basis set [34] for other atoms [35]. The coordinates of model complexes of OEC were taken from the X-ray crystallographic structure in
The models 1, 2 and 3 with and without extra two waters are examined as the active site of 1 in OEC. As a continuation of previous work [30], we examine the high-valent Mn(V)@O cores with the ligand fields revealed by the X-ray diffraction method [1]. In the model 1, three waters and two CH3COO anions were employed as the ligands,
K. Yamaguchi et al. / Polyhedron 26 (2007) 2216–2224
Fig. 4. Computational model 1: [Mn(V)@O (CH3CO2)2 (H2O)3]+1 without (a) and with (b) extra 2H2O, model 2: [Mn(V)@O (CH3CO2)2(H2O)2(OHCa(OH)2)]0 without (c) and with (d) extra 2H2O, and model 3: [Mn(V)@O (CH3CO2)2(H2O)2(OHCa(OH)2)(H2O)]0 without (e) and with (f) extra 2H2O.
while one water in model 1 is replaced with the (OH)Ca(OH)2 anion in the model 2 as shown in Fig. 4. Further one water is added to the Ca(II) ion in model 3. As shown previously [24], the Mn(V)@O core has the socalled oxene structure (r)2(dpx–ppx)2(dpy–ppy)2 with one dr–pr and two dp–pp bonds. However, the dp–pp bonds are usually spin-polarized because of strong electron correlation, and the resulting magnetic orbitals (wi) in Eq. (4) are more or less localized on the Mn and O sites, respectively. Here, ligand field effects on the Mn–O bonding are examined by our methods described in Section 2. Table 1 summarizes spin densities (Mulliken charge) on Mn, O, and ligand obtained by the UB3LYP calculations. The negative spin densities are populated on the O-site, in accord with the diradical character (Æ›Mn–OÆfl) of the Mn@O bond. Interestingly, the negative spin densities also appear on the ligands, namely CH3COO ligands in model 1 and Ca(OH)2 part in models 2 and 3, respectively. This means that the charge transfer (CT) from ligands (L) to the dpy–ppy antibonding orbital is not negligible, showing a contribution of the [Æ›Mn(IV)@OL Æ+fl] structure. Thus, the situation in the Mn(V)@O bond is similar to that of the high-valent Fe(V)@O and Mn(V)@O cores in porphyrine complex: [Æ›Fe(IV)@OPor Æ+fl] and [Æ›Mn(IV)@OPor Æ+ fl].
2219
However, the CT from ligands to Mn(V)@O is a little suppressed by addition of two extra waters as shown in the model 1 with 2H2O. The diradical character of the dpx–ppx bond is also decreased with change of the ligand field. For example, coordination of water to the Ca(II) ion largely reduced the spin density on the O-atom of MnO. The CT diradical character is rather significant in the models 2 and 3 with extra 2H2O. This implies that the cubane unit CaMn3O4 (4) in 1 play important roles in regulation of the nature of chemical bonds of the Mn– oxo part in 1. The present results indicate that the electrophilic character of the high-valent Mn(V)@O bond should be enhanced with suppression of the CT biradical character with CaMn3O4 in 1. This entails a possibility of the SE2 mechanism instead of the 1O- and/or 3O-models for oxygen evolution from waters, though the latter(s) are rather conceivable from strong diradical character of the Mn@O bonds in models 1 and 2, which can be regarded as models for synthetic manganese–oxo complexes [12–16,29]. The natural orbital analysis of the broken-symmetry (BS) UB3LYP solutions for the six models in Fig. 4 have been performed to obtain the natural orbitals and their occupation numbers, which are also available by the symmetry-adapted (SA) CASSCF procedure. Table 2 summarizes the occupation numbers of bonding (antibonding) dr–pr and dpx–ppx orbitals, together with those of the ligand orbital (L) and dpy–ppy antibonding orbitals. The dr–pr orbitals are almost doubly occupied, showing the nonradical character. While, the occupation numbers of the antibonding dpx–ppx orbitals are 0.602 (model 1), 0.562 (model 1 + 2H2O), 0.831 (model 2), 0.423 (model 2 + 2H2O), 0.748 (model 3), and 0.336 (model 3 + 2H2O), respectively. This in turn means that the orbital overlaps (Ti) between the magnetic dpx–ppx orbitals ðw i Þ are 0.398, 0.438, 0.169, 0.577, 0.252, and 0.664, respectively. Thus the diradical character of the dpx–ppx bond is sensitive to the ligand fields. On the other hand, the orbital overlaps (Ti) between the magnetic CT (dpy–py) orbitals are 0.113, 0.324, 0.002, 0.171, 0.210, and 0.184, respectively, indicating the strong CT diradical character. This indicates that contribution of the [Mn(IV)@OL Æ+] structure is significant in the model complexes 1, 2, and 3. Judging from the occupation numbers in Table 2, the four active orbitals and four active electrons [4, 4] are at least crucial for the complete active space (CAS) for SA CASCI treatment of the models 1, 2, and 3. However, inclusion of the bonding and antibonding dr–pr orbitals
Table 1 Spin densities (Mulliken charge) of the model complexes 1, 2 and 3 by UB3LYP
Table 2 Occupation numbers of natural orbitals for models 1, 2 and 3 by UB3LYP
Models
Mn
Ligands
Models
r (r*)
p (p*)
Model Model Model Model Model Model
1.881 1.396 1.681 1.701 1.455 1.457
0.833 0.625 0.865 1.243 1.006 1.089
Model Model Model Model Model Model
1.986 1.984 1.971 1.928 1.977 1.920
1.398 1.438 1.121 1.577 1.252 1.664
1 1 (2H2O) 2 2 (2H2O) 3 3 (2H2O)
O (1.884) (1.942) (1.886) (1.878) (1.906) (1.900)
1.048 0.771 0.816 0.458 0.449 0.368
(0.509) (0.529) (0.665) (0.762) (0.751) (0.765)
(1.375) (1.413) (1.221) (1.116) (1.155) (1.135)
1 1 (2H2O) 2 2 (2H2O) 3 3 (2H2O)
(0.014) (0.016) (0.029) (0.072) (0.023) (0.080)
L (p^*) (0.602) (0.562) (0.831) (0.423) (0.748) (0.336)
1.183 1.324 1.002 1.171 1.210 1.184
(0.817) (0.676) (0.998) (0.829) (0.790) (0.816)
2220
K. Yamaguchi et al. / Polyhedron 26 (2007) 2216–2224
as an example. These natural orbitals are utilized for successive SA computations of the complexes, 1, 2, and 3. The CASCI results will be published elsewhere. 3.2. Electronic structures of Mn–oxo porphyrine complex
Fig. 5. Graphic drawings of the bonding and antibonding pairs of dr– pr(r), dpx–ppx(p), and dpy–ppy(p) type natural orbitals of MnO in the model 1 with extra 2H2O (b in Fig. 4).
becomes essential for MO-theoretical tracing of the dissociation process of the Mn@O bond. The six natural orbitals for the model complex 1 with 2H2O are depicted in Fig. 5
Fig. 6. Potential curve of the Mn(V)@O porphyrine complex (7) with change of the Mn–O distance.
Here, a manganese–oxo porphyrin complex (8), [Mn(V)@OPor](H2O) is examined as an example of artificial high-valent manganese–oxo species. Fig. 6 shows variations of the potential curve of 8 with changing the Mn–O bond distance (R). At the dissociation limit (R = 1), 8 is regarded as the exchange-coupled low-spin (LS) state constructed of the triplet state of [Mn(III)Por](H2O) and triplet atomic oxygen (3O) as illustrated in Fig. 7. This characteristic property remains even at R 1. For example, the spin density (Mulliken charge) of Mn and porphy˚ , namely [Mn(III)Por](H2O) rine of 8 at R = 3.0 A fragment, are 2.57 (1.22) and 0.63 (0.38), respectively. Then the p-electron of porphyrine is spin-polarized because of the internal magnetic field of triplet Mn(III) ion. The net charge of Mn(III) is largely reduced by the coordination of porphyrine dianion. The oxygen site of 8 is regarded as triplet oxygen with negative spin density (1.94). These results are consistent with the triplet O (3O) model in Fig. 3. The Mn–O distance at the equilibrium geometry of 8 is ˚ and the binding energy is calculated to be 1.6 A 59.12 kcal/mol. The spin density (Mulliken charge) of Mn, O and porphyrine are 1.53 (1.42), 0.47 (0.43) and 1.06 (0.15), respectively. Judging from the orbital spin densities, the dpx–ppx covalent bond is considerably spin-polarized, namely [›dÆMn(0.47)–O(0.47)dÆfl] (where spin densities are given in parentheses), because of strong electron correlation. On the other hand, the charge transfer from the p-bonding closed-shell orbital of porphyrine to the dpy–ppy antibonding orbital of the MnO site occurs at the geometry, giving rise to the porphyrine p-cation radical, which is responsible for the CT biradical structure: [›ÆMn(IV)–O(1.06)PorÆ+(1.06)fl](H2O). This behavior is similar to that of the models 1, 2, and 3 for the Mn@O bond in OEC.
Fig. 7. (a) The exchange-coupled low-spin (singlet) state between triplet Mn(III) and triplet oxygen atom (3O) with the closed-shell porphyrine at a ˚ ) manganese–oxo porphyrine complex. (b) Schematic illustrations of the occupation numbers of natural orbitals for the charge dissociated (R = 3.0 A transfer (CT) diradical (singlet) state constructed of doublet Mn(IV)@O and doublet cation radical of porphyrine.
K. Yamaguchi et al. / Polyhedron 26 (2007) 2216–2224
2221
Fig. 8. Graphical drawings of the bonding (1 0 0) and antibonding (1 0 3) pairs of the dpy–ppy type natural orbital and those (1 0 1 and 1 0 2) of the CT type orbitals, which are constructed of the porphyrine p- and dpy–ppy antibonding orbitals. The CT diradical property is variable with Mn–O distance.
The natural orbital analysis of the broken-symmetry (BS) UB3LYP solution of 8 at the equilibrium geometry has been performed to elucidate symmetry-adapted (SA) CASSCF picture. Figs. 7 and 8 illustrate, respectively, populations of occupation numbers and shapes of natural orbitals. From Fig. 8, the natural orbitals (/i) 1 0 1 and 1 0 2 are delocalized over both Mn@O and porphyrine groups, and their occupation numbers are almost 1.0. Then the magnetic orbitals ðw i Þ given by the mixing of them are localized on the Mn@O group ðwþ i ¼ wA Þ and porphyrine group ðw ¼ w Þ, respectively, leading to the singlet biradB i ical configuration. On the other hand, the natural orbitals 1 0 0 and 1 0 3 are the bonding and antibonding dpx–ppx orbitals. The occupation number of the antibonding orbital is 0.23, indicating a homolytic diradical character. However, this small number does not suppress significantly the electron accepting property of this LUMO. This is compatible with the electrophilic property of MnO. Thus the high-valent Mn–O bond in porphyrine complex exhibits similar characteristic to that of the model complexes 1 and 2 for OEC in Fig. 4. 4. Possible mechanisms of oxygen evolution 4.1. Importance of the Mn(V)@O bond Past two decades [22–28], Yamaguchi et al. elucidated electronic structures and spin states of transition-metal oxides on the basis of ab initio broken-symmetry (BS) (UHF UDFT, GHF and GDFT) calculations followed by the approximate spin projection. It was found that the oxygen atom in the metal-oxo species MO (M = Cr, Mn, Fe) exhibits the nucleophilic character M+O in the case of the lower-valent stage of M+; M(II) and Mn(III). For example, the Mn(III) ion forms an ionic bond with hydroxide anion, [Mn(III)–OH]2+, as shown in Fig. 2. On the other hand, the oxygen atom in the high-valent metaloxo species such as Mn(V)@O may have singlet or triplet oxygen atom (O) character, showing an electrophilic property to many substrates as illustrated in Fig. 3, for example: MnðVÞ@O þ OH ! MnðIVÞAOOH
ð9aÞ
MnðVÞ@O þ HAOH ! MnðIVÞAOH þ OH MnðVÞ@O þ HAOH ! MnðIIIÞ þ HOOH
ð9bÞ ð9cÞ
The reaction (9a) may be operative in ion reactions to generate the O–O bond. The hydrogen abstraction from water by Mn(V)@O in (9b) is also conceivable for high-spin
states of manganese–oxo species, though the insertion (or very fast rebound mechanism) is more reasonable in the low-spin (LS) state of them (in Eq. (9c)). Isobe et al. [28] have performed the DFT calculations of the model compound (6) for the Limburg compound (7). They have found that the metal–oxo bonds (Mn(V)@O) in 6 show the diradical character ÆMn–OÆ (see Fig. 2), and therefore the oxygen atom in Mn(V)@O in 7 may undergo electrophilic reactions with substrates in Eq. (9): note that singlet biradical character of the low-spin (LS) Mn(V)@O bond decrease significantly in the case of insertion-type reaction in Fig. 3. Several evidence [29] suggests that chloride anion plays an important role for oxygen evolution in Limburg reaction systems (7) like native OEC (1) in Fig. 1. This implies that SE2-like mechanism is also conceivable as discussed later (see Fig. 10). Koizumi et al. [35] have carried out the DFT calculations of dimer of manganese–oxo (MnO) porphyrin (PO) synthesized and characterized by Naruta’s group [36]. They have investigated variations of the electronic structures of POMn(X)@O with the change of oxidation number (X) of the Mn ion. It was found that the Mn(V)@O bond in Naruta’s oxygen evolution system has the oxygen-diradical character, which may entail the oxygen-atom radical coupling as follows: ðPOMnðVÞ@OÞ2 ! POMnðIVÞAOAOAMnðIVÞPO ! ðPOMnðIIIÞÞ2 þ O2
ð9dÞ
However, more complex mechanisms involving ionic processes are conceivable even in this case. For example, Fig. 9a illustrates the radical coupling mechanism for the formation of molecular oxygen in Eq. (9d), which is theoretically feasible because of the biradical nature of the Mn@O bond as shown in Figs. 7 and 8. On the other hand, strong electrophilic nature of the high-valent [Mn(V)@O+ Por] and/or [Mn(IV)@O Por Æ+] bonds indicates a possibility of the ionic (SE2) process [24] in Fig. 9b, where electrophilic attack of the oxygen of MnO to the lone pair of water is a key step for the O–O bond formation in oxygen evolution. Thus our theoretical studies on native OEC and artificial OEC [28,30,35] systems have revealed the crucial role of the high-valent Mn(V)@O and/or Mn(IV)@O bonds. 4.2. SE2 mechanism of oxygen evolution The present computational results indicate that the insertion (or rapid rebound) mechanism, 1O-model [24], is
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K. Yamaguchi et al. / Polyhedron 26 (2007) 2216–2224
Fig. 9. (a) Radical coupling mechanism of the O–O bond formation in the artificial OEC system and (b) ionic (SE2) mechanism of the O–O bond formation. The latter mechanism is closely related to that of OEC in Fig. 10.
applicable to the oxygenation by high-valent Mn–oxo species examined here because of strong diradical characters. However, the diradical character of the Mn–O bond is found to be sensitive to environmental effects such as hydrogen bonding and clustering of waters (see Tables 1 and 2). This in turn indicates that the nature of Mn@O bonds in 1 is variable depending on the electronic states of the cubane unit CaMn3O4. Therefore, three mechanisms in Fig. 3 are conceivable theoretically. Present computational results indicate a possibility of our previous bimolecular electrophilic substitution (SE2) mechanism (see Fig. 3) for oxygen evolution reaction in OEC as illustrated in Fig. 10. From Fig. 10, the oxygen site of the high valent manganese–oxo bonds [Mn(V)@O+ 4] and/or [Mn(IV)@O 4 Æ+] in OEC undergoes the electrophilic attack of lone pair of water molecule, followed by the concerted proton migration with base (for example hydrogen-bonding networks involving protein side chains within local environment). This SE2 reaction produces the Mn(IV)–hydroperoxide anion complex, which undergoes second proton migration to afford the low-spin
Mn(IV)–superoxide anion complex. The regulation of charge on O2 fragment by CaMn3O4 (4)part is feasible in the case of 1. The back electron transfer from superoxide anion to Mn(IV) generates triplet molecular oxygen and triplet Mn(III) complex as follows: 1
1 3 3 3 3 ½MnðIVÞO 2 ! ½ MnðIIIÞ O2 ! MnðIIIÞ þ O2
ð9eÞ
3
It is noteworthy that O2 is generated without spin inversion via spin–orbit interaction. The key point of the SE2 mechanism is the electrophilic nature of oxygen site in the high-valent manganese–oxo bonds [24]. The SE2 mechanism in Fig. 10 is consistent with the proposal by Iwata and Barber on the experimental ground [37,38]. The reaction scheme in Fig. 10 is now under further investigation in our laboratory. 4.3. Implications to related oxygenation reactions Finally, implications of the previous [24–28] and present computational results are briefly discussed in relation to other oxygenation reactions by metal–oxo species. For
Fig. 10. Possibility of the bimolecular electrophic substitution (SE2) mechanism of oxygen evolution reaction from water in OEC of the photosynthesis II. The SE2 mechanism is a direct extension of that in Fig. 3 (see text). It does not entail the formation of hydroxyl radical as in the case of the 3O-model.
K. Yamaguchi et al. / Polyhedron 26 (2007) 2216–2224
example, the conversion of methane to methanol is catalyzed at the active site of a metalloenzyme known as methane monooxygenase (MMO) (Mn ions in 6 and 7 are replaced with Fe ions in MMO) CH4 þ NADH þ Hþ þ O2 ! CH3 OH þ NADþ þ H2 O
2223
Table 3 Classifications of the reaction mechanisms of methane monooxygenation by several theoretical groups Our proposalsa
Recent computational results
SE2 model O-model
Yoshizawa (concerted) modelb Friesner–Lippard (bound-radical) modelc Morokuma–Basch (hydrogen abstraction) modeld Siegbahn (hydrogen abstraction) modele
ð10Þ
1
Both cationic and radical intermediates (or transition structures) have been proposed for this reaction on the experimental grounds [39]. Past decade, several computations have been performed to elucidate the nature of the intermediate in MMO. According to our previous proposal [24], computational results on the iron–oxo (Fe(IV)@O) species in MMO are classified into three categories illustrated in Fig. 3. Yoshizawa et al. [40,41] have proposed a concerted (fourcentered) mechanism between Fe@O and H–CH3 fragments on the basis of the spin-restricted (RHF) calculations. Their mechanism is similar to the SE2 (concerted) mechanism in Fig. 3, though our SE2 mechanism is based on the high-spin configuration of the Fe(IV) center instead of their closedshell (RHF) configuration. On the other hand, Basch, Morokuma and co-workers [42,43] have been proposed a hydrogen-abstraction mechanism for hydroxylation reaction by MMO, assuming the four unpaired spins at each Fe(IV) center of Q (namely the high-spin 9A dimer) in the spin-unrestricted DFT (UDFT) calculations. The hydrogen-abstraction mechanism in the 9A dimer model is similar to the 3O (abstraction)-model in Fig. 3 since the reaction site is regarded as the 3O plus H–CH3 system. Siegbahn et al. [44,45] have proposed a hydrogen abstraction model in the high-spin mixed-valence (MV) state: Q = [Fe(II)(S = 5/2) Fe(IV)(S = 2/2)O-radical]. Siegbahn model is regarded as a high-spin (3O) model in our terminology (Fig. 3) [24]. Friesner, Lippard and their co-workers [46,47] proposed a bound-radical pair model, assuming the low-spin (antiferromagnetic) dimer state of the high-spin iron (Fe(IV)) centers. Friesner–Lippard model is similar to the 1O (insertion)model, where both insertion and rapid recombination between the singlet radical pair (ÆOH plus ÆCH3) are feasible, depending on the reaction conditions [24,26]. Table 3 summarizes the proposed reaction mechanisms of methane monooxygenation (MMO) by several theoretical groups. The conclusions are dependent on the assumed anti (AF) and ferro (F) magnetic spin couplings of the iron oxo cores (Fe2O2) in MMO. However, the low-spin (LS) AF broken-symmetry usually involves the high-spin (HS) component. Therefore use of an approximate spin projected (AP) BS solution [23–28] is desirable for location of transition structure on the pure LS surface. This situation clearly indicates necessity of further theoretical investigations based on more realistic reaction-site and spin-state models including protein environments. Both radical and ionic mechanisms are also proposed for hydroxylation reactions of P450 with the active site: [Fe(IV)@OÆPorÆ+] [48]. The situation is quite similar to those of MMO and OEC in the photosynthesis II system.
3
O-model
a b c d e
Refs. Refs. Refs. Refs. Refs.
Methods RHF UDFT
1
9
A by UDFT
high spin MV by UDFT
[24,26]. [40,41]. [46,47]. [42,43]. [44,45].
This in turn indicates that theoretical and computational efforts may provide a unified picture and key concepts for understanding of oxygenation reactions in general [24,26]. 5. Concluding remarks The nature of high-valent manganese–oxo (Mn(V)@O) bonds has been investigated on the basis of the hybrid DFT calculations of the model complexes 1, 2, and 3 for oxygen evolution center (OEC) and the Mn–oxo prophyrine complex (8). It is found that charge transfer from ligands to Mn(V)@O occur to indicate significant contribution of the [Mn(IV)@O L Æ+] configuration. Therefore the high-valent (HV) Mn–O bond is regarded as the superposed state of these two configurations in general, WðMnðHVÞ@OÞ ¼ C 1 W1 ðMnðVÞ@O LÞ þ C 2 W2 ðMnðIVÞ@O Lþ Þ;
ð11Þ
where Ci denotes the mixing coefficients, which are variable with ligands and environmental effects as shown in this paper. The dual character of the HV Mn–O bond would be a key factor for theoretical understanding of complex behaviors of chemical reactions by HV Mn–O compounds. Similar situations are also found in HV iron–oxo species in MMO and P450. The hybrid DFT (HDFT) followed by the natural orbital analysis is a useful and practical method for theoretical investigations of metalloenzymes as shown in this series of papers [49]. Acknowledgement This work has been supported by a Grant-in-Aid for Scientific Research on Priority Areas (Nos. 18350008 and 18205023) from Ministry of Education, Science, Sports and Culture, Japan. References [1] K.N. Ferreira, T.M. Iversion, K. Maghlaoui, J. Barber, S. Iwata, Science 303 (2004) 1831. [2] B. Kok, B. Forbush, M. McGloin, Photochem. Photobiol. 11 (1970) 457.
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