An ab initio molecular orbital study of a binuclear dioxygen complex as a model of the binuclear active site in cytochrome c oxidase

25 September 1998

Chemical Physics Letters 294 Ž1998. 459–467

An ab initio molecular orbital study of a binuclear dioxygen complex as a model of the binuclear active site in cytochrome c oxidase Yasunori Yoshioka

a,)

, Shigehiro Kubo a , Kizashi Yamaguchi a , Isao Saito

b,c

a

b

Department of Chemistry, Graduate School of Science, Osaka UniÕersity, Toyonaka, Osaka 560, Japan Department of Synthetic Chemistry and Biological Chemistry, Faculty of Engineering, Kyoto UniÕersity, Kyoto 606-01, Japan c CREST, Japan Science and Technology, Japan Received 21 May 1998; in final form 23 July 1998

Abstract Unrestricted Hartree–Fock calculations of a binuclear dioxygen complex as a model of the binuclear active site in cytochrome c oxidase are carried out in order to allocate the reaction intermediates in the early stage of the reduction of O 2 to H 2 O. The heme a3 in the binuclear active site is replaced by Fe–4NH 3 in our model. The following results are obtained: 1q x 1q x the geometries of the intermediates, w a 2q and w a2q 3 , OO–Cu B 3 –OO, Cu B , in the singlet state are estimated, the protonated 3q 1q 1q x state w a 3 –OOH, Cu B x is found to be 2.1 kcalrmol more stable than the w a2q state, and the early stage of the 3 , OO–Cu B reduction of O 2 proceeds cooperatively with the processes of O 2 capture and protonation. q 1998 Elsevier Science B.V. All rights reserved.

1. Introduction Cytochrome c oxidase ŽC cO. is known to be a terminal oxidase of cell respiration under the process that reduces the oxygen molecule to water molecules with electron transfer from cytochrome c and proton pumping from the matrix side of the mitocondorial membrane towards the cytosolic side w1,2x. Recently, the three-dimensional structures have been determined by X-ray diffraction analyses for C cOs which are isolated from bacteria w3x and beef heart muscle w4x. The active site of the fully reduced state of the bovine heart enzyme is composed of heme a3 and Cu B w4,5x. Heme a 3 has one ligand of imidazole from the histidine residue and Cu B also has three ligands of imidazoles.

)

Corresponding author.

0009-2614r98r$ - see front matter q 1998 Elsevier Science B.V. All rights reserved. PII: S 0 0 0 9 - 2 6 1 4 Ž 9 8 . 0 0 9 2 4 - 5

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The early stage of reduction is illustrated by w6x:

Ž1.

The reduced binuclear active site reacts with O 2 to form an oxy intermediate, which undergoes successive one-electron reduction to form peroxy and to ferryl intermediates. These electron transfers are coupled with proton translation to produce one water molecule. As the following step, the ferryl intermediate successively proceeds reduction to form another water molecule with coupling of electron and proton transfers w6x. A calculation of transition-metal dioxygen complexes in biology has been a challenging problem in theoretical chemistry. Iron–porphyrin complexes play important roles in binding with molecular oxygen reversibly in the hemoglobin and myoglobin enzymes. The electronic structures and geometries of iron–porphyrin dioxygen complexes have been investigated using ab initio molecular orbital ŽMO. methods such as HF, CASSCF and DFT w7–9x. Manganese ions are also important as an oxygen-evolving complex of photosystem II, the catalytic center of the oxidation of water to molecular oxygen. DFT studies have been performed for the geometries and electronic structures w10,11x. The binuclear copper active site of hemocyanins, well-known oxygen carrier proteins, has been investigated at several levels of theory such as SCF-Xa-SW, CASSCF and DFT w12–15x. However, no quantum-chemical calculation has yet been made on the geometries and electronic structures of the binuclear iron–copper active site of C cO, although the three-dimensional structure of C cO is now available w3,4x. In this Letter, ab initio MO calculations are performed for a model of the iron–copper dioxygen complex. The purpose of this work is to allocate quantum-chemically the intermediates of the early stage of reduction of the oxygen molecule to one water molecule and to elucidate the electronic structures and reaction mechanism.

2. Reaction mechanisms proposed One of the proposed mechanisms of reduction based on kinetic and spectral studies w6x is

The oxygen molecule is bound initially to Cu1q B in the binuclear active site and transferred intramolecularly to the ferrous a32q site as shown in Eq. Ž2a.. The oxy intermediate is formed within 5 ms in both the fully reduced and mix-valence enzymes w6x. Two schemes are considered as a next step from the oxy intermediate. Scheme Ž2b. is protonation of the dioxygen with electron transfer from a 2q and proton transfer from the 3

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461

Fig. 1. Orbital interactions between d- and p- Žor p ) . MOs. Reproduced with permission from Ref. w20x.

y y 2q x proton-pumping site w16x. The other ŽScheme 2c. is the formation of w a 3q with electron transfer 3 –O O , Cu B from the a 3 and Cu B sites. 1q x w The oxy intermediate decays with rate constants of 3 = 10 4 sy1 to w a 3q 6,17x and 5 = 10 3 sy1 3 –OOH, Cu B 3q y y 2q x w w x to a3 –O O , Cu B 6,18 . Although several intermediates of this scheme have been proposed by Raman scattering experiments w6x, the reaction mechanism is not well established experimentally or theoretically even for the early stage of reduction.

3. Theoretical background A simple system M–O 2 –MX , where M and MX denote transition metals, is similar to Prussian Blue analogs such as M–CN–MX discussed from the viewpoint of magnetic interactions w19–21x. The orbital interaction diagrams of a system comprising two transition metals, M–MX , are shown in Fig. 1A at the level of symmetry-adapted MO theory. The symmetric ŽS. and antisymmetric ŽA. MOs are nearly degenerate if the interatomic distance exceeds a certain limit, inducing instability of the wavefunction. This leads to the orbital descriptions based on the unrestricted Hartree–Fock ŽUHF. approximation, in which the MOs are symmetrybroken and essentially localized on the left and right transition metals, as shown in Fig. 1A. The insertion of the molecular oxygen between two transition metals M and MX leads to the interaction between the localized UHF MOs and the bonding p- and antibonding p )-orbitals of the molecular oxygen, as illustrated in Fig. 1B. The mixing ratios between the d-, p- and p )-molecular orbitals depend on the relative position of O 2 to the two transition metal atoms M and MX . The MOs for up- and down-spins are, therefore, constructed by mixing of these MOs as illustrated in Fig. 1B.

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4. Calculational procedures and construction of a model system The reaction system Žbinuclear active site. including a porphyrin ring and four imidazole rings bound to iron and copper atoms is too large and time-consuming to systematically perform a theoretical calculation in order to allocate the intermediates. Therefore, a simpler model should be constructed without loss of the essential effects for the reduction of O 2 in the binuclear active site of C cO. The iron–porphyrin complex ŽFe–por., which is constructed by the removal of two hydrogen atoms of free-base porphyrin w22–25x and insertion of a free iron atom into the center of the porphyrin ring, has formally a polarized structure, Fe 2q–por 2y, with two-electron transfer from iron to the porphyrin ring w7–9x. The d-orbitals directly interact with the s- Žn-.-type orbitals of four nitrogen atoms in the pyrrol rings that are on the plane including the porphyrin ring. The orbitals near the HOMO of Fe 2q–por 2y are composed of p-orbitals spread over the porphyrin ring. However, in the dioxygen heme complex the oxygen molecule is bound to the iron atom, so that the valence electrons of the oxygen molecule interact with d-electrons on the iron atom. In other words, the p-electrons on the porphyrin ring provide the secondary field to the bonding character between the iron atoms and the oxygen molecule. Therefore, the electronic structure of the iron atom is expected to be determined primarily by the interaction between the d-orbitals and the s-type orbitals of the nitrogen atoms in pyrrol, with electron transfer from the iron atom to the nitrogen atoms. The four nitrogen atoms of the pyrrol rings formally have lone-pair electrons pointing to the iron atom with two positive charges. A situation similar to this electronic configuration may be realized simply by replacing the four pyrrol rings by four ammonia molecules with lone-pair orbitals. In order to confirm the above consideration, we carried out SCF calculations for the singlet states of the Fe–por complex with zero total charge and a Fe 2q–4NH 3 model system with two positive total charges using the Tatewaki–Huzinaga basis sets w26x for the Fe atom and the 3-21G basis sets w27x for the C, N and H atoms. The geometry of the Fe–por complex comes from the corresponding moiety to the binuclear active site of fully-reduced C cO w4x. In this model system, the positions of the nitrogen atoms of the NH 3 molecules correspond to those of the porphyrin ring and the lone-pair orbitals of NH 3 are directed to the Fe 2q atom. The singlet state of the Fe–por complex gives net charges of 1.313 on the Fe atom and y0.959, y0.980, y0.963, y0.986 on the four nitrogen atoms of porphyrin, while the Fe 2q–4NH 3 system gives 1.333 on Fe 2q and y1.034 on the four nitrogen atoms of the NH 3 . These values are in reasonable coincidence, indicating that the Fe 2q–4NH 3 system is applicable for presenting the reaction field for the reduction of the O 2 molecule. The imidazole rings of four histidine residues are also replaced by NH 3 molecules. This replacement is supported by theoretical works w14,15x on hemocyanin, where the histidine residues bound to binuclear copper atoms are replaced by NH 3 molecules. Though this reaction model wNH 3 –a 3 , Cu B –3NH 3 x is simple, the NH 3 molecules give an appropriate reaction field for a systematic investigation of the reaction. The spin states of the ground state of Fe 2q, Cu1q and the oxygen molecule are a quintet, singlet and triplet, 1q x respectively. Therefore, the ground state of w a 2q can have spin states such as singlet, triplet, quintet 3 rOOrCu B and septet. It is well known that the ground state of the dioxygen heme complexes in hemoglobin and 1q x myogrobin is a singlet w7–9x. Therefore, the ground state of w a 2q is also expected to be a singlet. 3 rOOrCu B However, triplet or higher spin states cannot necessarily be excluded; an examination of high spin states will be reported elsewhere. In geometry optimizations, the geometries and positions of the oxygen molecule were optimized. The ˚ corresponding to that in the binuclear active site of distance between the Fe and Cu atoms was fixed at 4.695 A, w x reduced C cO 4 . Recently, the three-dimensional structure of oxidized C cO was observed by an X-ray analysis and the dioxygen was found in the binuclear active site w28x. The distance between Cu B and Fe Žheme a 3 . of ˚ of reduced C cO by only 0.2 A˚ w4x. The small change in the oxidized C cO w28x is longer than the 4.695 A distance supports the idea that fixation of the binuclear distance in the geometry optimization is an assumption that is not far from the real system of C cO. The Tatewaki–Huzinaga ŽTH. basis set Ž5333r533r5. augmented by the p-type function with the same

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1q x Fig. 2. Optimized geometry of the singlet state of w a 2q 3 , O–O–Cu B .

exponents as the 4s-type function of the TH basis set w26x was employed for the iron and copper atoms. The 6-31G basis set w29x was used for the O 2 molecule and the 3-21G basis sets w27x for C, N and H atoms. All calculations were carried out using the program package GAUSSIAN 94 w30x.

5. Results and discussion 5.1. Structures of [a32 qr OO r Cu B1q ] 1q x The optimized geometry of the singlet state of w a 2q 3 , OO–Cu B , which corresponds to the first step of the reduction of the O 2 molecule, shown Eq. Ž2., is depicted in Fig. 2. Apparently, the oxygen molecule is bound to ˚ shorter than the distance of 2.310 A˚ between another oxygen atom and the iron Cu B with a distance of 1.865 A, ˚ which are longer than the atom of heme a 3 . The bond distances between the oxygen atoms are 1.359 A, ˚ for the ground triplet state Ž3 Sg . and the first excited singlet state experimental distances of 1.207 and 1.22 A Ž1D g . of O 2 , respectively. We carried out geometry optimizations of the triplet state of isolated CuOOq by UHF and UB3LYP using the same basis set for the copper atom and 6-31G ) w31x for the O 2 molecule. The UHF method gave 2.319, ˚ and 152.18 for RŽCu–O., RŽO–O. and /Cu–O–O, respectively, while UB3LYP gave 1.943, 1.221 A˚ 1.167 A and 127.18. In comparison with isolated CuOOq, the distance of Cu B –O is shorter and the distance of O–O is 1q x longer in the w a 2q model system of the binuclear active site in C cO. 3 , OO–Cu B Table 1 summarizes the charge and spin densities on the Fe, Cu and O atoms of the optimized 1q x 2q w a 2q –4NH 3 3 , OO–Cu B . The Fe atom has a charge density of 1.400, which is similar to 1.333 of the Fe

Table 1 1q x Charge and spin densities of optimized intermediates of w a2q 3 rOOrCu B Fe Charge densities 1 2q w a 3 , OO–Cu1q x B 1 2q w a 3 –OO, Cu1q x B 1 3q w a 3 –OOH, Cu1q x B Spin densities 1 2q w a 3 , OO–Cu1q x B 1 2q w a 3 –OO, Cu1q x B 1 3q w a 3 –OOH, Cu1q x B

O

O

Cu

H

1.400 1.674 1.641

y0.190 y0.664 y0.543

y0.610 y0.700 y0.680

1.180 1.141 1.141

0.502

0.009 1.212 y1.184

y0.936 y0.054 0.054

y0.027 y0.157 y0.005

0.847 y0.812 0.823

y0.000

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1q x Fig. 3. Optimized geometry of the singlet state of w a 2q 3 –O–O, Cu B .

model system. The copper atom has charge densities nearly equal to 1.0 and the oxygen atom near the copper atom has large negative charge densities. The up- and down-spins are localized on the copper atom and the oxygen atom near the iron atom, respectively, forming a singlet biradical structure. The electronic structure of 1q x w 2q OO–Cu1q is quite different from that of isolated CuOOq. B in a 3 , OO–Cu B 1q x Fig. 3 shows the structure of w a2q 3 –OO, Cu B , where the oxygen molecule is captured by the Fe atom of ˚ respectively, and also heme a3 . This structure has nearly equal Fe–O and Cu–O distances, 1.870 and 1.903 A, ˚ which is much longer nearly planar geometry with a dihedral angle of 163.28. The O–O distance is 1.468 A, than the distance of the O 2 molecule. A similar elongation has also been observed in the three-dimensional structure of oxidized C cO by the X-ray analysis w28x. Though the three-dimensional structure of the dioxygen binuclear complex in reduced C cO has not been observed yet, the structures of the por–Fe–OO complex were determined experimentally w32–34x and ˚ obtained here is slightly longer than the experimental 1.75 A˚ theoretically w9x. The Fe–O distance, 1.870 A, ˚ ˚ shown in Fig. 3 is much longer than w32–34x and theoretical 1.77 A w9x distances. The O–O distance, 1.468 A, ˚ the experimental and theoretical values of 1.24 and 1.30 A, which are comparable with that of molecular oxygen. The Fe–O–O angle of 117.48 shown in Fig. 3, is smaller than the experimental 1318 w32–34x and the theoretical 1218 w9x. Table 1 shows that the negative charge densities are largely localized on the oxygen atoms. This shows that the dioxygen bound to the Fe atom can capture electrons, which is consistent with the elongation of the O–O distance. Furthermore, this structure is expected to be easily protonated proceeding reduction to the H 2 O molecule. This structure corresponds to the singlet biradical state in which the spins are localized on the iron and copper atoms and the dioxygen loses the spins. The experimental and theoretical works w9,32–34x of the por–Fe–OO complex, which suggested that the Fe–O bond was formally described as Fe 3q–Oy, are not in 1q x harmony with our results for the Fe–O bond in the binuclear w a 2q system. 3 –OO, Cu B 5.2. Early stage of reduction of O2 Since the oxygen atoms have large negative charges, the next step to the reduction of the O 2 molecule is expected to be protonation of the dioxygen atoms. The proton channels to reduce O 2 to H 2 O in the active site are not yet well determined w5x. Tsukihara et al. w5x proposed that the hydrogen-bond network from Lys 265 to His 240 bound to Cu B , which involves helices VI and VIII of subunit I and heme a3 , is most likely to work as a channel for protons to form water molecules. However, they noted that this system cannot be excluded as a proton pump via the His 240 , Cu B and His 291 bound to Cu B . The pathway of the proton transfer to the active site is still uncertain. Under these circumstances, it seems possible to suppose that protonation and formation of

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1q x Fig. 4. Optimized geometry of the singlet state of w a 3q 3 –O–OH, Cu B .

H 2 O occurs without the aid of the surrounding species such as water molecules, because the water molecules are not detectable in the active site w5x. 1q x Fig. 4 shows the optimized protonated structures in the singlet state of w a3q 3 –OOH, Cu B . In the process of ˚ are increased by about 0.1 A, ˚ in protonation, the distances of Fe–O and Cu–O of 2.005 and 2.028 A 1q x comparison with those in the structure of w a2q –OO, Cu shown in Fig. 3. The two oxygen atoms are also 3 B 1q x ˚ of w a2q stretched from 1.468 to 1.487 A –OO, Cu . From Table 1, the charge densities of the iron atom 3 B 1q x changes to values slightly smaller than that of w a 2q 3 –OO, Cu B , indicating that the iron atom is formally 2q 3q described as Fe instead of Fe . The charge and spin densities on the Fe, O and Cu atoms of the protonated 1q x state both remain at nonprotonated w a 2q 3 –OO, Cu B . Fig. 5 indicates an energy diagram of the intermediates and the protonated state of the singlet state of 1q x 1q x 1q x w a 2q w 2q state is 28 kcalrmol higher than the w a2q state; therefore, 3 rOOrCu B . The a 3 –OO, Cu B 3 , OO–Cu B the reaction pathway that proceeds through the intramolecular transfer of dioxygen atoms in the binuclear active site seems unacceptable because of the activation energy of higher than 28 kcalrmol at least. The protonated 1q x 1q x w 2q state, w a 3q state by 2.1 kcalrmol, is also expected 3 –OOH, Cu B , which is more stable than the a 3 , OO–Cu B 2q 1q 1q x to be led from the w a 3 –OO, Cu B x state. It can be considered that the direct pathway from w a 2q to 3 , OO–Cu B 3q 1q the protonated state w a 3 –OOH, Cu B x corresponds to a cooperative process of intramolecular transfer of the dioxygen atoms in the binuclear active site and proton transfer to the binuclear active site, with an activation 1q x energy smaller than the pathway from w a 2q 3 –OO, Cu B . This means that an early stage of reduction of the O 2

1q x Fig. 5. Energy diagram of the singlet states of w a2q 3 rO 2 rCu B .

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molecule proceeds cooperatively with O 2 capture in the binuclear active site and protonation. This reaction mechanism proposed here is in coincidence with the conclusion extracted from the experimental results that the 1q x x w6,17,18x. rate constant to w a 3q is ten times larger than that to w a33q–Oy Oy, Cu1q 3 –OOH, Cu B B 6. Concluding remarks We have carried out ab initio MO calculations for the singlet state of a binuclear dioxygen complex, a model of the binuclear active site of cytochrome c oxidase ŽC cO.. The early stages of the reduction of the O 2 molecule to water molecules have also been investigated. The main conclusions for the structure of intermediates are: 1q x 1q x 1. Geometries of two intermediates, w a 2q and w a 2q 3 , OO–Cu B 3 –OO, Cu B , in the singlet state are allocated. 2q 1q x w Ž 2. In the a3 –OO, Cu B state, the dioxygen captures electrons ; 1.4 ey. has an elongated O–O distance by ˚ 1.468 A. 1q x 1q x 3. The protonated state w a 3q has electronic structures similar to w a 2q and the iron 3 –OOH, Cu B 3 –OO, Cu B 2q 3q atom can formally be described as Fe in stead of Fe . The main conclusions for the reaction mechanism of the early stage of the reduction of O 2 are: 1q x 1q x 1. The protonated state w a3q is more stable than the w a 2q state by 2.1 kcalrmol in 3 –OOH, Cu B 3 , OO–Cu B our reaction model. 1q x x by 28.0 kcalrmol; the reaction pathway of 2. The w a2q state is less stable than w a 32q, OO–Cu1q 3 –OO, Cu B B 2q x reduction through w a 3 –OO, Cu1q is unlikely due to its high energy barrier. B 3. The early stage of reduction proceeds through a cooperative process of intramolecular transfer of the dioxygen atoms in the binuclear active site and proton transfer to the binuclear active site. The present reaction model of the binuclear active site of reduced C cO is based on the evidence that the electronic structure of the iron atom in the Fe 2q–4NH 3 model system is similar to that of the Fe–por complex and the change of the binuclear distance between the reduced and oxidized forms is small w28x. Although this model seems to represent the essential feature of the binuclear active site, it might be too simple to be a workable reaction model. One of the problems for further consideration is the histidine residue connected to heme a3 . It is well known that the histidine residue plays an important role in the binding with molecular oxygen reversibly in the hemoglobin and myoglobin enzymes w7–9x, showing that the distance between the histidine and iron atom becomes an important factor even in C cO. The potential fields induced by the p-electrons spread over the porphyrin ring an another factor. In addition, our study is limited to the singlet state. Although higher spin states such as the quintet and septet may be ignored, the triplet state should be taken into consideration for the structures and reactions. These problems remain to be solved in further theoretical work on cytochrome c oxidase. Acknowledgements The authors thank Prof. Tsukihara for helpful and fruitful discussions on the three-dimensional structures of cytochrome c oxidase. This work has been supported by Grants-in-Aid for Scientific Research on Priority Areas ŽNo. 283, ‘Innovative Synthetic Reactions’ and No. 401, ‘Metal Assembled Complexes’. from the Ministry of Education, Science, Sports and Culture, Government of Japan, and by CREST ŽCore Research for Evolutional Science and Technology. of Japan Science and Technology ŽJST.. References w1x B.G. Malmstrom, Chem. Rev. 90 Ž1990. 1247. w2x G.T. Babcock, M. Wikstrom, Nature 356 Ž1992. 301. w3x S. Iwata, C. Ostermeier, B. Ludwig, H. Michel, Nature 376 Ž1995. 660.

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