Identity of Green Plant Reaction Centers from Quantum Chemical

1442

J. Phys. Chem. B 2001, 105, 1442-1451

Identity of Green Plant Reaction Centers from Quantum Chemical Determination of Redox Potentials of Special Pairs Sambhu N. Datta,* Priya V. Parandekar, and Rohini C. Lochan Department of Chemistry, Indian Institute of Technology - Bombay, Powai, Mumbai - 400 076, India ReceiVed: March 27, 2000; In Final Form: December 1, 2000

We have carried out quantum chemical computations on the special pairs of chlorophyll-a molecules so as to resolve the ambiguity of the large oxidation redox potential of P680 and establish the identities of P680 and P700 by comparing the calculated potentials with the observed ones. The methodology adopted here has been INDO. At first the oxidation potential of chlorophyll-a has been determined from the calculations on model structures prepared from the crystallographic structure of ethyl chlorophyllide-a dihydrate with variously truncated side chains. A good value of the oxidation potential is found only for structures that have most of the side chains and hydrogen-bonded water molecules intact. The calculated oxidation potentials are about 0.68 V in dichloromethane and 0.77 V in acetonitrile at pH 4.5 at 298.15 K. The calculated numbers are in good agreement with the observed values 0.74-0.86 and 0.76 V, respectively, for chlorophyll-a in these solvents. The intact structures have been used to form the special pairs. The pairs studied include the Shipman model, Strouse model, Svensson model, and a trial model. The new model for the structure of the special pair is a result of the synthesis of the basic chlorophyll-a structure and the optimum π-π interaction between two macrocycles facing each other, and it has been specifically studied to complete investigations on structures that, in principle, fill the gap between the Shipman model and the Svensson pair model. The theoretically determined redox potentials are: (1) 0.45-0.56 V for the Strouse model, 0.56-0.57 V for the Shipman model, 0.54 V for the Svensson dimer, 0.16 V for the trial model (dimer of monohydrates), and 0.34 V for the trial model (dimer of dihydrates) in the absence of a methionine neighbor; and (2) in the presence of a methionine electrostatically interacting with one of the chlorophylls, 0.97-1.08 V for the Strouse model, 1.07-1.08 V for the Shipman model, 1.05 V for the Svensson pair, 0.68 V for the trial model (monohydrate dimer) and 0.85-0.86 V for the trial model (dihydrate dimer). Comparing these values with 0.46-0.52 V for P700, one can identify P700 with all of the dimers except the trial dimer of chlorophyll monohydrates. Pigment P680 that has a redox potential of 1.1 V can be identified with the Strouse, Shipman, and Svensson pair models. Interaction with the surrounding dielectric medium and possible bare ions holds the key for the increase of the redox potential from its monomeric value. The formation of the Shipman model from two chlorophyll-a molecules is, in principle, not kinetically favored. The formation of the trial dimer from the mono- or dihydrates is not thermodynamically favored. A reexamination of the experimental spectroscopic data for P700 is necessary to decide whether the Svensson dimer (without the neighboring methionine) can qualify as P700. Hence the issue remains open. Relatively recent crystallographic data rule out water as a ligand of magnesium of the chlorophylls in P680 and thus discount the Strouse, Shipman, and trial models. Our INDO calculations show that the structure of P680 proposed by Svensson et al. from homology modeling successfully explains the abnormally large oxidation redox potential of this pigment.

Introduction The chemical structure of the reaction centers P680 and P700 in thylakoid sac in chloroplast has been the subject of intensive investigations during the past few decades. Photosystem I (PSI) is known to have P700, and PSII contains P680. It is possible to estimate the number of molecular species that are involved in the delocalization of electrons from EPR and ENDOR studies.1 The number of nuclei that participate in hyperfine interaction with the unpaired electron determines the EPR line width and the ENDOR splitting. The EPR line width decreases by a factor of x2, and the ENDOR spectrum splitting is halved when a symmetrical dimer is formed from two monomers. Although both P680 and P700 are believed to be dimers of chlorophyll-a (chl-a), it is thought that the electrostatic interaction with the surrounding protein moiety leads to an

unequal distribution of positive charge between the two monomers present in the cations of these reaction centers. As a result, the experimental line width and splitting vary considerably from the predicted values. The earliest models proposed for the reaction centers are due to Katz and Norris2 and Fong.3 Characteristics of the Katz and Norris model are as follows: (i) two chlorophyll-a (chl-a) molecules are held together by a water molecule; the oxygen atom coordinates to the magnesium of one chl-a and the hydrogen atoms are hydrogen bonded to the ring V keto CdO and the carbomethoxy CdO of the other monomer; (ii) the distance between the two monomer planes is greater than 3.6 Å, and so there will be a very small π-π overlap. The Fong model is very similar: (i) two water molecules hold the two chlorophylls together in a symmetrical way with each water molecule being coordinated to the carbomethoxy of the other;

10.1021/jp001139z CCC: $20.00 © 2001 American Chemical Society Published on Web 01/25/2001

Oxidation Redox Potentials of Four Special Pairs (ii) the molecule has C2 symmetry; (iii) the interplanar distance is 5.6 Å, much greater than 3.6 Å that is required for the π-π interaction. On the basis of the investigation of the crystal structure of ethyl chlorphyllide-a dihydrate, Chow et al.4 proposed an essentially planar model of the special pair. Each magnesium is displaced by 0.39 Å above the macrocycle plane on the same side of the carbomethoxy group. This model will be henceforth referred to as the Strouse model. In this model, the two chlorophyll molecules are on the same crystal plane and the separation between the two magnesium atoms is 8.859 Å. One of the hydrogen atoms of the water molecule attached to each magnesium is hydrogen bonded to the oxygen atom of the second water molecule, which is in turn hydrogen bonded to the carbomethoxy group of the same chl-a. The other hydrogen atom is hydrogen bonded to the ring-V CdO of the second chla. One of the most celebrated models for chlorophyll reaction centers, especially P700, has been that of Shipman et al.5 The Shipman model was put forward to explain the visible and infrared spectra of the pigment. It has the following structural features: (i) two chl-a are held together with C2 symmetry by two water molecules, each of which is coordinated to magnesium of one chl-a and hydrogen bonded to the ring-V CdO of the other chl-a; (ii) the Mg-Mg distance is 8.9 Å and the interplanar distance is about 3.6 Å; (iii) the Mg‚‚‚O(H2) distance is 2.1 Å; the >C)dO‚‚‚H-O(H hydrogen bond system is linear and along one of the available sp2 directions of the CdO; the O-O distance is about 2.7 Å; (iv) most importantly, the magnesium atom of each chl-a is on the side of the macrocycle plane opposite to the carbomethoxy group, which facilitates the two macrocycle planes to stack in close proximity. This model is basically derived from the crystal structure studied by Chow et al.4 with two deviations: (i) in Shipman’s model the carbomethoxy group and the Mg atom are on opposite sides of the macrocycle plane, whereas the structure of chlorophyll-a crystal shows the Mg atom to be on the same side of the carbomethoxy group; and (ii) the two macrocycles are not stacked by crystal translation but with C2 symmetry. Both the Strouse and Shipman models were based on experimental observations, giving rise to a debate about possible water molecules bridging the chlorophyll dimers. Electron crystallography investigations of Ku¨hlbrandt et al.6 indicated the absence of bridging water molecules in P680. To our knowledge, the most successful model of PSII is the one of Svensson et al.7 This involves a histidine ligand attached to the magnesium in each chlorophyll belonging to a weakly coupled chl-a pair (P680), and was constructed by homology modeling using molecular mechanics calculations. The predicted centerto-center distance in the pair is 10.1 Å, which is somewhat larger than that predicted by the Shipman model. The two macrocycle planes are parallel to each other, and the distance between them is 3.4 Å. The angle between the Qy transitions is 152°. The Svensson model is consistent with a variety of experimental data.7 These structures, or structures very similar to them, would be undoubtedly formed in some of the green plant reaction centers. Therefore we have carried out a semiempirical quantum chemical investigation on them. However, we have also included in our studies a simple model that has been apparently overlooked so far. The macrocycle π-π interaction and overlap are hindered when the magnesium is on the same side of carbomethoxy group, mainly because the carbomethoxy group is hydrogen bonded to a water molecule in the vertical direction

J. Phys. Chem. B, Vol. 105, No. 7, 2001 1443 as revealed by the crystal structure analysis of Chow et al. The crowding is extensively reduced in case the two macrocycle planes are shifted and rotated relative to each other so as to generate the Mg-Mg distance 8.9 Å; the macrocycle plane separation is 3.6 Å and yet shows the least crowding effect. This model was included in our calculations in order to complete the investigation of possible alternative structures. It is worthwhile to mention here that from calculations based on atomatom potentials, Kashiwagi et al.8 concluded that the structure of the special pair would be close to, but not necessarily identical with, that proposed by Shipman et al. The new model in principle fills the gap between the Shipman model and the Svensson pair model. It looks somewhat like the Shipman model, but it is without the nuances of the latter. It can also be regarded as an alternative to the Svensson pair in the sense that the relative orientation of the second chl-a is different in the two cases. The experimental information that has relevance to this work is as follows. The oxidation potential of chl-a in acetonitrile is 0.76 V vs NHE, and it is 0.74-0.86 V for dichloromethane as solvent.9 The reduction potential of chl-a+ (≈ -0.8 V) is hence much lower than the oxidation redox potential of water (0.940.99 V vs NHE at pH 4-5 in the thylakoid). The difference of the oxidation and reduction potentials of chl-a is about 1.8 V. The pigment P680 has an oxidation redox potential of 1.1V vs NHE.10 In fact, this pigment is known to oxidize water in PSII via the mediation of other complexes. This observation led to a controversy as to whether P680 is a monomer or a dimer of Chl-a.11 Ordinarily, dimerization causes an increase of the oxidation potential and a lowering of the redox potential by an equal amount. If P680 is a monomer, it must be under a strongly oxidizing condition such as possessing an electron donor group. However, this would have been unusual and would have been detected by experiments such as EPR.11 A possible solution of the P680 puzzle is as follows: If P680 is a dimeric form of chl-a, the dimer must be more or less as stable as the two monomers, and the two macrocycles must be held together by weak bonding. This is achievable from π-π interaction. The surrounding protein moiety can stabilize the dimer by directly interacting with it, and it can also prevent the separation of the two monomers. This is in agreement with the electron diffraction data of Ku¨hlbrandt et al.6 In any case, the stability of the dimer cation relative to the neutral dimer is normally greater than the stability of the monomer cation relative to the neutral monomer. Therefore, the destabilization of the dimer cation which is so necessary for increasing the P680+/P680 redox potential, even making it positive, remains to be explained. This argument is also valid for P700, which is unambiguously known to be a dimer and has a redox potential ranging from 0.46 to 0.52 V.11 A summary of more recent experimental information is given here. Vrieze et al.12 have investigated the structure of the reaction center of PSI of plants by linear-dichroic absorbance detected magnetic resonance in zero magnetic field. The orientation of the Qy transition moment indicated different environments for P700 and chl-a. The pulsed EPR analysis of PSI single crystals by Bittl et al.13 shows two possible locations of phylloquinone within the electron-transfer chain. These two positions are related to each other by the pseudo C2 symmetry of the chlorophyll cofactors. Mac et al.14 have investigated the monomeric spin density distribution in the primary donor of PSI. Their estimate of the perpendicular center-to-center distance in P700+ is 3.8 ( 0.5 Å. Morris et al.15 have investigated the PSII core complex by electron crystallography. They confirm the dimeric nature of the complex, each monomer containing

1444 J. Phys. Chem. B, Vol. 105, No. 7, 2001 five domains. Hydrophobic loops of CP47 and CP43 form the extensive proteinaceous protrusions from the lumenal surface. The location of these loops indicates their possible involvement in the water-splitting process. Rhee et al.16 have carried out electron crystallography of the three-dimensional structure of the plant PSII reaction center at 8 Å resolution. These authors have found a PSII subcomplex containing the core complex and proteins D1, D2, CP47, and cytochrome b-559. The subcomplex can take part in light-mediated energy and electron transfer, but it is unable to oxidize water. Using electron microscopy and single particle analysis at 30 Å resolution, Nield et al.17 have discussed the positioning of the oxygen evolving complex proteins over the lumenal surface. With this background, we have determined the oxidation redox potentials of four special pairs, viz., the Strouse model,4 the Shipman model,5 the Svensson model,7 and the trial model, by theoretical (quantum chemical) means. First, of course, we have investigated the oxidation potential of chl-a. In an earlier work on the determination of the spectroscopic STS transition energy by the quantum chemical method,18 we showed that the calculated result becomes progessively better as one takes into account the substituents of the macrocycle in a systematic way. Here, too, we have found that the oxidation potential of chl-a can be explained only when the substituents are taken into consideration as completely as possible. A reasonably truncated phytyl chain of the monomer species has been used to form the dimer models. The theoretically determined dimer oxidation potentials lead us to identify the possible structures for P700 and P680. Method of Calculation Methodology. We have adopted the INDO/2 MOSCF methodology as discussed by Pople and Beveridge.19 This method is also retained in Gaussian 92 on Windows (G92W).20 The main body of the calculation was performed with our INDO program which had been modified in two ways. The first modification involves the inclusion of the second-row elements in the INDO calculation. While the exchange integrals had not been optimized for the second row elements, the major part of the exchange effects are reproduced by retaining the empirical values for G1 and F2 for the first-row element belonging to the same group. With this tactic, the INDO total energy would be in error only in the third place of decimal (in hartree) that implies a 5-digit accuracy for the involved systems, and when we compare the two total energies for reactants and products, the error in the energy difference would occur at most in the fourth decimal place. This error is less than the order of the limit of accuracy of the results expected from the INDO/2 method. The second modification involved the estimation of medium polarization effects in terms of the Born energy of ion-medium interaction and Onsager’s energy of dipole-reaction field interaction. The general principles involved were discussed in detail by Newton,21 who used a self-consistent modified continuum model for the medium that contains a solvated ion (electron). A similar self-consistent procedure gives rise to the self-consistent reaction field (SCRF) treatment for the interaction of a molecular dipole with the reaction field. Thus, the solute dipole polarizes the medium, the polarized medium in turn creates the reaction field at the center of the solute molecule, the solute dipole interacts with this electric field, and the Hartree-Fock equations are solved in such a way that the reaction field becomes self-consistent. Then the net stabilization of the solute-solvent system is evaluated. The G92W program has an option for the SCRF treatment, but there is a severe

Datta et al.

Figure 1. Structure of the dihydrates of chlorophyll-a, ethyl chlorophyllide-a and the modified structure for taking the effect of the phytyl chain into consideration.

restriction on the size of the molecule. The other method of accounting for the interaction with the medium is to include some aspects of the medium, such as the force field,22a fractional charges representing the molecules in the medium,22b etc., explicitly in the quantum chemical calculation. Because some of the molecules under investigation can be considerably large, even for the INDO calculation, we considered the medium as a dielectric continuum. Our program improvement was described elsewhere.23 In the present work, however, we have directly calculated the Born energy correction and the Onsager term,

EBorn ) -

Q2 1 12a0

(1)

( - 1) µ2 , (2 + 1)a30

(2)

(

)

and

EOnsager ) -

by using the results of the computations on the unsolvated species representing chlorophyll-a and special pairs. In the above, Q is the total charge, µ is the ground-state dipole moment calculated for the isolated species, and is the dielectric constant of the medium. The software G92W20 was used to compute the Onsager radius a0 and the total thermal energy. It was also used to perform the SCRF calculations on the small molecules H2, H2O, H3O+, and H5O2+. The reason for our adopting the INDO method for computation is as follows. The redox potentials involved correspond to energy differences of the order of 10-2 hartree. From our previous work,23,24 we have always found that the INDO method generates the tiny energy difference in excellent agreement with the observed potentials. This happens because of the parametrization scheme in this semiempirical theory, which indirectly admits the effects of electron correlation so as to generate reliable thermochemical properties in the ground state. A more theoretical procedure such as AM1, PM3, or an ab initio calculation will require not only a vast computing effort at the Hartree-Fock level but also extensive post-Hartree-Fock considerations in order to achieve a meaningful comparison with

Oxidation Redox Potentials of Four Special Pairs

J. Phys. Chem. B, Vol. 105, No. 7, 2001 1445

Figure 2. Different truncated forms of chlorophyll-a: (a) chl 45, (b) chl 48, (c) chl 88, (d) chl 89, (e) chl 91, and (f) chl 92.

the observed values, whereas more empirical techniques such as the extended Hu¨ckel and CNDO/2 methods are just not accurate enough. The largest species investigated here have 184 atoms and 494 valence orbitals. For more or less the same reasons, Hanson25 has used the INDO/s method to obtain reliable transition energies of chl-a, and the reported values turned out to be better than those calculated ab initio.26 Similarly, Plato et al.27 have used the restricted Hartree-Fock INDO spin polarization method to calculate the isotopic hyperfine coupling constants of the radical anion of chl-a. Chlorophyll. Atomic coordinates available from the crystallographic analysis of ethyl chlorophyllide-a dihydrate4 were retained in this work with minor alterations. See Figure 1 where we explicitly show the variation of the substituent R for chlorophyll-a, ethyl chlorophyllide-a and a more realistically modified structure. Because the chlorophyll molecule has many substituents, we have considered differently truncated structures for this molecule. These are shown in Figure 2 as they are visualized from different directions, with an effort to make the differences in the substituents as vivid as possible. The atoms involved in each diagram have crystallographic coordinates. Figure 2a shows the smallest possible entity that has the macrocycle with only hydrogen atoms as substituents, the magnesium atom and the water molecule hydrogen bonded to the magnesium. There are 45 atoms, and the species is called here as chl 45. Figure 2b shows chl 48 that has the second water molecule in its crystallographically determined position. Figures 2c and 2e similarly differ by the absence or presence of the second water molecule, as do Figures 2d and 2f. With R ) -CH2CH2COOCH2CH3, Figure 2c and Figure 2e show ethyl-

chlorophyllide-a monohydrate (chl 88) and ethylchlorophyllide-a dihydrate (chl 91), respectively. It would be useful to compare these diagrams with the structure in Figure 1. The structure chl 91 is identical with the C37 structure in Figure 1 of ref 4. It has the ethyl group in the place of the phytyl chain. The same group is present in chl 88, but the second water molecule (hydrogen bonded to the ring V ester substituent) is missing from this structure. To maintain the main effect of the phytyl chain, we have replaced the group R in Figure 1 by -CH2CH2COOCH2CHdCH2 to get chl 89 and chl 92 (the modified structures). The latter are shown in Figure 2d and Figure 2f, respectively. Coordinates of the -CHdCH2 atoms were calculated by using standard bond lengths and bond angles (C4C3 1.52 Å; C3-C3 1.46 Å; C3-H 1.08 Å; C3 angles 120°). In this work we also deal with chl 86 that can be obtained from chl89 or chl92 by removing the water molecules. It would be discussed later that the redox properties of chl-a are best reproduced by the structure chl 91 determined by Chow et al. and its updated version chl 92. These structures were used in this work to prepare the geometry of the possible dimers. The Strouse Dimers. The Strouse dimers, called here Strouse 91 and Strouse 92, were prepared from the monomers chl 91 and chl 92 respectively, by considering a crystal translation of 8.859 Å along the x-axis as suggested by Chow et al.4 So, except for the -CHdCH2 group representing the phytyl chain in chl 92, the crystallographic positions of atoms were maintained to obtain the two Strouse models of reaction center (Figure 3). The Shipman Model. The preparation of the other three models is a more demanding task. It involved a few common steps and a few specific final steps. The steps are as follows:

1446 J. Phys. Chem. B, Vol. 105, No. 7, 2001

Datta et al.

Figure 3. The Strouse model: (a) Strouse 91 and (b) Strouse 92. Figure 4. The Shipman model: (a) Shipman 91 and (b) Shipman 92.

1. Coordinates of the atoms belonging to the first (lower) monomer are calculated relative to the geometrical center of the four nitrogen atoms. 2. All of the atoms of the first chl-a are rotated through angle γ around the z-axis, then through angle β around the y-axis, and finally through angle R around the x-axis so as to bring the macrocycle to the xy-plane. The last task has been accomplished with R ) 54.0°, β ) 22.6°, and γ ) 9.5°. The z coordinates of the magnesium atom are found to be (0.0068, 0.0051, 0.3821) in Angstroms. 3. For the Shipman model: (a) The y and z coordinates of all atoms of chl-a except those of the group Mg‚‚‚OH2 are inverted (y f -y, z f -z), whereas only the y coordinates of the OH2 atoms are inverted (y f -y); the coordinates of magnesium remain unchanged. This procedure gives rise to a structure with the water molecule hydrogen bonded to magnesium and the carbomethoxy group on the opposite sides of the macrocycle; besides the HB of the water molecule (ref 4) will be eventually hydrogen bonded to the keto oxygen of ring-V of the second chlorophyll. (b) Initial coordinates of the atoms belonging to the second (upper) chl-a are prepared from the respective atomic coordinates of the first (lower) chl-a by the transformation (x, y, z) f (c1 - x, y, c3 - z), where c3 ) 3.6 and c1 ) 8.4226 in Angstroms. This yields a separation of 3.6 Å between the macrocycle planes with Mg-Mg distance 8.9 Å as suggested by Shipman et al.5 (c) All atoms of the first chl-a are rotated through angle φ in the xy plane around the magnesium atom of the first monomer, and all atoms of the second chl-a are rotated through angle -φ in the xy plane around the magnesium atom belonging to the second monomer. We find for φ ) 6.7° the following typical bond lengths and bond angles: O6(lower)-O1(upper) 2.7061 Å; O1(upper)-HB(lower) 1.7963 Å; C(upper)-O1(upper)-HB(lower) 131.52°; O1(upper)HB(lower)-O6(lower) 154.90°. The Svensson Pair Model. Steps (1) and (2) for the construction of the Shipman model were repeated for the species chl 86. For simplicity, the histidine ligands were not taken into account. Coordinates of the atoms belonging to the second (upper) chl-a were prepared as follows. (a)All atomic coordinates for the first (lower) chl-a are rotated through 180° around an axis on the xy-plane which subtends an angle of -14° onto the x-axis.

b)All the atoms are then translated along the y-axis through the distance R. c)All the z-coordinates are increased by 3.4 Å. For R ) 9.76 Å, we find the Mg-Mg distance of 10.1 Å. By construction, the y-axes of the two macrocycles make an angle of 152° with each other, and the two macrocycle planes are separated by 3.4 Å. The Trial Model. Steps 1, 2, 3(b), and 3(c) of the construction of the Shipman model [but not step 3(a)] were repeated. This model has basically the crystallographic structure for each monomer with the concerned water molecule(s) and the carbomethoxy group on the same side. This gives rise to a lot of crowding that is minimized when φ ) 19.0°. We find the following bond lengths and bond angles: O6(lower)-O1(upper) 5.42 Å; O1(upper)-HB(lower) 4.49 Å; C(upper)-O1(upper)HB(lower) 99.14°; O1(upper)-HB(lower)-O6(lower) 159.79°. Again in this model, atom HB and not HA is closer to the ring-V keto oxygen of the other chlorophyll, but the hydrogen bonding is necessarily very weak. By construction, the Shipman model (Figure 4), the Svensson pair (Figure 5) and the Trial models (Figure 6) all have C2 symmetry, whereas the Strouse model (Figure 3) relies on the symmetry of crystal translation. Table 1 gives a summary of the characteristics of these models. Difficulties in Computation. Although the task set in the Introduction seems to be straightforward, the species investigated are so large that in nine out of ten cases the INDO calculation leads to divergent or oscillatory total energies in the SCF loops. For the monomeric species, however, the cation calculation is always found to be convergent. Therefore, we have resorted to the following tactics. The neutral monomers have been successully investigated by starting with an initial density matrix. The latter was prepared by multiplying the density matrix of the cation by the factor N/(N - 1) where N is the number of valence electrons in the neutral monomer. The dimer calculations have been more complicated. Each 92-dimer consists of 184 atoms and 494 valence orbitals. Each dimer cation has been investigated by using an initial density matrix that was prepared from the monomer cation density matrices by following the stated method, the multiplicative factor in use being (2N - 1)/(2(N 1)). The computed density matrix of the cationic dimer has been



Figure 6. The trial models: (a) Trial 91 and (b) Trial 92. The monohydrate-dimers Trial 88 and Trial 89 are obtained by removing the second water molecule from each monomeric part of Trial 91 and Trial 92, respectively.

Figure 5. The Svensson pair model, based on Chl 86. Histidine ligands have not been included in this work.

similarly updated by the factor 2N/(2N - 1) and used to start the calculation on the neutral dimer. Atomic coordinates of the molecules H2, H2O, H3O+, and H2O‚H+‚H2O have been optimized by G92W, and then the respective dipole moments have been calculated by executing our INDO program.23,28 Computed Results and Discussion At first we set the INDO ∆G° for the dissociation of hydrogen molecule followed by ionization of hydrogen atoms and solvation of protons,

1/2H2(g) f H+(aq) + e-(g)

(3)

INDO results for the optimized geometries of H2, H2O, H3O+, and H2O‚H +‚H2O are given in Table 2. If we use these results (the total energy column in the same table), we get, neglecting the negligibly small (PV-TS) contributions,

1/2H2(g) + H2O(aq) ) H3O+(aq) + e-(g) ∆G° ) 0.2137 au (4) The calculated ∆G° value includes contributions from the INDO energy of the species, the solvation energy in the form of the Born energy correction and the Onsager reaction-field correction (from the SCRF treatment), and the thermal energy. The thermal energy of the electron is purely kinetic (3/2RT) and very small at room temperature. Other (PV-TS) terms are also very small29 and they have been neglected. However, the ∆G° calculated for process 4 represents an overestimation of the ∆G° for the overall process 3, because the proton polarizes strongly and it

can be coordinated to more than one water molecule. In fact, it is well-known that a hydrogen ion can rapidly transfer from H3O+ to another water molecule. This indicates the formation of another solvated complex as

1/2H2(g) + 2H2O(aq) ) H2O‚H+‚OH2(aq) + e-(g) ∆G° ) 0.1191 au (5) This process does not occur to the complete extent. The nature of the aquated proton oscillates from H3O+ to H2O‚H +OH2, and so the INDO ∆G° for reaction 3 is taken as the average of the INDO ∆G° values calculated for the processes 4 and 5. Although this is an approximation, it should yield a reasonably correct estimate. In fact we find the average ∆G° ) 0.1664 au (4.529 eV). The experimental value is 4.479 eV,30 and the INDO average is accurate to within 2% of the observed change in free energy. Computed molecular characteristics for different truncated forms of chl-a are given in Table 3. It is clear that a large-scale truncation yields a grossly incorrect ionization energy for the isolated chl-a molecule. Converged results are obtained only with structures containing most of the side chains intact. Therefore, only the forms chl 88, chl 89, chl 91, and chl 92 have been used for the calculation of the oxidation potential of chl-a in dichloromethane (dielectric constant ) 9.08) and acetonitrile ( ) 37.5). The calculation of free energy change requires the INDO energies, the Born corrections, the Onsager corrections, and the difference between the thermal energy of the neutral species and that of its cation. The G92W software could not perform normal-mode analysis for these bulkier species. Hence we have calculated the thermal energy for chl 45 (289.622 Kcal mol-1) and its monopositive cation (288.916 Kcal mol-1) at 25 °C and used the difference -0.706 Kcal mol-1 (-0.0306 eV or -0.00113 au) in the calculation of ∆Ethermal for the oxidation of each form. As it can be seen from Table 4, the calculated values of the oxidation potential of chl-a in these two solvents (dichloromethane: 0.68 V; acetonitrile: 0.77 V)


Datta et al.

TABLE 1: Characteristics of the Model Dimers model

constructed bondsa

geometry

Strouse

crystallographic geometry of ethyl chlorophyllide-a dihydrate (ref 4)

Shipman

dimer geometry based on the proposal in ref 5. Symmetry: C2. Methyl carboxylate chain of each ring is on the other side of Mg(H2O).

Mg(l)-Mg(u) 8.9 Å; O6(l)-O1(u) 2.71 Å; HB(l)-O1(u) 1.80 Å; HB(l)-O1(u)-C(u) 131.5o; O6(l)-HB(l)-O1(u) 154.9°; interplanar distance 3.6 Å.

Svensson

crystallographic geometry of ref 6 and homology modeling of ref 7. Symmetry: C2.

Trial

dimer geometry prepared by synthesizing the important points of Fong model (ref 3) and Shipman’s model (ref 5). Symmetry: C2. Methyl carboxylate chain of each ring is on the same side of Mg (H2O) just as it is in chl-a.

Mg(l)-Mg(u) 10.1 Å; interplanar distance 3.4 Å; the y axes are inclined to each other at 152o; (Mg has histidine ligand in place of water). Mg(l)-Mg(u) 8.9 Å; O6(l)-O1(u) 5.42 Å; HB(l)-O1(u) 4.49 Å; HB(l)-O1(u)-C(u) 99.1o; O6(l)-HB(l)-O1(u) 159.8°; interplanar distance: 3.6 Å.

a

other characteristics With the second monomer translated 8.859 Å from the first one along the x-axis Chiefly bounded by the interaction of the π densities of the two macrocycles, and also by H-bonds. The price to pay is the energy required to twist the methyl carboxylate substituent to the other side. So this dimerization can take place only in the controlled environment of the condensed phase. Fe2+ ion is 28.3 Å away from ChlD1,P680 and 28.2 Å away from ChlD2,P680. D1 Met 183 interacts electrostatically with ChlD1,P680. Bounded by the interaction of the π densities on both the macrocycle planes. The dimerization process is endothermic, so it can happen only in the controlled environment of the condensed phase where direct bonding interaction with other molecules can lead to an overall stability.

The letter l (u) indicates the lower (upper) monomer.

TABLE 2: G92W INDO Results for the Optimized Geometries of the Respective Species molecule

INDO energy (au)

Onsager radiusa (Å)

dipole moment (D)

hydration energyb (au)

thermal energyc (Kcal mol-1)

total energy (a.u.)

H2 (g) H2O (aq) H3O+ (aq) H5O2+(aq) e-(g)

-1.4747 -19.0394 -19.4679 -38.6253 0.0

2.42 2.46 2.88

0.0 2.14 0.0 0.0 0.0

-0.0036 -0.1062 -0.0906

9.929 19.70 28.47 50.79 0.889

-1.4589 -19.0116 -19.5287 -38.6350 0.0014

a This includes 1.04 Å contribution from the first hydration layer. b This includes the Born energy correction and the Onsager energy correction. Dielectric constant of water ) 78.5. c Used T ) 298.15 K.

TABLE 3: Molecular Characteristics of Chlorophyll-a from INDO Calculations INDO total energy in a.u.

molecular dipole moment in Debye radius (Å)c neutral cation

E(neutral)

[E(cation) E(neutral)]

-243.7038 -262.1407 -422.3524 -434.6369 -441.3533 -453.3018 -460.0182

0.2162 0.2400 0.1781 0.1681 0.1682 0.1666 0.1667

5.48 5.59 6.50 6.55 6.60 6.61 6.65

Shipman 91b -453.2841 Shipman 92b -460.0004

0.1673 0.1674

6.61 6.65

truncated froma Chl 45 Chl 48 Chl 86 Chl 88 Chl 89 Chl 91 Chl 92

7.381 7.268 8.755 6.406 7.219 10.66 8.840 9.799 8.750 10.15 8.615 8.001 8.491 8.275 9.901 10.89 10.02 11.43

a Truncated from the crystallographic geometry in ref 4: chl 89 and chl 92 have -CH2-CHdCH2 group in place of ethyl group in the ester linkage. b Shipman monomers with 91 and 92 atoms. c Computed radius contains a contribution from the aqueous sheath (G92W).

are in good agreement with the experimentally determined values.9 The slight differences can be ascribed to (i) the INDO parametrization, (ii) the existence of the ethyl or the allyl group in the structures studied in place of the phytyl chain in chl-a, (iii) adoption of the crystallographic molecular structure, and (iv) the neglect of PV and entropy contributions. We emphasize here that it is extremely difficult to attain such an agreement between the computed numbers and the observed values of so small an energy difference for these large species by any other method. The INDO method was designed to generate good

values of the changes in thermochemical properties and this fact is borne out by the results presented in this work. In all of these calculations, we have taken the kinetic energy of the free (gaseous) electron into account and neglected its entropy. Because the same value has been adopted for the oxidation of gaseous hydrogen, there is no error in the calculation of the oxidation potential, a quantity that is conventionally measured relative to the hydrogen electrode. Empirical considerations lend credence to the belief that the LUMO-HOMO energy gap gives a measure of the difference between the reduction and the oxidation potentials of the neutral species. In a nonempirical treatment, the comparison fails because of correlation effects and very large solvent effects. The energy gap and the redox difference are only of the same order of magnitude, but the latter is usually about three to four times smaller. The LUMO-HOMO gaps computed for different species are shown in Table 5. These are comparable to the gaps computed ab initio for a model of chlorophyll-a by Petke et al,31 but they vary considerably from the observed redox difference for chl-a, 1.77 V.9 The calculated gaps are somewhat larger than the INDO ionization energies for the isolated systems as given in Tables 3 and 4. The ab initio ionization energy is in general much larger at the Hartree-Fock level, for a very wellknown reason. Indeed, Kashiwagi et al.8 found from their ab initio calculations the inoization energy of 6.16 eV or 0.2264 au for the chlorophyll-water system. The INDO ionization energies (∼0.1666 au) ultimately lead to the calculated oxidation potentials in Table 4. The calculation of the reduction potential



TABLE 4: Calculation of the Oxidation Potential of chl-a structure solvent: dichloromethane ( ) 9.08) Chl 88 Chl 89 Chl 91 Chl 92 solvent: acetonitrile ( ) 37.5) Chl 88 Chl 89 Chl 91 Chl 92 c

∆E (INDO) in eV

∆Esolv in eV

∆E(total) or ∆G°exb in eV

∆G°ox - 1/2∆G°ox(H2) in eV

Eox (at pH) 4.5) in V 0.74-0.86c

4.5752 4.5782 4.5333 4.5362

-0.9949 -0.9949 -0.9600 -0.9602

3.5883 3.5913 3.5813 3.5839

-0.941 -0.938 -0.948 -0.945

0.675 0.672 0.682 0.679 0.76c

4.5752 4.5782 4.5333 4.5362

-1.0890 -1.0893 -1.0496 -1.0501

3.4942 3.4969 3.4917 3.4941

-1.035 -1.032 -1.037 -1.035

0.769 0.766 0.771 0.769

a The reaction investigated is chl-a (aq.) f chl-a+ (aq.) + e-(g). b Includes ∆Ethermal ) 0.0079 eV and neglects the small (PV-TS) contribution. At pH ) 4.5, ref 9.

TABLE 5: LUMO-HOMO Energy Gap Computed for the Chlorophyll-a Molecule Energy gap in a.u. truncated form

R spin

β spin

Chl 45 Chl 48 Chl 88 Chl 89 Chl 91 Chl 92

0.2519 0.2716 0.2374 0.2374 0.2372 0.2372

0.2519 0.2694 0.2445 0.2445 0.2449 0.2449

TABLE 6: Energy Differences Computed by the INDO Method for the Dimers of the Selected Species

model

dimer binding energya in Kcal mol-1

E(dimer cation) E(neutral dimer) in a.u.

Strouse 91 Strouse 92 Shipman 91 Shipman 92 Svensson 86 Trial 88 Trial 89 Trial 91 Trial 92

29.57 52.51 71.95 71.95 49.32 -20.32 -20.58 -101.92 -102.13

0.1521 0.1565 0.1641 0.1643 0.1755 0.1530 0.1530 0.1577 0.1578

a

Relative to the energy of the two isolated monomers.

of chlorophyll-a is a more demanding task, and the details of it will be communicated elsewhere. On the basis of these findings, one may reasonably expect that the identity of the special pairs can be investigated by considering the dimers of the less truncated species. Oxidation potentials have been theoretically determined for the dimers Strouse 91, Strouse 92, Shipman 91, Shipman 92, Svensson 86, Trial 88, Trial 89, Trial 91, and Trial 92. The INDO calculation on the Trial 86 dimer failed to converge. Energy differences computed for these dimeric species are given in Table 6. The dimer binding energy is positive for the Strouse dimers, the Shipman dimers and the Svensson dimer, that is, in these cases dimerization stabilizes the pair of monomers. The trial dimers are less stable compared to the isolated monomers, indicating that these dimers will be formed only in a favorable environment where the monomers are located proximate to each other and the dimers are stabilized by possible direct interaction with the neighboring molecules. Thus, although the trial dimers are somewhat less stable compared to the separated monomers, their formation in a condensed phase cannot be ruled out. This finding agrees with the observation of Sakuma et al.32 who, from their ab initio molecular orbital calculation on the chlorophyll dimer

with structure typical of the dimer in Rh.Viridis, found the dimerization energy to be unfavorable by about 16.1 Kcal mol-1. The dimers of the monohydrates, Trial 88 and Trial 89, have INDO binding energy only about -20 Kcal mol-1, and these species can easily gain an overall stability if they are directly linked to the surrounding protein fold. In comparison, the formation of the Shipman dimer from chl-a requires each monomer or the combined system to cross a relatively high energy barrier. The replacement of the ethyl group (in ethyl chlorophyllidea) by the allyl group (that yields R in the modified structure for chl-a in Figure 1) causes only minor alterations in all of the molecular properties. Table 3 as well as Tables 6 and 7 show that for both monomers and dimers, the INDO ionization energy and the Onsager radius slightly increase by this substitution. The dipole moment of the neutral species slightly decreases except in the case of the Shipman monomer (Table 3). The dipole moment of the cationic species increases except in the case of the Shipman dimer (Table 7). The net effect is to cause a tiny decrease of the calculated monomer oxidation potential. This is manifest in Table 4. Other molecular properties of the dimeric species are given in Table 7. These have been used to calculate the oxidation potentials of the possible special pairs in vivo. Following our previous work,24,28,33 we have assigned the dielectric constant 8.5 to the condensed phase of photosystems. Table 7 also shows the HOMO-LUMO gaps. In almost all of the cases, the gap has decreased from the value for the corresponding monomer. The calculation of the oxidation potential of the model dimers at the physiological pH (pH ) 7.0) is shown in Table 8. The INDO calculation indicates that, relative to the corresponding neutral species, the cations of the Strouse dimers and those of the Trial dimers of the monohydrates are the least unstable, and the cation of the Svensson dimer is the most unstable (Table 6). This trend would have resulted in a greater oxidation potential of the Strouse dimers and a considerably small potential for the Svensson dimer. However, in the Strouse model, the neutral dimers have large dipole moments and the dimer cations have much smaller dipole moments. The trend is exactly opposite for the dimers of C2 symmetry, namely, the Shipman, Svensson, and Trial dimers (Table 7). Because all of the dimers have more or less the same molar volume, the stability achieved by the dimer cations relative to the corresponding neutral species, from its interaction with the polar environment of the condensed phase, is lowest for the Strouse model and highest for the Svensson pair. See ∆E (medium interaction) in Table


Datta et al.

TABLE 7: Other Relevant Molecular Properties of the Dimeric Speciesa model dimer

dipole moment (D) neutral cation


19.27 19.21 9.949 9.750 12.46 3.351 3.186 5.392 5.201

Onsager radius b Å

2.493 3.652 15.04 14.99 31.21 17.73 18.19 16.10 16.30

8.33 8.38 8.33 8.38 8.19 8.25 8.32 8.33 8.38

E(LUMO) - E(HOMO) (a.u.) R spin β spin 0.2112 0.2111 0.2086 0.2085 0.2387 0.1992 0.1991 0.2069 0.2058

0.1834 0.1833 0.1883 0.1882 0.2428 0.1824 0.1823 0.1832 0.1830

a The LUMO-HOMO gap is shown for the neutral dimer. b This has been taken as 21/3 times the monomer radius, and used for the calculation of the Onsager stability and the Born interaction energy.

TABLE 8: Calculation of the Oxidation Redox Potential of Different Model Dimersa ∆Etot (eV) including systemb

∆EINDO (au)

∆Emedium interaction (au)c

thermal energyd

Fe2+ effect

methionine effect


0.1521 0.1565 0.1641 0.1643 0.1755 0.1530 0.1530 0.1577 0.1578

-0.0220 -0.0221 -0.0301 -0.0300 -0.0423 -0.0334 -0.0336 -0.0318 -0.0317

3.547 3.657 3.654 3.663 3.631 3.262 3.262 3.434 3.437

4.567 4.677 4.673 4.682 4.651 4.281 4.281 4.453 4.457

5.081 5.191 5.187 5.197 5.165 4.796 4.795 4.968 4.971

Eox (V) at pH 7 w/o Mete w/ Metf -0.452 -0.562 -0.558 -0.568 -0.536 -0.166 -0.166 -0.338 -0.342

-0.966 -1.076 -1.072 -1.082 -1.050 -0.681 -0.680 -0.853 -0.856

a We have used 1/2∆G (H ) ) 4.115 eV at pH ) 7 and T ) 298.15 K. The reaction for which ∆E has been investigated is (chl-a) (membrane) ox 2 2 f (chl-a)2+(membrane) + e-(g). The reduction potential corresponds to the opposite process. b Experimental reduction potential: P680 1.1 V vs NHE; P700 0.46-0.52 V vs NHE. c Dielectric constant of the condensed medium of photosystems is 8.5 (ref 28). d The small (PV-TS) contribution has been neglected, and ∆Ethermal ) 0.0079 eV has been used in every case. e Without methionine neighbor; for P700. f With methionine effect; for P680.

8. The interaction with the medium is a dominant effect, and as a result the calculated ∆Etot that includes the contribution of thermal energy for the oxidation process is nearly same for the Strouse, Shipman, and Svensson dimers, but somewhat less for the Trial dimers (Table 8). Nevertheless, the calculated ∆Etot values would still show positive oxidation potentials for all of the model dimers, as the calculated ∆G(1/2H2/H+) equals 4.1149 eV at pH 7 at 25 °C. Without additional environmental features, the high oxidation redox potential, that is, the (reduction) potential associated with the process

(Chl)2+ + e- ) (Chl)2

(6)

can never be explained. The observed potentials are 1.1 V for P68010 and 0.46-0.52 V for P70011 at the physiological pH at 25 °C as mentioned earlier. Hence, the oxidation potentials required are -1.1 V for P680 and -0.46 to -0.52 V for P700. This dilemma is solved by considering three more environmental features. These are discussed in the following. (1) The homology modeling by Svensson et al.7 reveals the presence of a ferrous ion about 28.25 Å away from both the chlorophyll molecules in PSII. It is expected that in PSI, too, an Fe2+ ion belonging to some of the Fe-containing complexes would be present at roughly the same distance from the chlorophylls of the special pair. Ignoring the exceedingly small differential effect of charge-dipole interactions, the presence of the Fe2+ ion is found to contribute 1.0194 eV to the ∆E of the oxidation process. The results are indicated in the column headed “Fe2+ effect” in Table 8. All of the dimers except the trial dimers of monohydrates are found to qualify as candidates for P700. Because the Shipman dimer (or a similar structure that has histidine ligands associated with Mg2+) is known to explain the spectroscopic features of P700,5,34 it is to be preferred over the

Strouse and Svensson pairs. The trial dimers of the dihydrates are similarly to be preferred. Nevertheless, the formation of the Shipman dimer from chlorophyll monomers requires the crossing of an energy barrier, and it is not kinetically favored, although the process may take place in the condensed phase environment of thylakoid. On the other hand, the trial dimers of the dihydrates Chl 91 or Chl 92 have negative dimer binding energy, indicating that their formation is not as such thermodynamically favored unless the dimer is stabilized by directly binding itself to the surrounding protein chain. (2) Relatively recent crystallographic data6 indicates the presence of a methionine residue near the chlorophyll ChlD1 of P680. Svensson et al.7 noticed from their homology modeling that D1 Met 183 interacts electrostatically with the nitrogen and the Mg2+ ion of ChlD1, P680. We consider a partial charge, +1/ 2, on methionine and that the methionine charge center is separated from the porphyrin charge center by about 7 Å. Because the INDO calculation yields an equal distribution of the positive charge of the special pair cation between the two constituent chlorophyll molecules, the presence of methionine contributes about 0.5143 eV to the ∆E of the oxidation process. The resulting ∆E values are shown in the column headed “methionine effect” in Table 8. Again, in this calculation we have neglected the differential effects of the charge-dipole and dipole-dipole interactions. The crystallographic data6 on PSII clearly discount the Strouse and the Shipman models for P680 on the ground that there is no water molecule bonded to the magnesium atoms, and we no longer consider these for P680. Similarly, the trial dimers are discounted, but even if we consider them, the calculated oxidation potentials would differ greatly from the observed ones. The Svensson pair leads to the oxidation potential -1.05 V,

Oxidation Redox Potentials of Four Special Pairs which is in very good agreement with the observed redox potential 1.1 V versus NHE at physiological pH at 25 °C. The unsymmetrical distribution of methionine can also help in understanding the EPR puzzles of P680.34 For instance, one may qualitatively expect the partial charge on D1 Met 183 to force the cationic charge to be mainly located on ChlD2, P680, and then the EPR g value and the EPR line width of P680+ would become indicative of the oxidation of a single molecule of Chl-a. (3) The crystallographic data6 also point out the presence of a histidine ligand with each chlorophyll of the special pair P680. Similarly, the EPR spectrum indicates the presence of histidine ligands in P700.14 The effect of this ligand replacing the water molecule would not make an appreciable change in the calculated oxidation potential of the Strouse, Shipman, and Trial dimers. But in the presence of this ligand, the ∆E for the formation of the Svensson dimer cation would decrease, as the latter cation would gain in stability relative to the neutral species. Simultaneously, the cation would be relatively less stabilized by interaction with medium as the Onsager radius would increase. These two opposing effects would partly cancel each other. Thus, the estimation of various environmental effects, along with the information gleaned from crystallography and spectroscopy, leads to two main conclusions. First, P700 must have a sandwich-type pair. Either the Shipman model or a variant of it, such as the trial dimer of chlorophyll dihydrates, can successfully explain the oxidation potential of P700. The Svensson dimer can also account for the same oxidation potential, if the methionine residue is absent from the vicinity of the special pair in PSI. The last possibility requires a reexamination of the spectroscopic data of P700, to evaluate the consistency of the optical and EPR spectra with the Svensson dimer. Second, the Svensson model explains the high redox potential of P680. The high potential is an outcome of the increase in the medium interaction energy of the cation due to the presence of the Fe2+ ion and the methionine neighbor. This potential is capable of splitting a water molecule, and it is indeed the driving force for the successful execution of Z-scheme. Acknowledgment. The authors gratefully acknowledge help from D. Shah, Prabhakar B. G. S., and V. Nehra in the preparation of the Figures. S.N.D. is thankful to CSIR for financial help. The authors thank one of the referees for making many valuable comments. References and Notes (1) Norris, J. R.; Uphaus, R. A.; Crespi, H. L.; Katz, J. J. Proc. Natl. Acad. Sci. U.S.A. 1971, 68, 625; 1974, 71, 4897. McElroy, J. D.; Feher, G. R.; Mauzcrall, D. C. Biochim. Biophys. Acta 1972, 267, 363. (2) Katz, J. J.; Norris, J. R. in Current Topics in Bioenergetics; Academic Press: New York, 1973; Vol. 5, p 41. (3) Fong, K. Proc. Natl. Acad. Sci. U.S.A. 1974, 71, 3692. (4) Chow, H. S.; Serlin, R.; Strouse, C. E. J. Am. Chem. Soc. 1975, 97, 7230.

J. Phys. Chem. B, Vol. 105, No. 7, 2001 1451 (5) Shipman, L. L.; Cotton, T. M.; Norris, J. R.; Katz, J. J. Proc. Natl. Acad. Sci. U.S.A. 1976, 73, 1791. (6) Ku¨hlbrandt, W.; Wang, D. N.; Fujiyoshi, Y. Nature 1994, 367, 614. (7) Svensson B.; Etchebest, C.; Tuffery, P.; van Kan, P.; Smith J.; Styring, S.; Biochemistry 1996, 36, 14486. (8) Kashiwagi, H.; Hirota, F.; Nagashima, U.; Takada, T. Int. J. Quantum Chem. 1986, 30, 311. (9) Watanabe, T.; Kobayashi, M. In Chlorophylls; Scheer, H., Ed.; CRC Press: Boca Raton, 1991; p 296. (10) Knaff, O. B.; Malkin, R. Arch. Biochem. Biophys. 1973, 159, 555. Evans, M. C. W.; Sihra, C. K.; Slabas, A. R. Biochem. J. 1977, 162, 75. Setif, P.; Mathis, P. Arch. Biochem. Biophys. 1980, 204, 477. Klimov, V. V.; Allakhverdiev, S. I.; Demeter, S.; Krasnovskii, A. A. Dokl. Akad. Nauk. SSSR 1979, 249, 227. (11) Mathis, P.; Rutherford, A. W. In Photosynthesis; Amesz, J., Ed.; Elsevier: Amsterdam, 1987; Chapter 4. Babcock, G. T. In Photosynthesis; Amesz, J., Ed.; Elsevier: Amsterdam, 1987; Chapter 6. (12) Vrieze, J.; Gast, P.; Hoff, A. J. J. Phys. Chem. 1996, 100, 9960. (13) Bittl, R.; Zech, S. G.; Fromme, P.; Witt, H. T.; Lubitz, W. Biochemistry 1997, 36, 12001. (14) Mac, M.; Bowlby, N. R.; Babcock, G. T.; McCracken, J. J. Am. Chem. Soc. 1998, 120, 13215. (15) Morris, E. P.; Hankamer, B.; Zheleva, D.; Friso, G.; Barber, J. Structure 1997, 5, 837. (16) Rhee, K. H.; Morris, E. P.; Barber, J.; Kuhlbrandt, W. Nature 1998, 396, 283. (17) Nield, J.; Kruse, O.; Ruprecht, J.; da Fonseca, P.; Buchel, C.; Barber, J. J. Biol. Chem. 2000, 275, 27940. (18) Datta, S. N.; Priyadarshy, S. Chem. Phys. Lett. 1990, 173, 360. (19) Pople, J. A.; Beveridge, D. L. In Approximate Molecular Orbital Theory; McGraw-Hill: New York, 1970. (20) Gaussian 92 for Windows, Gaussian Inc.: Pittsburgh, 1992. (21) Newton, M. D. J. Phys. Chem. 1975, 79, 2795. (22) (a) Warshel, A.; Parson, W. W. J. Am. Chem. Soc. 1987, 109, 6143. Parson, W. W.; Warshel, A. J. Am. Chem. Soc. 1987, 109, 6152. (b) Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. J. Chem. Phys. 1983, 79, 926; Ohtsuka, Y.; Ohkawa, K.; Nakatsuji, H. J. Comput. Chem. (in press). (23) Datta, S. N.; Deshpande, R. Ind. J. Pure Appl. Phys. 1997, 35, 483. (24) Datta, S. N.; Mallik, B. J. Phys. Chem. B 1997, 101, 4171, 5191. (25) Hanson, L. K. In Chlorophylls; Scheer, H., Ed.; CRC Press: Boca Raton, 1991; p 993. (26) Christoffersen, R. E. Int. J. Quantum Chem. 1979, 16, 573. (27) Plato, M.; Mo¨bius, K.; Lubitz, W. In Chlorophylls; Scheer, H., Ed.; CRC Press: Boca Raton, 1991; p 1015. (28) Datta, S. N.; Prabhakar, B. G. S.; Nehra, V. J. Phys. Chem. B 1999, 103, 2291. Datta, S. N.; Nehra, V.; Jha, A. J. Phys. Chem. B 1999, 103, 8768. (29) Noyes, R. M. J. Am. Chem. Soc. 1962, 84, 513. (30) ∆G°f for H(g) is 203.25 KJ mol-1, and ∆Esoln for H+(g) is -1090 KJ mol-1. These data have been taken from Barrow, G. M. Physical Chemistry, 5th ed.; Tata McGraw-Hill: New Delhi, 1992. Neglecting -TS for the gaseous electron and the aqueous proton, we find ∆G° for reaction 3 to be 4.4794 eV. (31) Petke, D.; Maggiora, M.; Shipman, L. L.; Christoffersen, R. E. Photochem. Photobiol. 1980, 32, 399. (32) Sakuma, T.; Takada, T.; Kashiwagi, H.; Nakamura, H. Int. J. Quantum Chem., Quantum Biol. Symp. 1990, 17, 93. (33) Datta, S. N.; Mallik, B. Int. J. Quantum Chem. 1997, 61, 865. (34) Malkin, R.; Bearden, A. J. Biochim. Biophys. Acta. 1975, 396, 250. Rutherford, A. W.; Paterson, D. R.; Mullet, J. Biochim. Biophys. Acta. 1981, 635, 205. Ke, B.; Inoue, H.; Babcock, G. T.; Fang, Z.-X.; Dolan, E. Biochim. Biophys. Acta 1982, 682, 297. Den Blanken, H. J.; Holf, A. J.; Jongenelis, A. P. J. M.; Diner, B. A. FEBs Lett. 1983, 157, 21.

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