theory of chemical bonds in metalloenzymes. xvii. symmetry breaking in manganese cluster structures...

Theory of Chemical Bonds inMetalloenzymes. XVII. SymmetryBreaking in Manganese ClusterStructures and ChameleonicMechanisms for the OAO BondFormation of Water Splitting Reaction

TORU SAITO,1 MITSUO SHOJI,1 KEITA KANDA,1 HIROSHI ISOBE,1

SHUSUKE YAMANAKA,1 YASUTAKA KITAGAWA,1 SATORUYAMADA,1 TAKASHI KAWAKAMI,1 MITSUTAKA OKUMURA,1

KIZASHI YAMAGUCHI2

1Department of Chemistry, Graduate School of Science, Osaka University, Toyonaka, Osaka 560-0043, Japan2Center for Nanomaterial Design, Osaka University, Toyonaka, Osaka 560-8531, Japan

Received 28 April 2011; accepted 26 July 2011Published online 19 January 2011 in Wiley Online Library (wileyonlinelibrary.com).DOI 10.1002/qua.23255

ABSTRACT: Symmetry breaking in cluster structures of manganese oxides by dop-ing of Ca(II) ion is examined in relation to chameleonic mechanisms of water splittingreaction. The orbital and spin correlation diagrams have been depicted to clarify one-electron transfer and electron-pair transfer mechanisms for the reaction. The spin-polar-ized molecular orbital models have been applied to elucidate correspondence betweenmagnetic-coupling mode and reaction mechanism of the oxygen–oxygen (OAO) bondformation and oxygen evolution catalyzed by multicenter Ca(II) manganese oxides andrelated systems. The present UB3LYP calculations followed by the natural orbital analy-ses have been performed to elucidate electronic structures of the key intermediates andthe transition state structure for the OAO bond formation. The results indicate that thereaction proceeds through the continuous diradicaloid mechanism without discreet freeradical fragments and/or electron-pair transfer mechanism induced by symmetry break-ing with Ca(II) in the pure low-spin singlet state. The computational results are compat-

Additional Supporting Information may be found in the online version of this article.Correspondence to: T. Saito; e-mail: [email protected] grant sponsor: Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan.Contract grant number: 22108515, 23550016.

International Journal of Quantum Chemistry, Vol. 112, 121–135 (2012)VC 2011 Wiley Periodicals, Inc.

ible with local singlet and triplet diradical-coupling mechanisms for the OAO bond for-mation in the low- and high-spin states, respectively. Thus, magnetic (exchange) cou-pling modes in the oxygen evolution complex are directly related to the local singletand triplet diradical mechanisms as in the case of soluble methane monooxygenase.VC 2011 Wiley Periodicals, Inc. Int J Quantum Chem 112: 121–135, 2012

Key words: symmetry breaking; cluster structure; electron-pair transfer; correlationdiagram; OAO bond formation

1. Introduction

M any metalloenzymes have binuclear andmultinuclear transition-metal complexes

that play important roles as active sites for cata-lytic cycles in biological reactions [1]. The 3d tran-sition-metal ions including Mn, Fe, Cu, and soforth in these systems are usually magnetic in na-ture, and they are exchange coupled. Therefore,their temperature-dependent paramagnetisminvestigated by magnetic and optical experimentsis a measure of cooperative interactions [2]. Mag-netism and chemical bond is an important guid-ing principle for theoretical analysis of these sys-tems. In this series of papers, we have elucidatedcorrespondence between magnetic-coupling modeand reaction mechanism of several oxygenationreactions [3]. As shown in part XIV of this series[4], binuclear iron di-l-oxo complex, so-called in-termediate Q, in soluble methane monooxygenase[5–10] exhibits antiferromagnetic and ferromag-netic exchange couplings. The antiferromagneticand ferromagnetic states corresponds, respec-tively, to the local singlet and triplet diradicalmechanisms for the monooxygenation reaction ofmethane as illustrated in Eq. (1) in Scheme 1. The-oretically, the same mechanisms are conceivablefor the oxygen–oxygen (OAO) bond formation forbinuclear manganese di-l-oxo complex and hy-droxide anion (or water) as illustrated in Eq. (2)in Scheme 1 [11–18]. On the other hand, a nucleo-philic attack of hydroxide anion to electrophilicoxygen site has also been proposed for the OAObond formation as illustrated in Eqs. (3) and (4)of Scheme 1.

The concept of symmetry and broken symme-try in cluster structures plays an important rolefor water splitting reaction, because many differ-ent cluster structures of manganese oxides havebeen proposed for active sites of the reaction atoxygen-evolving complex in native and artificialphotosystem II (PSII; Refs. 11–18). For example,

Vincent and Christou [19] have considered theMn4O4 cuboid structure A as illustrated inScheme 2. The key step of their proposal is thehomolytic diradical coupling between oxyradicals:charge and spin populations are symmetricbecause of the cluster symmetry of A,

X� O � þ � O� X ! X� O� O� X

ðX ¼ MnÞ: ð1aÞ

Ruttinger and Dismukes [13] have developedthe Mn4 cuboid complexes A for an effective cata-lyst for water splitting reaction. Similarly, Berke-ley (Yachandra, Yano, and their collaborators)group has proposed the radical-coupling mecha-nism for the OAO bond formation in the dimer ofdimer structure B on the experimental grounds[11]. It is noteworthy that these catalytic clusters(A and B) consist of only Mn and O atoms, lead-ing to the homopolar diradical intermediate inEq. (1a).

Pecoraro et al. [20] have considered a broken-symmetry cluster structure C that has a divalentCa(II) as shown in Scheme 2. The key concept oftheir proposal is the nucleophilic attack of hy-droxide anion to electrophilic oxygen. It meansthat the Ca(II) ion plays an important role forintroduction of heterolytic character in the OAObond formation. Theoretically, Ca(II) does nothave local spin that more or less induces the spinpolarization at an oxygen site. Therefore, intro-ducing Ca(II) ion into MnO clusters breaks thecluster symmetry (topology), providing the zwit-terionic character for the OAO bond formation.

X� Oþ½ � þ �OH� Y½ � ! X� O� OH� Y

ðX ¼ Mn; Y ¼ CaðIIÞ � � � Þ ð1bÞ

Iwata and Barber [21] have also proposed asimilar nucleophilic mechanism of water to elec-trophilic oxo species on their X-ray structure of

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122 INTERNATIONAL JOURNAL OF QUANTUM CHEMISTRY DOI 10.1002/qua VOL. 112, NO. 1

CaMn4O4 cluster D where one of Mn ion of thecuboid cluster is substituted with Ca(II) ion asillustrated in Scheme 2. Thus, Ca(II) plays an im-portant role for stabilization of a hydroxide anion(or a water molecule).

Symmetry breaking is indeed a fundamentalconcept for theoretical understanding of complexbehaviors of multinuclear transition-metalenzymes in biology [1]. In this series of papers[22–24], we have examined several iron–sulfurclusters that play important roles in electrontransfers and several chemical reactions. Thebinuclear iron–sulfur (2Fe–2S; A) and tetranucleariron–sulfur (4Fe–4S; B) clusters have D2 and Td

symmetries, respectively, as shown in Scheme 3.

Interestingly, the D2 symmetry is broken in thecase of Rieske-type 2Fe–2S cluster (C) due to thedifferent ligand field [24]. Similarly, the Td sym-metry is also broken in 4Fe–4S cluster of aconitase(D) [1]. Furthermore, a substitution of metalsite(s) with another metal ion often breaks thecluster symmetry in larger iron–sulfur clusterssuch as the conversion from P-cluster (E) to FeMocofactor (F) in the nitrogen fixation catalyst [25].Thus, symmetry and broken symmetry play animportant role for characterization of clusterstructures of multinuclear iron–sulfur complexesin chemistry and biology. These are closelyrelated to homolytic and heterolytic bond clea-vages (or formations) in chemical reaction as dis-cussed previously [3, 4, 22–25, 26].

SCHEME 1. CH3AOH and OAO bond formation inbinuclear complexes in soluble methane monooxygen-ase (sMMO) and OEC of PSII.

SCHEME 2. Proposed active sites (A–D) at the OECof PSII.

SCHEME 3. Symmetry breaking found in the active sites (A–F) of multinuclear iron–sulfur complexes in enzymes.

THEORY OF CHEMICAL BONDS IN METALLOENZYMES

VOL. 112, NO. 1 DOI 10.1002/qua INTERNATIONAL JOURNAL OF QUANTUM CHEMISTRY 123

Theoretically, distinct mechanisms in Eqs. (1a)and (1b) correspond, respectively, to the extremecases in the valence-bond (VB) description of theOAO bond formation in water splitting reactionat oxygen-evolving complex (OEC) of PSII (detailsfor the VB description of the OAO bond, see Sup-porting Information). In fact, the broken-symme-try density functional theory (BS DFT) calcula-tions followed by the natural orbital analysis haveelucidated that the OAO bond formation proc-esses are qualitatively described by the superposi-tion of these extreme VB configurations as UBS–Cl

¼ C1w1(DR) þ C2w2(ZW), where Ci means a linearcombination coefficient of the BS configuration re-sponsible for the extreme diradical (DR) or zwit-terion (ZW) electronic structure. As shown in theprevious papers [3, 4], the weight of DR or ZW ishighly dependent on environmental conditionssuch as hydrogen bonding. The DR character ofthe Mn¼¼O bond can be variable as illustrated inScheme S1A, Supporting Information, showingthat the environmental conditions heavily affectthe reactivity. Therefore, theoretical analyses ofhomolytic and heterolytic characters in Eq. (1a)and (1b) are useful for understanding the charac-teristic behaviors of manganese oxides with dif-ferent cluster structures. In fact, we have alreadyexamined the OAO bond formation in the case ofthe diradical extreme in part XV of this series[26], assuming possible cluster structures [27–30].Our computational results indicated that the envi-ronmental effects enhance the zwitterionic (heter-olytic) character for the OAO bond formation asshown in Figures S1B and S1C, Supporting Infor-mation.

X�Oþ½ �EE þ �OH� Y½ �EE ðEE : environmental effectÞ! X� O� OH� Y

ðX ¼ Mn; Y ¼ CaðIIÞ � � � Þ ð1cÞIn the previous papers [31, 32], we have con-

sidered both the Cl-anion and the water-assistedOAO bond formation for water splitting reactionlike base-catalyzed oxygenations in accord withEq. (1c) (for the water-assisted mechanism, seeFig. 10 in Ref. 32).

Very recently, Umena et al. have revealed theX-ray diffraction structure of the CaMn4O5 clusterin the OEC of PSII refined to 1.9 A resolution[33]. The hydrogen-bonding networks at OEC ofPSII have been elucidated for the first time on thebasis of their X-ray structure. Therefore, a water-assisted OAO bond formation can proceed at least

for the native OEC system. As a continuation ofpart XV [26], we here examine a more generalcase that involves more or less ZW character inEqs. (1b) and (1c). The broken symmetry (topol-ogy) in Mn cluster structures by doping of Ca(II)ion are extensively investigated in relation to theenhancement of the ZW character. Orbital andspin correlation diagrams have been depicted toelucidate possible mechanisms of water splittingreaction on the theoretical grounds. Hybrid DFTcalculations for a binuclear model cluster con-structed on the basis of the very recent 1.9 A reso-lution X-ray structure [33] are also performed toobtain an energy profile for the OAO bond forma-tion. Implications of the present results are brieflydiscussed in relation to computational results byseveral other groups and experimental resultsavailable [11–18].

2. Possible Mechanisms for the OAOBond Formation

2.1. ONE-ELECTRON AND ELECTRON-PAIRTRANSFER MECHANISMS FOR BINUCLEAR MNCOMPLEXES WITH MN(V)¼¼O SPECIES

First of all, let us consider the nucleophilicattack of hydroxide anion to formal electrophilicMn(V)¼¼O bond in terms of the broken-symmetrymolecular orbital (MO) descriptions [34–39] asshown in Figure 1. We have already investigatedthis OAO bond formation process in the case ofmononuclear manganese complexes in part XVIof this series [40]. It was found that a spin crossover was crucial during the reaction since the sin-glet coupling between oxyl-radical (O�

� %) andhydroxy-radical (OH� :) is requisite. This meansthat multinuclear manganese complexes are cru-cial for a smooth OAO bond formation without aspin cross over. As shown previously, severalguiding principles for structure and reactivity ofmanganese oxides have been obtained by the pre-vious BS DFT calculations of these species [26, 34,41–43]. These principles (A–F) summarized inSupporting Information can be used for the watersplitting reaction in the OEC.

Here, the guiding principles (A–F) [26, 40] areapplied to the nucleophilic attack of hydroxideanion to electrophilic oxygen site of formalMn(V)¼¼O species (21a) as shown in Figure 1. Thespin polarization usually occurs to give the dirad-ical configuration 21b [34]. Other possible

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electronic configurations of Mn(V)¼¼O species aredepicted in Figure S2, Supporting Information.The following one-electron transfer is feasiblefrom oxyl-radical site in 21b to the Mn(IV) ion,providing 22c. Therefore, the electron-pair transfereasily occurs in this configuration to form theOAO bond (24b). On the other hand, the one-elec-tron transfer is also feasible from OH� to theMn(IV) ion in 21b, giving 23b with the local sin-glet diradical configuration. The radical-couplingyields the product 24b. Thus, two possible reac-tions for the OAO bond formation can be pro-posed on the theoretical grounds. However, the22c and 23b configurations in Figure 1 are corre-sponding to the extreme cases in the VB descrip-tion, and the true doublet state is given by theconfiguration mixing between one-electron trans-fer (OET) and electron-pair transfer (EPT) as UBS–

Cl ¼ C1UEPT(22c) þ C2UOET(

23b), where the mixingcoefficients are variable with environmentaleffects. The weight of the electron-transfer diradi-cal character can be analyzed by evaluating theorbital overlap between broken-symmetry MOs.As the diradical character is sensitive to computa-tional methods [44], it is difficult to make a clear-cut theoretical distinction between one-electronand electron-pair transfer mechanisms.

As shown in Figure 2, for the high-spin binu-clear complex, the one-electron transfer fromoxyl-radical site in 61b to the Mn(IV) ion is unfav-

orable because of the generation of the intermedi-ate spin state of Mn(III). The spin inversionshould occur to form 82c. The subsequent elec-tron-pair transfer in 82c state easily forms theOAO bond, providing the high-spin product 84b.On the other hand, the one-electron transfer isalso feasible from OH� to the Mn(IV) ion of 61b,giving 63b with the local triplet diradical (LTD)configuration. The conversion from the LTD pair(O�

� %…� %OH) to the local singlet diradical(LSD) pair (O�

� %…� :OH) in 83b is required toyield the product 84b. The spin exchange can alsooccur to form the other LSD configuration (63b0).The OAO bond formation is feasible even in 63b0,but it gives the unstable product 64b on the basisof the model. The 64b state becomes more unfav-orable than 84b because of the guiding principle(A) in the Supporting Information. It means thatthe spin cross over from the sextet to the octetstate occurs during the OAO bond formation. Thesituation is true of mononuclear Mn complexes[40]. Possible energy levels are derived from theguiding principles on the basis of the Huckel–Hubbard–Hund model as illustrated in Figure 3.From Figure 3, the antiferromagnetic and ferro-magnetic spin-coupling modes play an importantrole for state correlation diagrams. The energylevels of the quartet state 41a or the quartet 44aand sextet 64b states can be obtained using thefollowing Eqs. (2) and (3) [34, 41–43].

FIGURE 1. Orbital and spin correlation diagram for nucleophilic attack of hydroxide anion to electrophilic oxo site offormal Mn(V)¼¼O (21a) species in the low-spin state. First, spin-polarization (SP) transforms 21a to 21b, while two-elec-tron transfer (TET) provides 22c. For

21b, the OET gives 22c or 23b. The product 24a can be obtained from 23b via radi-cal coupling (RC) or 22c via EPT.



DE ¼ �J ðS� 1ÞS� SðSþ 1Þf g ¼ 2SJ: (2)

Under this approximation, the J values by ourapproximate spin projection procedure are givenby the simple equation [34, 41–43]:

J ¼ LSE� HSE� ��

HS S2� �� LS S2

� �� ; (3)

where YE and YhS2i denote, respectively, the totalenergy and total angular momentum for a spinstate Y. To describe these intermediate spin states,the resonating BS configuration interaction andmultireference approaches based on the BS natu-ral orbitals are desirable [44]. The guiding princi-ples (A–F) can also be applicable to electrophilicoxygen site Mn(IV)¼¼OH instead of Mn(V)¼¼O(see Figs. S3–S5, Supporting Information).

2.2. ENHANCEMENT OF ZWITTERIONICCHARACTER FOR BINUCLEAR MN OXIDES

The orbital and spin correlation diagrams haveclearly revealed the analogy between the monoox-ygenation of methane and the OAO bond forma-tion as mentioned above. This in turn indicatesthe significant role of the local singlet diradicalconfiguration even in the low-spin state, becauseleakage of free radical (�OH) is prohibited particu-larly in biological systems [1]. Therefore, theintroduction of unsymmetrical ligand fields isnecessary for enhancement of zwitterionic charac-ter in the nucleophilic attack of hydroxide anionto the oxo site like in the case of C and D inScheme 3. Note that the configuration mixingbetween pure diradical and zwitterion providesthe covalent-bonding character [26]. Similarly, thesymmetry breaking of the cluster introducing aCa(II) ion is also effective as illustrated in C andD in Scheme 2 (see also F in Scheme 3), because

FIGURE 3. Possible state correlation diagrams for theOAO bond formation between formal Mn(V)¼¼O and hy-droxide anion in Figures 1 and 2 on the basis of theHuckel–Hubbard–Hunt model.

FIGURE 2. Orbital and spin correlation diagram for nucleophilic attack of hydroxide anion to electrophilic oxo site offormal Mn(V)¼¼O (21a) species in the high-spin state. First, spin-polarization (SP) transforms 61a to 61b, while two-elec-tron transfer (TET) with spin inversion (SI) provides 82c. For

61b, the OET gives 63c, while OET with SI yield 82c. Theproduct 84b (or 64b) can be obtained from 82cc via EPT or radical coupling (RC) or 63b via SI (83b or 63b

0), followed byradical coupling (RC).

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Ca atom usually exists in the spin-less Ca(II)state.

As shown in Figure 4, we consider a binuclearfragment 11a(S0) on the basis of the very recent X-ray structure [33]. The deprotonation of the watermolecule ligated to Mn1 ion and its oxidation bythe first photoexcitation provides the intermediate22a(S1, S2). Further photoexcitation induces protonand electron releases, giving the antiferromagneticintermediate 13a(S3). The subsequent photoexcita-tion for 13a(S3) provides the short-lived intermedi-ate 24a( S4a). The spin polarization of Mn1(V)¼¼Obond in 24a( S4a) gives rise to the oxyl-radical sitein 25a( S4b). The one-electron transfer type (1)from hydroxide anion to Mn2(IV) ion in 25a( S4b)gives the local singlet diradical configuration 26a(S4c) that collapses to the product 27a(S4f) with theMn1(IV)O-OH moiety. On the other hand, theone-electron transfer type (2) from oxyl-radicalsite (�Mn1(IV)¼¼O�) to the Mn2(IV) ion generatesthe zwitterionic pair 26a0( S04c). The electron-pairtransfer is feasible for 26a0( S04c), yielding theproduct 27a(S4f). These essential features are the

same as the conventional di-l-oxo Mn2O2 modelwithout Ca(II) ion (see Figure S6, Supporting In-formation), because the antiferromagneticexchange coupling between Mn ions is crucial forsmooth OAO bond formation. It is noteworthy,however, that the symmetry breaking due toCa(II) ion stabilizes the hydroxide anion, and itcan enhance weight of the electron-pair transferprocess. The HOAOH bond formation can beexplained in a similar way as shown in FiguresS7 and S8, Supporting Information.

3. Hybrid DFT Calculations of theOAO Bond Formation

3.1. COMPUTATIONAL DETAILS

We constructed a binuclear manganese com-plex on the basis of the X-ray structure (PDBcode: 3arc) [33] as shown in Figure 5(a). In theprevious study [40], we performed partial geome-try optimizations for a mononuclear manganese

FIGURE 4. The configuration correlation diagram for the OAO bond formation with the binuclear manganese com-plex that is isoelectronic to the Q (Fe–O2–Fe) intermediate in soluble methane monooxygenase. SI, RC, OET, EPT,and SP represent spin inversion, radical coupling, one-electron transfer, electron-pair transfer, and spin-polarization,respectively.



complex constructed from the same X-ray struc-ture (see Fig. S9, Supporting Information) tolocate the reactant (R), transition state (TS), andthe product (P) at the UB3LYP/def2-SVP levels[45, 46]. All heavy atoms except for O3 and O8atoms were kept fixed on the X-ray structure dur-ing the partial geometry optimizations. Here, wesuperimposed these optimized O3 and O8 atomson the present binuclear model for the initialstructures corresponding to R, TS, and P. Foreach structure, the hydrogen atoms were opti-mized, while all heavy atoms including O3 andO8 atoms were kept fixed to obtain the approxi-mate R, TS, and P. Then, the single-point energycalculations both for the low-spin (LS; S ¼ 1/2)Mn1( %)Mn2( :) and for the high-spin (HS; S ¼5/2) Mn1( :)Mn2( :) states were performed at theUB3LYP/def2-SVP levels. Natural orbital analysesof the UB3LYP solutions for both the LS and theHS states have also been performed to elucidatethe bond nature corresponding to the OAO bondformation. All calculations were performed withGaussian 09 program package [47].

3.2. COMPUTATIONAL RESULTS

Table I summarizes spin populations on theselected atoms for the LS and HS states at R, TS,and P. The obtained energy profiles for the low-and high-spin states are depicted in Figure 5(b).

The magnitudes of the calculated spin popula-tions on both Mn1(V) and Mn2(IV) atoms arequite larger than their formal values of 2.0 and3.0 due to the spin polarization effect of the oxospecies. In fact, the spin populations on the bridg-ing oxo atoms (O4 and O5) are �0.595 (�0.566)and 0.570 (�0.395) for the LS (HS) states, respec-tively. These values provide an evidence for par-tial charge transfer from the bridging-oxo speciesto the high-valent Mn ions. The tendency is trueof the O3, O6, and O8 atoms. As the spin popula-tions on the O3 and O8 atoms are 0.740 and�0.405 for the LS state, the local singlet diradicalpair should be generated. On the other hand, inthe HS state, the O3 and O8 atoms form the localtriplet diradical pair with the corresponding spinpopulations of �0.683 and �0.410. These elec-tronic structures support the orbital and spin cor-relation diagram as described in Section 2.1. How-ever, this case differs from the general cases(presented in Figs. 1 and 2) in the way that notMn2(IV) but oxo species are involved in the one-electron transfer from the O8 site. Unlike the cal-culated results with the use of a more realistic forthe CaMn4O5 cluster [48], the O3 and O8 atoms inthe high-spin state have also the local singlet dir-adical configuration at TS. According to the natu-ral orbital analysis, the orbital overlaps corre-sponding to the reactive p bond in the Mn1¼¼O3moiety at R are 0.652 and 0.665 for the low-spin

FIGURE 5. (a) Binuclear model structure based on the basis of the 1.9 A resolution X-ray structure. (b) State correla-tion diagrams for the low-spin (S ¼ 1/2) and high-spin (S ¼ 5/2) states obtained at the UB3LYP/def2-SVP level. [Colorfigure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

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and high-spin states, respectively, as depicted inFigure 6. The calculated diradical character (y)values are 8.5 and 7.8% for the LS and HS states,respectively. Note that the y values are calculatedusing Eq. (4) [22–26, 38].

y ¼ 2WD ¼ 1� 2T

1þ T2(4)

The diradical character of the reactive p bondis small regardless of the LS and HS state, sup-porting the zwitterionic character for the O3AO8

bond formation. In fact, the y values correspond-ing to the O3AO8 bond are 0.0% for both the LSand the HS states at TS. As shown in Figure 5(b),the activation barrier is only 5.0 kcal/mol in theLS state due to the smooth local singlet diradicalcoupling. The reaction energy of the formation ofP is exothermic (�14.2 kcal/mol). In contrast, theactivation barrier height in the HS state is signifi-cant large (29.5 kcal/mol), and the reactionenergy to form P is endothermic by 12 kcal/mol.It strongly indicates that the local triplet diradicalconfiguration followed by the O3AO8 bond for-mation is unfavorable in the HS state without thegeometry relaxation. We did not perform a fullgeometry optimization in the HS state, because itcan raise artificial geometric changes caused bythe truncated model complex. From the calculatedresults on the basis of the 1.9 A X-ray structure, itis confirmed that the antiferromagnetic exchangecoupling between Mn sites and Ca(II) ion are req-uisite for the smooth OAO bond formation withless diradical character.

4. Discussion

4.1. SYMMETRY BREAKING BY SUBSTITUTIONOF MN ION WITH CA(II) ION IN TETRANUCLEARMANGANESE OXIDE COMPLEXES

As shown in Section 2, the OAO (or HOAOH)bond formation can be explained even for theantiferromagnetic binuclear manganese com-plexes. However, multicenter Mn complexes arenecessary for the next step: namely facile deproto-nation of MnOOH (or MnHOOH) to generatetriplet molecular oxygen (;�OAO�;). As shownpreviously [26, 48], the ferromagnetic exchange-

TABLE ISpin populations on the Mn, O, and Ca atoms for LS and HS states of binuclear manganese modelcomplexes.

Atom

R TS P

LS HS LS HS LS HS

Mn1 �3.693 3.706 �4.182 2.813 �4.423 2.499Mn2 3.848 4.189 3.848 4.236 3.841 4.246O3 0.740 �0.683 0.087 0.050 0.040 �0.005O4 �0.595 �0.566 0.316 �0.697 0.498 �0.604O5 0.570 �0.395 0.719 �0.938 0.764 �0.793O6 0.511 �0.968 0.419 �0.335 0.361 �0.380Ca7 0.032 0.065 �0.024 0.027 �0.029 0.033O8 �0.405 �0.410 �0.147 �0.179 �0.008 �0.017

FIGURE 6. The bonding and antibonding natural orbitalscorresponding to the O3AO8 bond formation at R and TS(see also Fig. 5). [Color figure can be viewed in the onlineissue, which is available at wileyonlinelibrary.com.]



coupled :MnAMn: site is necessary for the gener-ation of ;�OAO�;, because reactant water mole-cules are closed-shell singlet species. The singlet-coupled singlet pair 1[(:;)(:;)] of reacting watersis transformed into the singlet state 1[(::)(;;)]constructed of exchange coupling between tripletmolecular oxygen (;�OAO�;) and ferromagnetic:MnAMn: site. Past decades dimer of binuclermanganese oxide and cuboid tetranuclear Mnoxides have been utilized for mimicking activesites of the water splitting reaction [11–18]. Asmentioned above, Dismukes [12] has elucidatedthat cuboid Mn4O4 oxides (Ia) depicted in Figure7 undergoes the OAO bond formation via theradical-coupling mechanism (see also A inScheme 2). In part XV, we discussed severalresults calculated by DFT methods starting fromIa [26].

On the other hand, the hetero cuboid clusterCaMn3O4 (IIa) without the Td symmetry is pro-vided with substitution of Ca for Mna. The bro-ken-symmetry (topology) CaMn3O4 unit IIa is thebasis of several active sites that have been pro-posed (IIIa–VIa) depicted in Figure 7. In particu-lar, VIa obtained by Shen and coworkers is mostreliable at the present stage [33]. Although theBerlin (Dau) structure (Va) [30] has the sameCaMn4O5 unit as VIa, its coordination environ-ment around Ca(II) is different from VIa. The car-bonyl groups of Asp189 and one water moleculeare coordinated to Ca(II) ion in Va, while twowater molecules are coordinated to Ca(II) ion inVIa. VIa can also be reduced to the Berlin (Loll)

structure (IVa) [29] and to the London structure(IIIa) [27] by removing the O4 and O5 atoms,respectively.

4.2. MN OXIDE CLUSTERS BY REMOVAL OFCA(II) ION AND OXYGEN DIANION FROM PAR-ENT CLUSTERS

The removal of the Ca(II) ion from the clusters(IIIa, IVa, Va, and VIa) in Figure 7 provides ho-mogenous Mn clusters (IIIb, IVb, Vb, and VIb)as illustrated in Figure S10, Supporting Informa-tion. The depletion of Ca(II) ion entails blockingof the OAO bond formation in the case of thenative OEC of PSII [11–18]. Further removal of O1

provides the ladder-like clusters (IIIc, IVc, Vc,and VIc) with and without dangling Mn ion. Onthe other hand, the removal of O2 provides thebroken sheet-like clusters (IIId, IVd, Vd, andVId). For Mn ions, Ca(II) ion would be necessaryin the biomimetic complexes in Figure S10, Sup-porting Information to satisfy the octahedralligand field. The removal of the Ca(II) ion fromIIa gives the Mn3O4 cluster (IIb) with C3 symme-try as shown in Figure 7. Su and Messinger [49]have proposed the cluster structure VIIa derivedfrom the IIb unit as an active site of OEC at PSIIas shown in Figure 8. Interestingly, VIIa also hasthe di-l-oxo Mn2O2 unit (VIII) as depicted in Fig-ure S11, Supporting Information. Several linearand branching forms of Mn clusters (X–XVII) aswell as XIV and D in Scheme 2 can be con-structed based on VIII [11–18]. The homolyticradical-coupling mechanism becomes predomi-nant for the OAO bond formation in these clus-ters because of homogenous cluster structures.

FIGURE 7. Cuboid structures (Ia, IIa, and IIb) foractive sites for water splitting reaction. IIIa, IVa, Va,and VIa denote London, Berlin (Loll), Berlin (Dau), andShen–Kamiya structures, respectively.

FIGURE 8. Open-form cluster structures for activesites for water splitting reaction. IXb (I, II, IIa, and III)denote Berkeley-type structures proposed on theEXAFS results.

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The removal of O4 from IIb in Figure 7 leadsIIc as shown in Figure 8. The Mn3O3 unit (IIc) hasbeen used for the construction of so-called Berke-ley structures [28] on the basis of the Extended X-ray Absorption Fine Structure (EXAFS) experi-ments (IXa(I), IXa(II), IXa(IIa), and IXa(III)). Theseopen-form structures do not have the IIa unit,and they are topologically different from IIIa–VIa.Important roles of networks of exchange-couplinginteractions between Mn ions for the characteriza-tion of topological structures have already beeninvestigated by Zein et al. [50] and Kanda et al.[51]. In contrast to VIIa and IXa, adding Ca(II)ion breaks the topological symmetry of thesestructures, leading to VIIb and IXb. Thus, thecoordination of Ca(II) ion is crucial for the topo-logical symmetry breaking, which enhances zwit-terionic character for the OAO bond formation.Besides these structures, many other cluster struc-tures have been proposed as possible active sitesfor water splitting reaction. For example, Narutaet al. have synthesized artificial catalytic systemsbased on two Mn-porphyrin fragments [52].

4.3. POSSIBLE MECHANISMS FOR THE OAOHAND HOAOH BOND FORMATION AND DIOXYGENEVOLUTION

There are four important elementary reactionsin water splitting reaction at the native OEC ofPSII: (1) deprotonation of waters, (2) oxidation of

Mn ions, (3) OAO bond formation, and (4) evolu-tion of triplet molecular oxygen [11–18]. Histori-cally, active reaction sites for these processes areregarded as high-valent Mn ion and Ca(II) asshown in Eq. (4) in Scheme 1 and C and D inScheme 2 on the experimental grounds. Becausethe proposed active sites IIIa–VIa in Figure 7 sat-isfy these conditions, common reaction mecha-nisms are conceivable. The key points are theOAO bond formation and oxygen evolution inwater splitting reaction. As shown in part XV[26], the homolytic diradical mechanism is con-ceivable if one of oxygen atom in the Ca(II)Mn4O4

skeleton of IIIa–VIa is involved in the OAO bondformation with the dangling spin-polarized�Mn(IV)¼¼O�. Siegbahn [53–55] has performedmany UB3LYP calculations for this type of theOAO bond formation starting from IIIa.

Pecoraro et al. [20] have already proposed thenucleophilic attack of hydroxide anion to electro-philic oxygen of high-valent Mn¼¼O as shown inD of Scheme 2. Similarly Iwata and Barber [21]have proposed the nucleophilic attack of watermolecule to the electrophilic oxygen (Mn(V)¼¼O)based on their X-ray structure. We have also pro-posed dual possibilities on the theoreticalgrounds: (i) OAO bond formation at the S4 stepand (ii) HOAOH bond formation at the S3 step ofKok cycle (see Fig. S12, Supporting Information).Here, these mechanisms are further developed onthe basis of the orbital and spin correlations

FIGURE 9. OAO bond formation between hydroxide anion (OH�) on Ca(II) and the Mn(V)¼¼O species on the basis ofthe London structure. (The same diagram is feasible for Berlin (Loll), Berlin (Dau) and Shen–Kamiya cluster structures,because they are also have the Ca(II) site.) SI, RC, OET, EPT, and SP represent spin inversion, radical coupling, one-electron transfer, electron-pair transfer, and spin-polarization, respectively.



diagrams revealed by the broken-symmetrytheory of chemical bonds as shown in Figure 9.The London structure (IIIa) [27] is used todescribe a possible mechanism for the OAO bondformation. It is noteworthy that the same theoreti-cal scheme is applicable to other structures IVa–VIa in Figure 7 and VIIa–IXb in Figure 8.

Pecoraro et al. [20] and Iwata and Barber [21]did not discuss explicitly charge and spin degreesof freedom in the nucleophilic reaction. Figure 9shows possible mechanisms of charge and spintransfer for the OAO bond formation and oxygenevolution in the first scenario (i), where the for-mal high-valent Mn(V)¼¼O is formed at the S4step: A( S4a), though intermediate A( S4a) can beconverted to intermediate B via the spin polariza-tion effect as discussed in our early paper [30].Moreover, the down-spin transfer occurs from hy-droxide anion on Ca(II) to Mnd(IV) ion, yieldingC (DR) with the local singlet diradical configura-tion. The intermediate C(DR) undergoes the OAObond formation to provide the MnOOH interme-diate E( S4b). On the other hand, the down-spintransfer is also feasible from Mna(V)¼¼O�; to

Mnd(IV) site to give the intermediate D (ZW).Then, the electron-pair transfer mechanism pro-vides the intermediate E( S4b). The relative contri-bution of DR and ZW configurations at the transi-tion state structure can be elucidated by thenatural orbital analysis as discussed above.

The oxygen evolution step is also important forfull theoretical understanding of water splittingreaction. The deprotonation of MnOOH in inter-mediate E( S4b) generates MnOO with the molecu-lar oxygen dianion (OAO2�) site. The one-electrontransfer from OAO2� to Mnc(IV) site provides theintermediate F(S4c) with superoxide anion(MnAOAO�

�;). The further one-electron transferfrom MnAOAO�

�; to Mna(IV) site generates thetriplet molecular oxygen with two down spins;�OAO�;. Thus, the antiferromagnetic and ferro-magnetic exchange-coupled MnAMn pairs in tetra-nuclear manganese clusters play, respectively, theimportant roles for the OAO bond formation andoxygen evolution. It is noteworthy that theexchange couplings between Mn ions in the OECof PSII are not at all trivial, because they are closelyrelated to active controls of both charge and spin

FIGURE 10. Orbital and spin correlation diagram for water splitting reaction, assuming the HOAOH bond formationat the S3 stage of the Kok cycle based on the London structure. (The same diagram is feasible for Berlin (Loll), Berlin(Dau), and Shen–Kamiya cluster structures, because they are also have the Ca(II) site.) SI, RC, OET, EPT, DR, ZW,and SP represent spin inversion, radical coupling, one-electron transfer, electron-pair transfer, diradical, zwitterion,and spin-polarization, respectively.

SAITO ET AL.


degrees of freedom in water splitting reactions.Four steps are necessary to generate the key inter-mediate A( S4a) in Figure 9 at the S4 stage.

Several experimental results such as EXAFS [11]have indicated that the high-valent Mn(V) ion hasnot been generated in the course of water splittingreaction, suggesting a possibility of the OHAOHbond formation at the S3 state. Figure 10 illustratespossible mechanisms of the HOAOH bond forma-tion and oxygen evolution in the second scenario(ii), where intermediate A(S3) with two hydroxyanions is considered as the key intermediate. Thiscorresponds to the second scenario (ii) in our pre-vious paper (see Fig. S13, Supporting Information;Refs. 48 51). As in the case of the first scenario (i),possible reaction pathways for the second scenario(ii) are presented in Figures S14 and S15, Support-ing Information, respectively.

4.4. SYMMETRY BREAKING AND IONICPROPERTY FOR WATER SPLITTING REACTION

As a continuation of part XV [26], we haveexamined possible mechanisms for the OAObond formation and oxygen evolution in watersplitting reaction. The key concept is the instabil-ity of formal Mn(V)¼¼O that is reorganized intospin-polarized �Mn(IV)¼¼O� as shown previously[34]. Recently, Siegbahn [53–55], Brudvig and co-workers [56–59], and Nocera and coworkers [60,61] have also emphasized the same character forhigh-valent Mn-oxo species. In part XV, we haverevealed possible homolytic diradical mechanismsfor the OAO bond formation under the assump-tion that the spin polarization (SP) �Mn(IV)¼¼O�

can attack the SP oxygen site of the main skeletonCaMn4O4 in IIIa, IVa, and IXb in Figures 7 and 8[27–29]. It was found that the local singlet and tri-plet diradical mechanisms are applicable for theo-retical understanding of the radical-coupling reac-tions via the one-electron transfer for the OAObond formation and generation of triplet molecu-lar oxygen in these systems. The essential featuresof these reactions are not different among thecluster structures IIIa–VIa. Very recently, wehave shown that the same mechanism is also pos-sible for the CaMn4O5 complex (VIa) [61]. Corre-spondences between local singlet (triplet) mecha-nism and antiferromagnetic (ferromagnetic)coupling between Mn ions are clearly demon-strated on the theoretical grounds. These corre-spondences are also emerged in the case of solu-ble methane monooxygenase as shown in partXIV of this series (see Scheme 1) [4]. However, no

free radical (�OH) is generated because of signifi-cant covalent bonding between OH and CH3 radi-cals [1–10]. Moreover, the introduction of symme-try breaking in ligand fields in binuclear Mncomplexes enhances the zwitterionic character inthe case of the antiferromagnetic-coupling state asshown in Figures 1–3. The same situation is notedfor 2Fe–2S and 4Fe–4S iron–sulfur clusters asillustrated in Scheme 3.

As shown in the present UB3LYP calculation inSection 2, the metal diradical character of MnAO pbond is reduced along the OAO bond formationprocess in the case of nucleophilic attack of hy-droxide anion on Ca(II) to its oxo site, showingthat the diradical character disappears at TS in Fig-ure 5. Thus, the Ca(II) ion plays a crucial role forenhancement of zwitterionic (or nonradical) char-acter at TS. The symmetry breaking in tetranuclearmanganese clusters with doping of Ca(II) ion iscommon among several cluster structures in Fig-ures 7 and 8. The charge and spin degrees of free-dom in the course of water splitting reaction canbe controlled with the topological (structure) sym-metry breaking in these clusters as shown in Fig-ures 9 and 10, suggesting an important role ofCa(II) ion that has no local spin inducing spin-polarized oxygen site. Therefore, Mna and Ca(II)sites with water are considered as active sites forwater splitting reaction in Figures 9 and 10. This inturn means that the real situation is expressed bythe superposition of the one-electron and electron-pair transfer extremes that is chemically regardedas a diradicaloid without free radical. In fact, ourrecent UB3LYP calculations [48] have elucidatedthat the diradical character is almost negligible atthe transition structure for the OAO bond forma-tion in the case of VIa [33]. Thus, symmetry break-ing in cluster structures by Ca(II) indeed plays animportant role of introduction of zwitterionic ornonradical character. Our previous [26, 48, 61] andpresent UB3LYP calculations have revealed chame-leonic (radical/zwitterionic) mechanisms for theOAO bond formation for water splitting reactionthat are highly dependent on symmetry breakingof manganese cluster structures by doping ofCa(II) ion and environmental effects as in the caseof [NiFe] and [FeFe] hydrogenases [62–65].

5. Concluding Remarks

Theoretical studies have been performed to elu-cidate electronic and spin structures of manganese



oxides that mimic the catalytic sites of water split-ting reaction in the OEC of PSII. Correspondencebetween magnetic coupling and mechanism ofradical coupling for the OAO bond formation hasbeen elucidated. Thus, magnetically coupled mul-tinuclear transition-metal complexes with localhigh-spin configurations are effective for thesmooth and continuous formation of chemicalbonds in oxygenation reactions, because atomicand molecular oxygen have the triplet groundstates. Therefore, we feel that biomolecular mag-netism is an important concept for theoreticalunderstanding between molecular magnetism andreactive oxygen and oxyradicals. Moreover, dop-ing of Ca(II) into multinuclear Mn oxide com-plexes induces symmetry breaking in clusterstructure that plays an important role for intro-duction of zwitterionic character for the OAObond formation in water splitting reaction. Suchtopological symmetry breaking is already wellknown in the case of the CAC cross-couplingreactions [66, 67]. In fact, different metals areused for stabilization of four center zwitterionictransition states for these reactions. Many Ca-doped manganese oxides have been investigatedin relation to active control of their electronic,magnetic, and optical properties in the field ofsolid state physics [68, 69]. This suggests an im-portant role of doping of Ca(II) (or other ion) intomanganese clusters for molecular design of artifi-cial oxygen-evolving systems for the OAO bondformation. We hope that quantum chemistry cal-culations are useful and effective for design ofactive catalysts for water splitting reactions,which are generated by chemical doping instrongly correlated electron systems consisted ofmagnetic atoms (Mn, Fe, Co, Ni, Cu, etc.).

ACKNOWLEDGMENT

T. S. is grateful for the Research Fellowshipsfrom Japan Society for the Promotion of Sciencefor Young Scientists (JSPS).

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theory of chemical bonds in metalloenzymes. xvii. symmetry breaking in manganese cluster structures...

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