Role of a Water Network around the Mn4CaO5 Cluster in

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The role of a water network around the Mn4CaO5 cluster in photosynthetic water oxidation: A study by Fourier transform infrared spectroscopy and QM/MM calculation Shin Nakamura, Kai Ota, Yuichi Shibuya, and Takumi Noguchi Biochemistry, Just Accepted Manuscript • DOI: 10.1021/acs.biochem.5b01120 • Publication Date (Web): 30 Dec 2015 Downloaded from http://pubs.acs.org on January 5, 2016

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The Role of a Water Network around the Mn4CaO5 Cluster in Photosynthetic Water Oxidation: A Study by Fourier Transform Infrared Spectroscopy and QM/MM Calculation

Shin Nakamura, Kai Ota, Yuichi Shibuya, and Takumi Noguchi*

Division of Material Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8602, Japan

*corresponding author: Takumi Noguchi E-mail: [email protected]. Telephone: +81-52-789-2881. Fax: +81-52-789-2883.

Funding: This study was supported by the Grants-in-Aids for JSPS Fellows (15J10320 to S.N.) and for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology (24000018, 24107003, and 25291033 to T.N.).

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ABBREVIATIONS FTIR, Fourier transform infrared; Mes, 2-(N-morpholino)ethanesulfonic acid; PSII, photosystem II; QM/MM, quantum mechanics/molecular mechanics; WOC, water-oxidizing center; XFEL, X-ray free electron laser.


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ABSTRACT: Photosynthetic water oxidation takes place at the Mn4CaO5 cluster in photosystem II. Around the Mn4CaO5 cluster, a hydrogen bond network is formed by several water molecules including four water ligands. To clarify the role of this water network in the mechanism of water oxidation, we investigated the effects of the removal of Ca2+ and substitution to metal ions on the vibrations of water molecules coupled to the Mn4CaO5 cluster by means of Fourier transform infrared (FTIR) difference spectroscopy and quantum mechanics/molecular mechanics (QM/MM) calculations. The OH stretching vibrations of nine water molecules forming a network between D1-D61 and YZ were calculated using the QM/MM method. Based on the calculated normal modes, a broad positive feature at 3200-2500 cm−1 in an S2-minus-S1 FTIR spectrum was attributed to the vibrations of strongly hydrogen-bonded OH bonds of water involving the vibrations of water ligands to a Mn ion and the in-phase coupled vibration of a water network connected to YZ, while bands in the 3700-3500 cm−1 region were assigned to the coupled vibrations of weakly hydrogen-bonded OH bonds of water. All the water bands were lost upon Ca2+ depletion and Ba2+ substitution, which inhibit the S2→S3 transition, indicating that a solid water network was broken by these treatments. By contrast, Sr2+ substitution slightly altered the water bands around 3600 cm−1, reflecting minor modification in water interactions, consistent with the retention of water oxidation activity with a decreased efficiency. These results suggest that the water network around the Mn4CaO5 cluster plays an essential role in the water oxidation mechanism particularly in a concerted process of proton transfer and water insertion during the S2→S3 transition. 3 ACS Paragon Plus Environment

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INTRODUCTION Photosynthetic water oxidation, which takes place at the water-oxidizing center (WOC) in photosystem II, is a light-driven reaction to gain electrons necessary for CO2 reduction in synthesizing sugars.1-8 Besides electrons, water oxidation generates protons and molecular oxygen. Released protons produce a proton gradient across the thylakoid membrane, which is used to synthesize ATP. On the other hand, molecular oxygen liberated to the air is the main source of oxygen in the atmosphere. Thus, photosynthetic water oxidation sustains life on the earth both as an energy and oxygen source. The WOC consists of a Mn4CaO5 cluster stabilized by seven amino acid ligands from the D1 [D170, E189, H332, E333, D342, and A344 (C-terminus)] and CP43 (E354) proteins of PSII.9-12 Water oxidation proceeds through a cycle of five intermediates designated as Sn states (n = 0−4), with a larger value of n implying a higher oxidation state.13,14 Among them, the S1 state is the most stable in the dark, and the Sn state (n = 0−3) advances to the Sn+1 state by abstraction of an electron by a photo-oxidized chlorophyll dimer P680 through a redox-active tyrosine YZ (D1-Y161). The S4 state is a transient state that immediately relaxes to the S0 state by releasing O2. A breakthrough of the water oxidation research was given by the X-ray crystallographic structure of PSII at 1.9 Å resolution,11 which provided the atomic structure of WOC including oxygen atoms bridging Mn and Ca ions, four water ligands, and two nearby Cl− ions (Cl-1 and Cl-2). There was, however, a criticism that the Mn4CaO5 cluster in this structure suffered from damage by a high dose of X-ray radiation and actually represented lower oxidation states than the S1 state.15,16 Suga et al.12 recently reported a 1.95 Å structure free from X-ray damage obtained using ultra-short X-ray pulses from 4 ACS Paragon Plus Environment

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an X-ray free electron laser (XFEL), and showed that the basic structure of the Mn4CaO5 cluster was the same between the two structures although partial reduction of Mn ions was found in the former 1.9 Å structure. In these 1.9-1.95 Å structures, in addition to the four water ligands (W1 and W2 attached to Mn4 and W3 and W4 to Ca; see Figure 1 for numbering of the Mn ions and water molecules), several water molecules were found interacting with the water ligands forming a hydrogen bond network between the Cl-1/D1-D61 and YZ sites.11,12 However, without resolving hydrogen atoms, the protonation states of the water molecules and their hydrogen bond structures remain unknown. During an S-state cycle, four protons are released by oxidation of two water molecules. A proton release pattern was shown to be 1: 0: 1: 2 for the S0→S1, S1→S2, S2→S3, and S3→S0 transitions, respectively.17-19 Because an electron is abstracted in each transition, this proton release pattern indicates that an excessive positive charge is accumulated on the Mn4CaO5 cluster in the S2 and S3 states. It was suggested that the presence of an excessive positive charge requires proton release before electron transfer in the S2→S3 and S3→S0 transitions, whereas an electron was proposed to be first transferred before proton transfer in the S0→S1 transition.20-25 In clarifying the water oxidation mechanism, it is crucial to know which water molecule releases a proton and how the water network around the Mn4CaO5 cluster is used for the proton transfer. Relevant unanswered questions are which channel leading from WOC to the lumen11,26-33 is functional in proton release and water insertion and whether the channel is different depending on the S-state transitions. Another key element to understand the water oxidation mechanism is the role 5 ACS Paragon Plus Environment

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of Ca2+ in the Mn4CaO5 cluster. It has been known that Ca2+ can be removed and replaced with other metal ions without decomposition of the Mn4 cluster.1,34-41 However, only Sr2+, except for original Ca2+, can restore the water oxidation activity albeit with a lower O2 evolution rate, while Ca2+ depletion and substitution to other metal ions suppress the S2→S3 transition. A recent EXAFS study42 and theoretical calculations43-45 indeed showed that the removal of Ca2+ did not affect the basic structure of the Mn4 cluster. Thus, the role of Ca2+ in water oxidation has been extensively argued and possibilities such as direct involvement in the reaction by binding substrate and retaining a hydrogen bond network necessary for proton transfer have been suggested.41-47 In this study, the role of the water network around the Mn4CaO5 cluster was investigated with relevance to the Ca2+ function. We assigned the OH vibrations of water molecules in a Fourier transform infrared (FTIR) difference spectrum of WOC using quantum mechanics/molecular mechanics (QM/MM) calculations, and further examined the effect of Ca2+ depletion and Sr2+ and Ba2+ substitution on the water vibrations. Light-induced FTIR difference spectroscopy is a powerful technique to study the detailed structures and interactions of cofactors and their environments.48-50 It is especially sensitive to hydrogen bond structures of water and amino acid residues, and thus suitable to the study of the water oxidation reaction in PSII.51-59 Meanwhile, quantum chemical calculations were recently extensively applied to the water oxidation mechanism.16,43-45,60-73 Density functional theory (DFT) and QM/MM calculations based on the X-ray crystallographic structures provided the structures of the Mn4CaO5 cluster in all the individual S states and hence could predict the reaction mechanism of water 6 ACS Paragon Plus Environment

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oxidation. Our study provided evidence that a water network around the Mn4CaO5 cluster is destroyed upon Ca2+ depletion and Ba2+ substitution, whereas it is slightly modified by Sr2+ substitution. With these results, the roles of the water network and Ca2+ in the water oxidation mechanism are discussed.

MATERIALS AND METHODS Samples.

Oxygen-evolving PSII membranes of spinach were prepared as

reported previously74 and suspended in a pH 6.5 buffer (40 mM Mes-NaOH, 400 mM sucrose and 20 mM NaCl). Ca2+ depletion was performed by a low pH treatment.39,40 The PSII sample was treated with a pH 3.0 citrate buffer (10 mM citrate-NaOH, 400 mM sucrose, and 20 mM NaCl) for 5 min on ice, and then 0.1 volume of a pH 7.5 Mops buffer (0.5 M Mops-NaOH, 400 mM sucrose, and 20 mM NaCl) was added, followed by incubation for 20 min on ice. The Ca2+-depleted PSII membranes were washed two times with the above pH 6.5 buffer additionally involving 0.5 mM EDTA. For Sr2+ and Ba2+ substitution, Ca2+-depleted PSII membranes were suspended in a pH 6.0 buffer involving 40 mM Mes-NaOH, 400 mM sucrose, 20 mM NaCl, and 20 mM SrCl2 or BaCl2 and incubated for 1 h on ice.75 For FTIR measurements, 1 mL of the sample suspension (0.5 mg Chl/ml) in a pH 6.0 buffer (20 mM Mes-NaOH and 5 mM NaCl) with additional 5 mM XCl2 (X = Ca, Sr and Ba for Ca2+-PSII, Sr2+- PSII, and Ba2+-PSII, respectively) or 1 mM EDTA (for Ca2+-depleted PSII), was centrifuged at 150,000 g for 5 min. The pellet was resuspended in 100 μL of the same buffer involving XCl2 or EDTA, diluted with 880 μL of Milli-Q water, and then mixed with 16 μL of 100 mM sodium ferrocyanide and 4 μL of 100 mM 7 ACS Paragon Plus Environment

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tris(tetrabutylammonium)hexacyano ferrate(III). The sample was centrifuged at 4,000 g for 5 min, and the 900 μL of supernatant was removed. Note that we used these ferricyanide and ferrocyanide compounds instead of usually used potassium ferricyanide/ferrocyanide to avoid the interaction of K+ with the Ca2+ site.76 The precipitation was suspended in the remaining solution and the aliquot of suspension (10 μL) was loaded on a CaF2 (for Ca2+-, Sr2+, and Ba2+-PSII) or a ZnSe (for Ca-depleted PSII) plate.77 The sample was dried under N2 gas flow to make a dry film of PSII membranes, and then was covered with another CaF2 (or ZnSe) plate with a silicone spacer (0.5 mm in thickness). In this sealed infrared cell, 2 μl of 40 % (V/V) glycerol/water solution was placed without touching the sample to form a moderately hydrated film.78 FTIR measurements.

FTIR spectra were recorded using a Bruker IFS-66/S or

VERTEX 80 spectrophotometer equipped with an MCT detector (InfraRed D313-L).75 The sample temperature was adjusted to 10 ˚C by circulating cold water in a copper holder. Flash illumination was performed using a Q-switched Nd:YAG laser (INDI-40-10; 532 nm; ~7 ns fwhm; ~7 mJ pulse−1 cm−2). For control Ca2+-PSII and Sr2+- and Ba2+-substituted PSII, single-beam spectra with 40 scans (20-s accumulation) were recorded before and 2-s after a single flash, and the measurements were repeated with an interval of 15 min. Spectra of 256 cycles using 8 samples for Ca2+-PSII and those of 128 cycles using 3-4 samples for Sr2+and Ba2+-substituted PSII were averaged to calculate S2/S1 difference spectra. The 2-s interval after the flash was inserted to remove the signals of quinone electron acceptors (QA and QB) as much as possible from the spectra. For Ca2+-depleted PSII, which shows a slower relaxation of the S2 state, single beam spectra were measured with 100 scans (50-s accumulation) before and after single-flash illumination and the measurements were 8 ACS Paragon Plus Environment

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repeated with an interval of 3 h. Spectra of 24 cycles using 5 samples were averaged. Quantum chemical calculations.

Quantum chemical calculations were

performed using the Gaussian09 program package. 79 QM/MM calculations were performed using the ONIOM (our own n-layered integrated molecular orbital and molecular mechanics) method80 as described previously.25 The atomic coordinates of amino acid residues, water molecules, Mn4CaO5 cluster, and Cl− ions located within 20 Å from the Ca atom were taken from the X-ray structure of the PSII complex at a 1.95 Å resolution by XFEL (PDB code: 4UB6)12. The hydrogen atoms were generated and optimized using Amber. The QM region (Figure S1) consists of the Mn4CaO5 cluster, Cl-1, nine water molecules near Ca and Cl-1 (W1-W9; see Figures 1 and S1 for numbering of the water molecules), amino acid ligands to the Mn and Ca ions (D1-D170, D1-E189, D1-H332, D1-E333, D1-D342, D1-A344, and CP43-E354), YZ, D1-H190, and nearby amino acid side chains and backbones (D1-D61, CP43-R357, D2-K317, backbones between D1-F182 and D1-M183 and between D1-S169 and D1-G171), while other atoms in the selected region of PSII (amino acid residues and Cl− within 20 Å from the Ca; Figure S2) were assigned to the MM region (Amber was used as a force field). The geometry of the QM region was optimized by fixing other atoms in the MM region using ONIOM (B3LYP:Amber). Normal mode calculations were performed for the optimized geometries of the QM region. As basis sets in QM calculations, LANL2DZ is used for Ca and Mn, and 6-31G(d) for other atoms. The absence of vibrations with imaginary frequencies was checked to confirm the structure in an energy minimum. No scaling was adopted for the calculated frequencies.


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RESULTS Effects of Ca2+ depletion and metal substitution on an S2/S1 FTIR difference spectrum Light-induced FTIR difference spectra upon S1→S2 transition (hereafter designated S2/S1 spectra) were obtained using control (+Ca2+), Sr2+-substituted, Ba2+ substituted, and Ca-depleted PSII preparations (Figure 2). The region of 1800-1200 cm−1 (Figure 2C), which represents protein vibrations, involving asymmetric and symmetric COO− stretches (1600-1450 and 1450-1350 cm−1, respectively), and amide I (1700-1600 cm−1) and amide II (~1550 cm−1) vibrations, reproduced previously reported spectra.75-77,81-84 In particular, spectral features in the symmetric COO− region (1450-1350 cm−1) showed characteristic changes: the bands at 1404 and 1364 cm−1 in control spectra were lost upon Ca2+ depletion and Ba2+ substitution,76,77,81 while upon Sr2+ substitution, the peak at 1435 cm−1 was slightly upshifted to 1440 cm−1, the negative peak at 1421 cm−1 was weakened, and a new structure was observed at 1384/1379 cm−1.75,76,82-84 These spectral changes indicate that metal substitutions and Ca2+ depletion were appropriately performed in the PSII preparations. Further notable changes by these treatments were observed in bands in higher-frequency regions of 3650-3550 cm−1 (Figure 2A) and 3200-2500 cm−1 (Figure 2B), which have been attributed to the vibrations of weakly hydrogen-bonded OH bonds of water molecules and the vibrations of a hydrogen bond network with polarizable protons, respectively.85-92 Bands at 3613/3590 cm−1 and a broad feature in 3000-2500 cm−1 both disappeared upon Ba2+ substitution and Ca2+ depletion (Figure 2A,B, traces c and d). It should be noted that small peaks on the broad feature (e.g., at approximately 2900 and 2800 cm−1), which were attributed to the Fermi resonance peaks of a His side 10 ACS Paragon Plus Environment

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chain by 15N labeling,93 seemed to remain in the spectra. By contrast, when Ca2+ is replaced with Sr2+, the spectral features in these regions were mostly retained (Figures 2A, B, traces b); The broad feature with Fermi resonance peaks in 3000-2500 cm−1 was virtually unchanged, whereas the peak at 3613 cm−1 upshifted to 3621 cm−1 and a prominent negative peak appeared at 3638 cm−1. These results were significantly different from recent results by Polander and Barry,94 in which by Ca2+ depletion only the peak at 2880 cm−1 diminished leaving a broad feature from 2200 to 3200 cm−1, and Sr2+ substitution showed the same change as Ca2+ depletion. Furthermore, a differential signal around 3600 cm−1 was not observed even in an intact Ca2+-PSII sample. They assigned the 2880 cm−1 band to a cationic water cluster. However, in our previous data, the corresponding peak at ∼2900 cm−1 downshifted upon global 15N and 13C labeling but was unchanged by H218O substitution,86,93,95 indicating that this peak arises from one of several Fermi resonance peaks of His (these data were organized in Fig. S5 of ref. 25). In addition, the peaks in the weakly hydrogen-bonded water region have been reproduced in many studies by different groups85-92 except the group of ref. 94. Thus, their assignment of the band at 2880 cm−1 to a cationic water cluster has no experimental basis.

QM/MM calculations of water vibrations To assign the OH stretching vibrations of water molecules around the Mn4CaO5 cluster in the S2/S1 difference spectra, we performed normal mode analysis using the QM/MM method. The QM region include the Mn4CaO5 cluster, Cl-1, and nine water molecules (W1-W9) together with surrounding amino acid residues (Figure 11 ACS Paragon Plus Environment

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S1). We assumed the oxidation states of the Mn atoms in the S1 state as (Mn1, Mn2, Mn3, Mn4) = (III, IV, IV, III) following a widely accepted view,16,43-45,60-72 and protonation states of O5 and W2 as O2− and H2O, respectively.16,43,44 Calculations were performed based on the X-ray structure by XFEL at 1.95 Å resolution (PDB: 4UB6).12 The heavy atoms (C, O, N, S, and Cl) of the MM regions were fixed to the coordinates of these original structures, while the structure of the QM region was optimized. The hydrogen bond structure of water molecules in the optimized geometry in the S1 state is shown in Figure 1. A linear hydrogen bond chain is formed from D2-K317 and D1-D61 near Cl-1 to YZ through W9, W8, W2, W5, W6, and W7, while a cyclic water cluster is formed by W3, W5, W6, and W7. W1 and W4 are not directly involved in this water network but directly hydrogen-bonded to D1-D61 and YZ, respectively. The average value of hydrogen bond distances of water molecules was 2.83 Å (Table 1) in good agreement with the experimental one (2.86 Å). Hydrogen bond distances between the oxygen atoms of W1-D61, W2-W8, W5-W6, and W7-YZ, which were calculated to be 2.63, 2.68, 2.68, and 2.67 Å, respectively, were significantly short compared with other hydrogen bonds. The optimized geometry of the S2 state was calculated by oxidation of one Mn atom in the S1 model. It has been shown that two forms of the Mn4CaO5 cluster are stably optimized: an open cubane form with Mn4(IV) and a closed cubane form with Mn1(IV).64,66,68,71,72 Our calculation also provided two forms of the S2 state with Mn4(IV) and Mn1(IV) (Figure S3). The hydrogen bond patterns of water molecules were unchanged by the S1→S2 transition in both the S2 forms (Table 1). Some of the hydrogen bonds such as D1-D61, W3-W7, W4-YZ, W5-W6, and W8-Cl were shortened 12 ACS Paragon Plus Environment

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by S2 formation. Normal mode analysis was performed for the optimized structures in the S1 and S2 states. Normal modes with large contributions of water OH vibrations obtained in the calculation were collected in Tables 2, and were depicted in Figure 3 superimposing the control S2/S1 FTIR difference spectrum of Ca2+-PSII. It is shown that the OH stretching vibrations of water molecules exhibited frequencies between 3720 and 2600 cm−1, overlapping the weakly hydrogen-bonded water OH bands in a higher-frequency region (Figures 3B) and the broad feature of a hydrogen bond network in a lower-frequency region (Figures 3A) in the S2/S1 difference spectrum. Many modes are significantly delocalized over several water molecules, and lower frequency vibrations generally have higher intensities (Table 2) due to stronger hydrogen bonds.96 Also, the frequencies and intensities of individual modes are rather different between the S1 (Figure 3, negative black bars) and S2 (red and blue bars) state, and even between the two S2 forms with Mn4(IV) (red bars) and Mn1(IV) (blue bars). Using the obtained vibrations, S2/S1 difference spectra were simulated assuming Gaussian bands with 20 and 200 cm−1 widths (FWHM) for modes in the weakly and strongly hydrogen-bonded OH regions, respectively, and equal populations of the two S2 forms due to a thermal equilibrium (Figure 3, green curve). These bandwidths were selected to reproduce the experimental spectrum based on the general tendency that a stronger hydrogen bond significantly broadens the width of a OH band concomitant with a downshifted freqency.96,97 It is noted that in normal mode analysis, normal mode vibrations are estimated only for the optimized geometry and hence the effects of thermal fluctuations at room temperature are involved in the assumed bandwidths. In the strongly 13 ACS Paragon Plus Environment

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hydrogen-bonded region of 3200-2400 cm−1, a positive broad feature on the lower-frequency side was well reproduced, although the band center was slightly lower than the experimental one (Figure 3A). The lowest-frequency modes of the S2 forms with Mn4(IV) and Mn1(IV) at 2618 and 2745 cm−1, respectively, arise from the W1a proton (see Figure 1 for numbering of protons) hydrogen-bonded with D1-D61, which has a short hydrogen bond distance of 2.53-2.57 Å (Table 1). The second lowest-frequency modes at 2911 [S2 with Mn4(IV)] and 2778 [S2 with Mn1(IV)] cm−1 are due mainly to the W2b vibration. Intriguing modes in the low-frequency region are those at 3177 [S2 with Mn4(IV)] and 3164 [S2 with Mn1(IV)] cm−1 arising from the coupled vibrations of W5a, W6a, W7a, W2a, and W3b with the largest contribution of W5a forming a strong hydrogen bond with W6 (the hydrogen bond distance is 2.65 Å). This mode shows an in-phase motion from water ligands, W2 and W3, to W7 hydrogen-bonded with YZ through a water network (directions of the displacement vectors are depicted in Figure 4). A similar type of coupled vibration of water molecules with a relatively lower frequency was also identified in a water wire in bacteriorhodopsin.98 In the weakly hydrogen-bonded region of 3750-3500 cm−1 (Figure 3B), simulated bands (green curve) at 3642 (+), 3587(-), 3500(+), and 3469(-) cm−1 seem to correspond to the experimental bands at 3613(+), 3590(-), ~3517(+), and 3469(-) cm−1, respectively. Most of the modes result from significant couplings with several vibrations, which mainly arise from the OH groups hydrogen-bonded with amino acid residues or Cl−.


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DISCUSSION Assignments of the OH vibrations of water molecules around the Mn4CaO5 cluster The hydrogen bond structures (Figure 1 and Table 1) and the OH vibrations of water molecules (Table 2 and Figure 3) around the Mn4CaO5 cluster were calculated for the S1 state and the two forms of the S2 state [an open cubane form with Mn4(IV) and a closed cubane form with Mn1(IV)] using the QM/MM method based on the X-ray structure by XFEL at 1.95 Å resolution.12 The calculated OH vibrations of water were found in a wide frequency range between 3720 and 2600 cm−1 (Table 2), reflecting significantly scattered hydrogen bond distances between 3.29 and 2.53 Å in the water network (Table 1). Most of the water OH vibrations are coupled among several water molecules in the network (Table 2). Recently, Yang et al.44 also performed normal mode analysis of water molecules in the S2 state using QM/MM calculations based on the 1.9 Å structure by synchrotron radiation.11 Although the resultant hydrogen bond pattern of water molecules was similar to ours, the obtained OH frequencies and the vibrational modes were significantly different from those in Tables 2. The calculated frequencies were found between 3752 and 3150 cm−1 and OH modes with frequencies lower than 3000 cm−1 were not obtained. This discrepancy between the results of ref. 44 and our study could arise from the following differences in calculations. (1) The difference in the X-ray structure used for calculations. We used a damage-free structure by XFEL12 in contrast to a partially damaged structure by a strong dose of X-ray radiation11 used in ref. 44. Because the coordinates of heavy atoms other than hydrogen atoms in the MM region were directly adopted from the X-ray structures without optimization, the 15 ACS Paragon Plus Environment

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difference in the X-ray structure could result in slightly different optimized structures of the QM region. (2) The difference in the QM region for geometry optimization. Although the geometry-optimized QM region in ref. 44 included more amino acid residues than our study, the main chain amide of D1-F182 that interacts with W6 was not included, whereas all the amino acid residues and main chain amides interacting with W1-W9 were included in our QM region. The difference in the QM region, especially the absence of a residue directly interacts with a water molecule, could change the hydrogen bond interactions of the water network. (3) The difference in the region used for the normal mode calculation. The authors in ref. 44 abstracted a narrower part from the QM region for vibrational analysis by excluding most of amino acid residues directly interacting water molecules as well as a Cl− ion, whereas we used the whole QM region involving all the amino acid residues around the water molecules and the Cl− ion (Figure S1). Indeed, when we performed normal mode analysis using a narrower part identical to ref. 44 abstracted from our optimized QM structure, the frequencies were largely shifted from the original ones in Table 1; for example, the vibrations at 2618, 2911, 3177 cm−1 in the lower-frequency region shifted by −18, +139 and +38 cm−1 to 2590, 3050, and 3215 cm−1, respectively. However, the thus calculated frequencies did not reproduce the frequencies reported in ref. 44. Thus, although a large-enough region for normal mode calculation must be important for obtaining correct vibrational frequencies, the exact reason for the discrepancy between the two studies is unknown at present. The calculated OH frequencies well overlap the regions of water and hydrogen bond networks in the experimental S2/S1 FTIR difference spectrum (Figure 3), 16 ACS Paragon Plus Environment

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involving a weakly hydrogen-bonded OH region of water in 3700-3500 cm−1 and a lower-frequency region with a broad positive feature in 3200-2500 cm−1.85-92 In particular, the latter broad feature, which has been assigned to the vibrations of polarizable protons in hydrogen bond networks,86 was sufficiently reproduced in the calculation (Figures 3A). The optimized geometry (Table 1) showed that this positive feature is caused by the strengthened hydrogen bonds of some water OH groups such as W1a and W2b (Figure 1) upon the S2 formation, shifting their OH vibrations to lower frequencies. The stronger hydrogen bonds are probably caused by accumulation of an excess positive charge on the Mn4CaO5 cluster in the S2 state, increasing the polarity of the ligands and the environment. The lowest-frequency mode in the S2 state arises from W1a hydrogen boned with D1-D61 [2618 and 2745 cm−1 in the S2 forms with Mn4(IV) and Mn1(IV), respectively; Table 2 and Figure 3]. W2b hydrogen bonded with W8 (2911 and 2778 cm−1) and the in-phase coupled vibration of W5a, W6a, W7a, W2a, and W3b (3177 and 3164 cm−1) also showed relatively low frequencies (Figure 3A). In a high frequency region of 3700-3500 cm−1 in the S2/S1 difference spectrum, weakly hydrogen-bonded OH bonds of water have been observed as a differential signal at 3613/3590 cm−1 (Figure 2Aa).85-92 There was another negative peak at 3663 cm−1, which showed an appreciable intensity in core preparations of Synechosystis sp. PCC 680388,90-92 but showed only a minor or almost no contribution in PSII preparations of Thermosynechococcus elongatus and spinach (Figure 2Aa).85,86,89 Our calculation showed that the OH vibrations of water molecules, which are hydrogen bonded with amino acid residues or Cl− with relatively long hydrogen bond distances, mainly contribute to the bands in this weakly hydrogen-bonded region (Table 2 and Figure 3A). 17 ACS Paragon Plus Environment

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The vibrations are severely coupled among several water molecules, and hence it is unlikely that the 3613/3590 cm−1 signal arises from a simple shift of one water vibration to a higher frequency as previously proposed.85 The negative band can arise from a coupled mode of W7ab, W4a, W3ab, and W6ab, while the positive band is from the coupled vibrations of W7b, W1b, W8b, W9b, and W6ab (Figure 3A). These water molecules mostly have asymmetric hydrogen bond structures with a strongly and weakly hydrogen bonds (Table 1), consistent with the previous experimental result.85 Our measurements of S2/S1 FTIR spectra showed that Ba2+ substitution and Ca2+ depletion, both of which block the S2→S3 transition,1,34,35 diminished both the lower-frequency broad feature in 3000-2500 cm−1 and the higher-frequency differential signal at 3613/3590 cm−1 (Figure 2A, B). By contrast, Sr2+ substitution, which retains the O2 activity, virtually unchanged the broad feature, but slightly affected the weakly hydrogen-bonded OH bands in the high frequency region. A positive band at 3613 cm−1 was upshifted to 3621 cm−1 by 8 cm−1 and a negative peak at 3638 cm−1 appeared (Figure 2A, trace b). In addition, Debus91 recently showed that D1-D61A mutation, which significantly reduced the efficiency of the S3→S0 transition,91,99,100 eliminated a negative 3663 cm−1 peak, typical of Synechosystis PSII core preparations, as well as the broad feature in 3000-2500 cm−1. These observations are consistent with the assignment that the broad band in 3000-2500 cm−1 and the OH vibrations around 3600 cm−1 arise from water molecules coupled with Ca and D1-D61 in a hydrogen bond network. In particular, the effect of D1-D61A mutation on the broad feature91 is consistent with the contribution of the localized vibration of W1a having a strong hydrogen bond with D1-D61 to this feature (Figures 3A). In addition, the loss of the 3663 cm−1 peak91 could 18 ACS Paragon Plus Environment

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be attributed to the W1b vibration at 3706 cm−1 calculated in the S1 state (Figure 3B). On the other hand, the change in the positive 3613 cm−1 peak by Sr2+ substitution is consistent with the involvement of W7b in the positive feature near this region (Figure 3B). W7 is hydrogen-bonded with W3, a ligand to Ca, and the X-ray crystallographic study of Sr2+-substituted PSII101 showed a slight displacement of W3. Therefore, the present experimental observation of the loss of both the board feature at 3000-2500 cm−1 and the bands at 3613/3590 cm−1 by Ca2+ depletion and Ba2+ substitution (Figure 2A, B) suggests that a solid hydrogen bond network of water molecules located between D1-D61 and Ca are broken by these treatments and instead this space is filled with non-structured water molecules.

Role of the water network in the water oxidation mechanism In the water oxidation mechanism, proton release takes place in the S0→S1, S2→S3, and S3→S0 transitions.17-19 For efficient proton release, proton transfer pathways by hydrogen bond networks involving water molecules are necessary to be formed in proteins. In particular, polarizable protons in water chains play an important role in rapid proton transfer using the Grotthuss mechanism.97,102 Several water channels were found around the Mn4 CaO5 cluster leading to the lumenal side.11,26-33 Among them, many authors suggested that the hydrogen bond network starting from D1-D61 through protonatable residues near Cl-1 is effective for proton transfer.31-33,60,99,103-106 In this pathway, the OH stretching vibration of W1a forming a strong hydrogen bond directly with D1-D61 (Figure 1), which was calculated at 2750-2610 cm−1 in the S2 state and probably contributes to the broad positive feature in 19 ACS Paragon Plus Environment

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the S2/S1 FTIR spectrum (Figure 3A), should work in proton transfer from W1, a ligand to Mn4, to D1-D61. In addition, the vibration of W2b strongly hydrogen bonded with W8 (calculated at 2920-2700 cm−1 in the S2 state), which may also be a constituent of the broad FTIR feature, can be effective for proton transfer from W2 to D1-D61 through W8 and W9 (Figure 1). This proton pathway through D1-D61 may be functional at least in the S3→S0 transition, because mutations of D1-D61 significantly retarded the S3→S0 transition and reduced the efficiency of this transition.91,99 On the other hand, the channel near YZ has been proposed as another proton transfer or water access pathway.11,22,25,27,29,30 We recently proposed a novel proton transfer mechanism via the YZ• radical in the S2 and/or S3 states, which require proton release before electron transfer due to an excess positive charge on the Mn4CaO5 cluster.25 Our QM/MM calculation showed that one water molecule near YZ moves closer to D1-H190 upon YZ• formation. It was suggested that hopping of a polarizable proton located between YZ• and D1-H190, which showed a broad feature around 2800 cm−1 in a YZ•/YZ FTIR spectrum, to this water triggers proton transfer from substrate water on the Mn4CaO5 cluster to the lumen.25 Alternatively, it might be possible that the first proton transfer takes place from W7 to W4, which is now connected with the hydrogen bond network to the lumen by the moved water molecule. In any case, in the mechanism of proton transfer through YZ or a nearby region, the in-phase coupled vibration of a water network involving W5a, W6a, W7a, W3a, and W2a (the directions of proton movements are shown in Figure 4), which was calculated at 3180-3160 cm−1 (Table 2, Figure 3A), may be effective in proton transfer from W2 and W3, candidates of substrate, to YZ. Using such a vibrational mode, rapid proton transfer from substrate 20 ACS Paragon Plus Environment

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to the YZ site will be possible by the Grotthuss mechanism immediately after or concerted with the trigger reaction of proton hop from YZ-HisH+ or W7. An EXAFS study42 and theoretical calculations43,44 suggested that Ca2+ is not a crucial element in maintaining the basic structure of the Mn4CaO5 cluster, but is necessary for organizing a surrounding water network. Indeed, the present FTIR study provided evidence that solid hydrogen bond network of water molecules around Ca2+ were destroyed upon Ca2+ depletion and Ba2+ substitution (see above). Such destruction of the solid water network should suppress the fast proton transfer from substrate to the YZ site. Because the proton transfer through YZ was suggested to function in the S2 state,22,25 this is consistent with the inhibition of the S2→S3 transition upon Ca2+ depletion and Ba2+ substitution.1,34,35 The significance of the water network around Ca2+ in proton transfer in the S2→S3/S3→S0 transition has also been suggested in the kinetic analysis of Sr2+ substituted PSII and the mutants of D1-173 amino acid located near YZ.46,47 Furthermore, the perturbation of water interactions by Sr2+ substitution as shown in the slight change in the water bands around 3600 cm−1 (Figure 2A, trance b) is consistent with the decrease in O2 evolution activity in Sr2+-substituted PSII.36-38 Alteration of a hydrogen bond network near Ca2+ by Sr2+ substitution has also been suggested by HYSCOPE spectroscopy107 and QM/MM calculation63 as well as X-ray crystallography.101 Theoretical studies suggested that in the S2→S3 transition a water molecule is inserted into Mn1 or Mn4 from bulk or possibly from W3, a water ligand to Ca.7,60,61,66,68,69,71,72 This idea is consistent with the elongation of the Mn-Mn distance in the S2→S3 transition detected by EXAFS.8,108 Previous FTIR studies also suggested 21 ACS Paragon Plus Environment

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water insertion into WOC in the S2→S3 transition.55,78,87 If W3 on Ca moves to Mn1 or Mn4, the inserted water could bind to Ca to compensate for the position of W3. A proton could be released from W3 using the YZ pathway before its movement, which can also explain the activity decrease by substitution with Sr2+ having different Lewis acidity.41 It is thus possible that the water network near YZ and Ca can be used for the concerted process of proton release and water insertion. Ca2+ depletion that destroys the solid water network may inhibit such a concerted process in the S2→S3 transition.

SUPPORTING INFORMATION AVAILABLE The optimized structure of the whole QM region, the structure of the whole QM/MM region, and the comparison of the optimized structures of the S1 state and the two forms of the S2 state. This material is available free of charge via the Internet at http://pubs.acs.org.

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cluster in photosystem II: The protonation pattern and oxidation state in the high-resolution crystal structure. J. Am. Chem. Soc. 134, 7442–7449. (68) Isobe, H., Shoji, M., Yamanaka, S., Umena, Y., Kawakami, K., Kamiya, N., Shen, J.-R., and Yamaguchi, K. (2012) Theoretical illumination of water-inserted structures of the CaMn4O5 cluster in the S2 and S3 states of oxygen-evolving complex of photosystem II: Full geometry optimizations by B3LYP hybrid density functional. Dalton Trans. 41, 13727−13740. (69) Isobe, H., Shoji, M., Yamanaka, S., Mino, H., Umena, Y., Kawakami, K., Kamiya, N., Shen, J.-R., and Yamaguchi, K. (2014) Generalized approximate spin projection calculations of effective exchange integrals of the CaMn4O5 cluster in the S1 and S3 states of the oxygen evolving complex of photosystem II. Phys. Chem. Chem. Phys. 16, 11911–11923. (70) Shoji, M., Isobe, H., Yamanaka, S., Umena, Y., Kawakami, K., Kamiya, N., Shen, J.-R., and Yamaguchi, K. (2013) Theoretical insight in to hydrogen-bonding networks and proton wire for the CaMn4O5 cluster of photosystem II. Elongation of Mn-Mn distances with hydrogen bonds. Cat. Sci. Technol. 3, 1831–1848. (71) Shoji, M., Isobe, H., and Yamaguchi, K. (2015) QM/MM study of the S2 to S3 transition reaction in the oxygen-evolving complex of photosystem II. Chem. Phys. Lett. 636, 172–179. (72) Bovi, D., Narzi, D., and Guidoni, L. (2013) The S 2 state of the oxygen-evolving complex of photosystem II explored by QM/MM dynamics: Spin surfaces and metastable states suggest a reaction path towards the S3 state. Angew. Chem. Int. Ed. 52, 11744−11749. 31 ACS Paragon Plus Environment

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(106) Suzuki, H., Yu, J., Kobayashi, T., Nakanishi, H., Nixon, P., and Noguchi, T. (2013) Functional roles of D2-Lys317 and the interacting chloride ion in the water oxidation reaction of photosystem II as revealed by Fourier transform infrared analysis. Biochemistry 52, 4748–4757. (107) Chatterjee, R., Milikisiyants, S., Coates, C. S., Koua, F. H. M., Shen, J.-R., and Lakshmi, K. V. (2014) The structure and activation of substrate water molecules in Sr2+-substituted photosystem II. Phys. Chem. Chem. Phys. 16, 20834–20843. (108) Pushkar, Y., Yano, J., Sauer, K., Boussac, A., and Yachandra, V. K. (2008) Structural changes in the Mn4Ca cluster and the mechanism of photosynthetic water splitting. Proc. Natl. Acad. Sci. U.S.A. 105, 1879−1884.


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Table 1: Calculated hydrogen bond distances (Å) of water molecules (between water oxygen and an acceptor atom) in comparison with the experimental distances in the X-ray structure experimentiii

calculation

S state S2 S2 S1 (oxidized Mn S1 [∆d]ii (Mn4) (Mn1) in S2) W1a-D61i 2.63 [−0.06] 2.57 2.53 2.69 W1b-S169 2.99 [+0.16] 3.08 2.94 2.83 W2a-W5 2.79 [+0.03] 2.78 2.75 2.76 W2b-W8 2.68 [+0.05] 2.66 2.60 2.63 W3a-W7 2.80 [−0.12] 2.75 2.76 2.92 W3b-W5 2.73 [−0.19] 2.75 2.76 2.92 W4a-YZ 2.78 [−0.12] 2.75 2.74 2.90 W4b-Q165 2.72 [+0.06] 2.70 2.69 2.66 W5a-W6 2.68 [−0.02] 2.65 2.65 2.70 W5b-D170 3.19 [−0.14] 3.24 3.25 3.33 W6a-W7 2.83 [−0.10] 2.86 2.85 2.93 W6b-F182 2.99 [+0.15] 2.95 2.93 2.84 W7a-YZ 2.67 [+0.14] 2.65 2.65 2.53 W7b-E189 2.86 [−0.11] 2.94 2.93 2.97 W8a-Cl 3.29 [0.00] 3.22 3.21 3.29 W8b-N181 2.77 [−0.09] 2.76 2.70 2.86 W9a-D61 2.71 [+0.02] 2.74 2.73 2.69 W9b-W8 2.90 [0.00] 2.89 2.90 2.90 2.83 [−0.03] 2.83 2.81 average 2.86 i Refer to Figure 1 for the numbering of water and its protons. ii Difference from the experimental value. iii Average of the XFEL X-ray structures of four monomers in two dimers (PDB: 4UB6 and 4UB8).12


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Table 2: Frequencies (cm−1) and assignments of the OH stretching vibrations of water molecules around the Mn4CaO5 cluster estimated by QM/MM calculations S2 (Mn4 = IV) frequency assignmentii (IR Int.)i W6a,b, W7b 3685 (640) W5b 3677 (259) W1b 3638 (693) W7b, W6a,b, W3a 3634 (470) W9b, W8a 3628 (308) W6a,b, W7a,b 3581 (205)

S1 frequency (IR Int.)i 3715 (322) 3706 (483) 3679 (190) 3648 (207) 3623 (224) 3592 (523) 3590 (629) 3578 (959) 3542 (627) 3534 (509) 3505 (359) 3477 (289) 3468 (1081) 3397 (456) 3390 (741) 3310 (849) 3246 (978) 3105 (2167) 3072 (1631) i

assignmentii W6a,b W1b W5b, W3b, W2a W8a, W9b W9b, W8a W7b, W3a, W6a, W4a W7a,b, W3a,b, W4b, W6a,b W4a, W7a, W3a,b, W6a W3b, W2a, W5a,b, W6a, W7b W6a, W7b W3a,b, W7a,b, W4a,b, W6a, W2a W2a, W3b, W4b W4b, W3b, W2a W8b W7a, W3a W9a W5a, W3b, W6a,b, W2a W1a, W2b W2b, W1a

Calculated IR Intensity (km/mol)

S2 (Mn1 = IV) frequency assignmentii (IR Int.)i W6a,b, W7b, W5b 3685 (574) W5b 3681 (311) W7b, W1b, W6b 3648 (896) W9b 3647 (271) W1b, W7b, W9b 3647 (342) W6a,b 3582 (302)

3549 (330)

W8a, W9b

3565 (318)

W8a

3504 (995)

W3b, W4a, W2a

3505 (875)

W3b, W2a, W4a

3498 (548)

W4a, W3b

3492 (563)

W4a

3427 (862) 3410 (507)

W3a, W7a, W6a W2a, W3b

3437 (769) 3400 (689)

W3a, W7a W2a, W3b

3392 (940) 3383 (429) 3323 (1180) 3288 (1026) 3177 (1203)

3387 (697) 3364 (547) 3289 (1029) 3257 (1527) 3164 (1192)

2911 (2940)

W4b W9a W8b W7a, W3a, W4a W5a, W6a, W7a, W2a, W3b W2b

2778 (4903)

W4b W9a W7a, W3a, W4a W8b W5a, W6a, W7a, W2a, W3b W2b, W1a

2618 (2485)

W1a

2745 (1244)

W1a, W2b

ii

Refer to Figure 1 for the numbering of water and its protons.


Biochemistry

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Figure Captions

Figure 1.

Hydrogen bond structure of water molecules near the Mn4CaO5 cluster

optimized by QM/MM calculation. The water molecules and the interacting parts in the QM region are selectively shown. Amino acid residues in which the subunit name is not specified in the labels are all on the D1 subunit. The full QM region is shown in Figure S1.

Figure 2. Light-induced FTIR difference spectra upon the S1→S2 transition of PSII membranes of spinach in the regions of 3680-3530 (A), 3150-2200 (B), and 1800-1200 (C) cm−1. a: control Ca2+-PSII; b: Sr2+-substituted PSII; c: Ba2+-substituted PSII; d: Ca2+-depleted PSII. Dotted lines in (A) and (B) are dark-minus-dark spectra representing baselines.

Figure 3. OH stretching vibrations of water molecules around the Mn4CaO5 cluster estimated by QM/MM calculation, superimposed on an experimental S2/S1 difference spectrum (black curve). (A) Strongly hydrogen-bonded region; (B) weakly hydrogen-bonded region. Black negative bars: the S1 state; red and blue positive bars: the S2 state with Mn4(IV) and Mn1(IV), respectively. A simulated S2/S1 difference spectrum (green curves) was obtained assuming Gaussian bands with widths (FWHM) of 200 and 20 cm−1 for strongly (A) and weakly (B) hydrogen-bonded OH vibrations, respectively, and an thermal equilibrium of the two S2 forms. The experimental spectrum of control Ca2+-PSII is identical to the spectrum in Figure 2, trace a. See 40 ACS Paragon Plus Environment

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Biochemistry

Figure 1 for numbering of water protons in assignments.

Figure 4. Directions of the displacement vectors of the in-phase coupled vibrations of a water network involving W5, W6, W7, W2, and W3.


Biochemistry

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Figure 1

F182 H190

YZ W6

b

D170 b a W5 S169

N181 W8 W9 b a

D2-K317

b a a

a

W2 Mn4

W1

D61

Q165

a

W4

W3 Ca

b

E189

O5 O1

O4

Cl

a

b

b

a b

b

W7

a

Mn1

O2 Mn2

Mn3 O3


ACS Paragon Plus Environment

43 3590

3591

3600

3613

3621

3638

3650

d

c

b

a

A

3550

-1

-5

2x10

Wavenumber (cm )

A

A

2800 2600

-1

2400

-5

2x10

Wavenumber (cm )

3000

B C

2200 1800

d

c

b

a

A

1700

1705

1705

1704

1677 1654

1600 1500

-1

1400

Wavenumber (cm )

1664 1656 1637

1626 1568 1544 1521

1638

1618

1552 1545 1531 1526

1641

1553 1567 1544 1522

1532

1504

1504 1432 1418 1404 1388

1418 1405 1389

1431

1421

1405 1379 1352

1354

1357

1696 1705 1685 1676 1670 1661 1650 1641 1633 1585 1567 1553 1544 1531 1521 1504 1440 1420 1404 1384 1365

1353

1685 1668 1652 1586 1553 1532 1504

1435

1364

1300

-5

4x10

1200

d

c

b

a

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Figure 2

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Biochemistry

Biochemistry

Figure 3

IR Intensity (km/mol)

6000

2b,1a

A 4000

2b

5a,6a,7a, 2a,3b

1a,2b 1a

5a,6a,7a, 2a,3b

2000

0

-2000 1a,2b

2b,1a

3200

3000

2800

2600 -1

2400

Wavenumber (cm ) 2000

IR Intensity (km/mol)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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7b,1b, 1b,7b, 3b,2a, 3b,4a, 6b 2a 9b 7b,6ab, 4a 6ab,7b 3a 6ab,7ab 1b 4a,3b 5b 6ab,7b, 8a,9b 9b,8a 4a 5b 5b 6ab 8a

B 1000

0

-1000

1b

8a,9b

6ab

3ab,7ab, 4ab,6a,2a

9b,8a 5b,3b,2a

-2000

3700

7b,3a, 6a,4a 7ab,3ab, 4b,6ab

4a,7a, 3ab,6a

6a,7b

3b,2a,5ab, 6a,7b

3600

2a,3b, 4b 4b,3b, 2a

3500

-1

Wavenumber (cm )


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Biochemistry

Figure 4

YZ

W6 W5

W8

W7 W2 Mn4

W3 Ca

W1 Mn1


W4

Biochemistry

For Table of Content Use Only

The Role of a Water Network around the Mn4CaO5 Cluster in Photosynthetic Water Oxidation: A Study by Fourier Transform Infrared Spectroscopy and QM/MM Calculation

Shin Nakamura, Kai Ota, Yuichi Shibuya, and Takumi Noguchi

YZ W6 W7 W5 W2 W3

W8 W9

W4

IR Intensity

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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W1 3200

3000

2800

2600

Wavenumber

Mn4CaO5


2400 (cm-1)

Role of a Water Network around the Mn4CaO5 Cluster in

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