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. 2022 May 30;2(5):423–429. doi: 10.1021/acsphyschemau.2c00019

Release of a Proton and Formation of a Low-Barrier Hydrogen Bond between Tyrosine D and D2-His189 in Photosystem II

Manoj Mandal †, Keisuke Saito ‡,§, Hiroshi Ishikita ‡,§,*
PMCID: PMC9955220  PMID: 36855688

Abstract

graphic file with name pg2c00019_0005.jpg

In photosystem II (PSII), the second-lowest oxidation state (S1) of the oxygen-evolving Mn4CaO5 cluster is the most stable, as the radical form of the redox-active D2-Tyr160 is considered to be a candidate that accepts an electron from the lowest oxidation state (S0) in the dark. Using quantum mechanical/molecular mechanical calculations, we investigated the redox potential (Em) of TyrD and its H-bond partner, D2-His189. The potential energy profile indicates that the release of a proton from the TyrD...D2-His189 pair leads to the formation of a low-barrier H-bond. The Em depends on the H+ position along the low-barrier H-bond, e.g., 680 mV when the H+ is at the D2-His189 moiety and 800 mV when the H+ is at the TyrD moiety, which can explain why TyrD mediates both the S0 to S1 oxidation and the S2 to S1 reduction.

Keywords: low-barrier hydrogen bond, redox-active tyrosine, histidine radical, delocalized H-bond network, proton-coupled electron transfer, oxygen-evolving complex, dark adaptation, photoactivation

Introduction

Oxygen evolution occurs at the catalytic Mn4CaO5 cluster in photosystem II (PSII), removing four electrons and four protons from two substrate water molecules. To oxidize the water molecules, the electron transfer pathway proceeds from the Mn4CaO5 cluster via a H-bond pair, the redox-active tyrosine (TyrZ) and D1-His190, toward chlorophyll [PD1/PD2]•+ (Figure 1). As electron transfer occurs, the oxidation state of the Mn4CaO5 cluster, Sn, increases from S0 to S3 via S1 and S2: S0 → S1 → S2 → S3 → S0 (e.g.,1,2), and O2 evolves in the S3-to-S0 transition. In the proton-coupled electron transfer, the neutral radical TyrZ• is transiently formed upon oxidation of TyrZ by [PD1/PD2]•+ on a timescale of tens to hundreds of nanoseconds in intact PSII.3,4

Figure 1.

Figure 1

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Redox-active groups on the lumenal side of PSII. Dotted lines indicate H-bonds for the tyrosine–histidine pairs.

TyrZ forms an unusually short (2.46 Å5) low-barrier H-bond with Nε of D1-His190,6 facilitating proton-coupled electron transfer.6,7 Low-barrier H-bonds can form only when the pKa values of the H-bond donor and acceptor moieties are nearly equal.8−10 The H+ can be delocalized along the low-barrier H-bond, whereas the redox potential11 and absorption wavelength12 change in response to the H+ movement. This does not necessarily mean that these values fluctuate in the proteins, as low-barrier H-bonds often appear in the transition intermediate states (e.g., during the photocycles in microbial rhodopsins and photoreceptors12,13). The low-barrier H-bond formation is observed when proton transfer occurs in PSII, e.g., TyrZ and D1-His190,6,7 QB and D1-His215,14 a ligand water molecule (W1) of the Mn4CaO5 cluster and D1-Asp61,15,16 and the O4 site of the Mn4CaO5 cluster and the O4–water chain.17,18

In contrast, the H-bond distance between D2-Tyr160 (TyrD) and D2-His189 on the D2 side is longer (2.74 Å in the crystal structure).5 TyrD is not involved in the electron transfer pathway from the Mn4CaO5 cluster. However, the neutral deprotonated radical TyrD-O• is formed upon oxidation of TyrD-OH by [PD1/PD2]•+19−22 and this occurs in a tens of ms timescale23 (also see ref (24)). The proton released from TyrD-OH is transferred along the downhill proton transfer pathway that proceeds via D2-Arg180 and a series of waters toward D2-His61, the protein bulk surface.25−27 Thus, once formed, TyrD-O• is highly stable for several hours.19,21 This suggests that normal enzyme activity occurs in the presence of the tyrosine radical.21 TyrD-O• was also observed in the D2-His189 mutant proteins,28,29 which confirms that TyrD is redox-active. In response to the TyrD-O• formation, a water molecule, which accepts a H-bond from TyrD-OH (i.e., proximal water-binding position), moves toward D2-Arg180 (i.e., distal water-binding position).5,25 In the dark-adapted PSII crystal structure, the water molecule is observed at both the proximal and distal positions,30 which indicates that TyrD-OH and TyrD-O• coexist.

It has been considered that TyrD-O• serves as an electron acceptor from S0 in the dark and is the component that stabilizes the second-lowest oxidation state of the Mn4CaO5 cluster, S1, rather than the lowest oxidation state, S0 (e.g.,21). Long adaptation of PSII to the darkness results in the oxidation of S0 to S1 via electron transfer from S0 to TyrD-O•.21,31,32 In pea thylakoids, S0 disappears in ∼20 min.31 On the other hand, TyrD-O– donates the electron to S2, reducing it to S1 in the dark.21,32 TyrD-O• could be formed in the seconds timescale upon illumination33 because higher S-states (e.g., S2 and S3) are formed upon illumination and then reduced to S1 upon oxidation of TyrD-OH to TyrD-O•.34 This was confirmed by the two-flash-illuminated structure (S3: 46%).30 Based on the negative peak at the proximal water-binding position in the two-flash-minus-dark isomorphous difference Fourier map, Suga et al. reported that the water molecule moves toward the distal binding position, forming TyrD-O•,30 as originally suggested in theoretical studies by Saito et al.25

Thus, the presence of TyrD is likely to be associated with S1 being the most stable oxidation state in PSII. Based on these findings, it seems plausible to assume that Em(S0/S1) < Em(TyrD) < Em(S2/S1).35 Using the PSII crystal structure and solving the linear Poisson–Boltzmann equation, it was reported that Em(TryD) is 690 mV, which is >200 mV lower than Em(TyrZ).36 The difference between Em(TyrZ) and Em(TyrD) is due to the difference in the protonation state of the H-bond partner D1-Asn298, which allows D1-His190 to protonate at the Nδ site, or D2-Arg294, which does not allow D2-His189 to protonate at the Nδ site.36 The calculated Em difference between Em(TyrZ) and Em(TyrD) is consistent with the experimentally estimated Em difference of 240 mV.37 Similar values for Em(TyrD) and Em(TyrZ) have also been obtained using a quantum mechanical/molecular mechanical (QM/MM) approach based on the PSII crystal structure.38 This approach also allows the calculation of the Em for the Mn4CaO5 cluster based on the molecular orbital energy levels. However, among the calculated Em values, Em(TyrD) is the lowest (680 mV), even lower than Em(S0/S1) (730 mV).38 The low Em(TyrD) value is due to the absence of the protein electrostatic environment that can increase Em(TyrD-O•/–) (note: Em(Tyr-O•/–) = 680 mV in water39). If the TyrD...D2-His189 H-bond is a low-barrier H-bond, electron transfer may be pronounced, altering the Em value in response to the H+ movement.11 That is, both the Tyr and His moieties ultimately contribute to the redox activity of the Tyr...His H-bond. However, the TyrD...D2-His189 H-bond is not a low-barrier H-bond in the redox/protonation state of the crystal structure.25 It is unclear how Em(S0/S1) < Em(TyrD) < Em(S2/S1)35 can be explained in terms of the PSII protein environment of the reported PSII crystal structures. Here, we specifically focused on TyrD and re-examined the factors that affect Em(TyrD) in the PSII protein environment, using a QM/MM approach based on the PSII crystal structure.

Methods

The atomic coordinates of PSII were obtained from the PSII crystal structure (PDB code, 3ARC).5 The atomic charges of the other cofactors in the MM region were taken from a previous study.40

Em Calculations

The highest occupied molecular orbital (HOMO) energy level is largely correlated with Em for one-electron oxidation (e.g.,41,42), whereas the lowest unoccupied molecular orbital (LUMO) energy level is largely correlated with Em for one-electron reduction (e.g.,43). We included all redox-active cofactors (Mn4CaO5 cluster, TyrZ, PD1, and PD2) simultaneously in the QM region44,45 (see below), identified HOMOs of Mn4CaO5, TyrZ, PD1, and PD2 in S1 on the basis of the Mulliken population analysis46 (results provided in a previous study38), and obtained the Em values. The Em values of the redox sites are calculated using eq 1

graphic file with name pg2c00019_m001.jpg 1

where EHOMO is the HOMO energy level (meV).11,38,47 Although eq 1 was obtained only assuming that Em(TyrD) = 680 mV and Em(TyrZ) = 970 mV,35,36 it reproduced Em(PD1) and Em(PD2) of 1100–1200 mV.48,49 In addition, eq 1 reproduced Em(PD1) < Em(PD2),50,51 which is consistent with the experimentally measured larger PD1•+ population than PD2•+.52−54 Furthermore, eq 1 yielded Em(S0/S1) = 730 mV,38 which is 100 mV lower than Em(S1/S2) and Em(S2/S3): the uniquely low Em(S0/S1) value is consistent with the Em(S0/S1) value estimated previously.35,55

QM/MM Calculations

The unrestricted density functional theory method was employed with the B3LYP functional using the QSite program.56 The LANL2DZ basis set is considered for Mn and Ca atoms and the 6-31G* basis set is used for other atoms (i.e., LACVP*).57 A diffusion function was not used in the present study, as (i) no significant difference in the geometry was observed with a diffusion function58 and (ii) the Mn sites were >25 Å away from the focusing TyrD...D2-His189 H-bond. In the present study, the Mn4CaO5 cluster was included in the QM region to compare the Em values between the TyrD...D2-His189 pair and the Mn4CaO5 cluster. See refs (15, 17, 38, 58, 59) for the detailed electronic structure of the Mn4CaO5 cluster.

The QM and MM regions interact via Coulombic interaction between MM charges and the QM wavefunction (electrostatic embedding QM/MM scheme) and van der Waals interaction between QM and MM atoms (both of which employ van der Waals parameters).56 Note that the QSite’s frozen-orbital methodology was not used to build the QM/MM interface. In the QM region, all of the atomic coordinates were fully relaxed (rigid convergence criterion with a self-consistent field (SCF) energy convergence threshold of 5.0 × 10–6 [hartree] and an SCF density convergence threshold of 5.0 × 10–7 [hartree]). In the MM region, the positions of the H atoms were optimized using the OPLS2005 force field,60 while the positions of the heavy atoms were fixed.

For Em calculations, the Mn4CaO5 cluster was considered to be in S0 with antiferromagnetically coupled Mn ions; the resulting Mn oxidation states (Mn1, Mn2, Mn3, Mn4) and the magnetic spin quantum number Ms were (III, IV, III, III) and 1/261,62 (↑↓↑↓) (corresponding to the spin multiplicity 2S + 1 = 2) in S0. O1–O3 and O5 were considered to be unprotonated (O2–) and O4 was considered to be protonated (OH–) in S0.17,18,63−65 The results are likely to remain unchanged even if O1–O4 are unprotonated and O5 is protonated because the distances between the Mn4CaO5 cluster and TyrD are sufficiently large and nearly equal (O4...TyrD = 30 Å and O5...TyrD = 28 Å5). The four water ligand molecules, W1–W4, were considered to be water molecules (H2O). The Mn4CaO5 geometry was obtained from our previous studies.15,17 The initial-guess wavefunctions were obtained using the ligand field theory66 implemented in the QSite program. The QM region was defined as the Mn4CaO5 cluster (including the ligand side chains of D1-Asp170, D1-Glu189, D1-His332, D1-Glu333, D1-Asp342, and CP43-Glu354, and the backbone of D1-Ala344), ligand water molecules of W1–W4, O4–water chain (W539, W538, and W393), Cl-1 binding site (Cl-1, W442, W446, and side chains of D1-Asn181 and D2-Lys317), second-sphere ligands (side chains of D1-Asp61 and CP43-Arg357), the H-bond network of TyrZ (side chains of D1-Tyr161, D1-His190, and D1-Asn298), a diamond-shaped cluster of water molecules6 (W5, W6, and W7), and PD1/PD2. The MM region was defined as the entire PSII protein, as in a previous study.38 D1-His337 was considered to be protonated,67 whereas all other titratable groups were in the standard protonation states. See ref (38) for the QM/MM-optimized atomic coordinates.

According to Schutz and Warshel, the identification of a low-barrier H-bond is valid only if the shape of the potential energy profile of the H-bond is symmetric.9 As H atoms are not identified in the original PSII crystal structure,5 the QM/MM-optimized geometry is needed to analyze the potential energy profiles of the H-bond. To obtain the potential energy profiles of the O···H···N H-bond between TyrD and D2-His189, the LACVP* basis set68 was employed if not otherwise specified. The QM region was defined as [TyrD (D2-Tyr160), D2-His189, D2-Arg294, CP47-Glu364], whereas other protein units and all cofactors were approximated by the MM force field. Note that the influence of the Mn4CaO5 cluster on the TyrD...D2-His189 H-bond can be approximated as the MM region (e.g., O4...TyrD = 30 Å and O5...TyrD = 28 Å5). The QM/MM-optimized geometry was used as the initial geometry. The H atom under investigation was moved between O and N by 0.05 Å before the geometry was optimized by constraining the O–H and H–N distances, and the energy was calculated. This procedure was repeated until the H atom reached the O and N atoms. See the Supporting Information for the atomic coordinates of the QM/MM-optimized geometry.

Results and Discussion

The neutral radical TyrD-O• exists when the proton is at the D2-His189 moiety (forming singly protonated His189-NH; OTyrD...ND2-His189 = 2.75 Å, OTyrD...H...ND2-His189 = 173.5°), whereas the neutral radical His189-N• exists when the proton is at the TyrD moiety (forming TyrD-OH, OTyrD...ND2-His189 = 2.71 Å, OTyrD...H...ND2-His189 = 176.2°)25 (Figure 2). These OTyrD...ND2-His189 are close to 2.74 Å in the crystal structure,5 which corresponds to protonated TyrD-OH.25

Figure 2.

Figure 2

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H-bond network of the TyrD...D2-His189 pair. (a) TyrD-O•. (b) His189-N•. (c) Low-barrier H-bond pair. H+ is at the D2-His189 moiety. (d) Low-barrier H-bond pair. H+ is at the TyrD moiety. Cyan balls indicate the proton along the TyrD...D2-His189 H-bond. Red and blue spheres indicate HOMO.

The potential energy profile suggests that TyrD and D2-His189 form a low-barrier H-bond [TyrD-O...H...N-His189]− in response to the release of the proton from TyrD-OH...N-His189-NH (Figure 3a). The low-barrier H-bond is also observed when the potential energy profile is analyzed using other basis sets (6-31G(tm),69Figure S1a) or functionals (B97D,70Figure S2a). The low-barrier H-bond [TyrD-O...H...N-His189]− is likely to exist prior to electron transfer, as high-frequency electron nuclear double-resonance spectroscopy studies suggested that D2-His189 was already deprotonated prior to electron transfer.71 Fourier transform infrared (FTIR) spectroscopy showed that TyrD is involved in a strong H-bond at high pH (i.e., deprotonation of the H-bond is pronounced), which is in line with the present finding of the low-barrier H-bond between TyrD and D2-His189.72 The OTyrD...ND2-His189 distance is significantly shortened to 2.55 Å in response to the low-barrier H-bond formation. Both the H-bond distance OTyrD...ND2-His189 and the H-bond angle OTyrD...H...ND2-His189 remain at 2.55 Å and ∼180° independently of the H+ position (e.g., 2.55 and 178.5° for [TyrD-OH...N-His189]− and 2.55 Å and 178.2° for [TyrD-O...HN-His189]−), which is consistent with the features of low-barrier H-bonds.

Figure 3.

Figure 3

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Proton-coupled electron transfer via TyrD. (a) Potential-energy profile of the H-bond for [TyrD-O...H...N-His189]− and [TyrD-O...H...N-His189]•. The left panels indicate the proton transfer pathway from TyrD toward the protein bulk surface.25−27 Note that each conformation (black closed circle) is the QM/MM-optimized geometry. (b) Shifts in the cofactor Em values in response to the H+ migration along the TyrD...D2-His189 H-bond. Vertical arrows indicate electron transfer. Black horizontal lines indicate the “redox-active” H+ positions, which facilitate electron transfer in the S0 to S1 oxidation and S2 to S1 reduction.

The low-barrier H-bond formation between TyrD and D2-His189 resembles that between TyrZ and D1-His190.6,7 However, the mechanism for the low-barrier H-bond formation differs: pKa(TyrZ-OH/TyrZ-O–) ≈ pKa(HN-His190-NH+/HN-His190-N) for the TyrZ...D1-His190 H-bond, whereas pKa(TyrD-OH/TyrD-O–) ≈ pKa(N-His189-NH/N-His189-N–) for the TyrD...D2-His189 H-bond. In the TyrZ...D1-His190 pair, a cluster of water molecules at the Mn4CaO5 ligand moiety donates a H-bond to TyrZ, decreasing pKa(TyrZ) to the level of pKa(HN-His190-NH+/HN-His190-N) (∼7 in water).6 On the other hand, anionic D2-His189 prevents TyrD-OH deprotonation, thereby increasing pKa(TyrD) to the level of pKa(N-His189-NH/N-His189-N–) (∼14 in water73). Note that the difference in the histidine protonation state is due to the difference in the H-bond partner D1-Asn298, which allows D1-His190 to protonate at the Nδ site, or D2-Arg294, which does not allow D2-His189 to protonate at the Nδ site.36

The Em value for [TyrD-O...H...N-His189]−/• depends on the H+ position along the low-barrier H-bond (Figure 3b), as observed for the low-barrier H-bond between TyrZ and D1-His190.11 The Em value at the TyrD moiety, Em(TyrD-O–/•), increases as the H+ moves toward the TyrD moiety and decreases as it moves toward the His189 moiety. The observed Em dependence of the entire low-barrier H-bond [TyrD-O...H...N-His189]− pair on the H+ position ultimately originates from Em(N-His-N•/–) = ∼790 mV in water,7,74 which is ∼100 mV higher than Em(Tyr-O•/–) (= 680 mV39). These results confirm that the H+ transfer of only ∼0.4 Å can alter Em by ∼100 mV (Figure 3b) in low-barrier H-bonds.11

Figure 3b shows that Em(TyrD-O–/•) = 670 mV and Em(His189-N–/•) = 970 mV when the H+ is at the D2-His189 moiety; Em(TyrD-O–/•) (= 830 mV) is close to Em(His189-N–/•) (= 800 mV) when the H+ is at the TyrD moiety. As Em(S0/S1) = ∼700 mV,35,38 the TyrD...D2-His189 pair can serve as an electron acceptor for S0 during the oxidation of S0 to S1 in the dark (dark adaptation) (Figure 3b). The similar Em values suggest that the two moieties can substantially and cooperatively serve as an electron acceptor from S0/S1. Even if Em(S0/S1) was lower (e.g., −100 mV estimated by Amin et al.75), the TyrD...D2-His189 pair could serve as an electron acceptor for S0.

On the other hand, the TyrD...D2-His189 pair can also serve as an electron acceptor for S2 during the rapid decay of S2 to S1 in the dark,21,31,32 as Em(S2/S1) = 830 mV38 is higher than Em for the TyrD...D2-His189 pair, especially when H+ is at the D2-His189 moiety (Figure 3b). Although this does not necessarily mean that the histidine radical is involved in the electron transfer, the characteristics of the D2-His189 moiety are pronounced when the TyrD...D2-His189 H-bond serves as an electron donor to S2/S1.

In summary, TyrD and D2-His189 can form a low-barrier H-bond in response to the release of the proton toward the protein bulk surface (Figure 3a). The Em value depends on the H+ position along the low-barrier H-bond. This may explain why TyrD mediates both the S0 to S1 oxidation and the S2 to S1 reduction, serving as both an electron acceptor and an electron donor.

Acknowledgments

This research was supported by JST CREST (JPMJCR1656 to H.I.), JSPS KAKENHI (18H05155, 18H01937, 20H03217, and 20H05090 to H.I., 16H06560 and 18H01186 to K.S.), and the Interdisciplinary Computational Science Program in CCS, University of Tsukuba (to K.S.). M.M. thanks the Department of Biotechnology, Government of India, for the Ramalingaswami Re-entry Fellowship scheme.

Supporting Information Available

The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsphyschemau.2c00019.

  • Potential energy profiles for H-bonds analyzed using the 6-31G(tm) basis set or the B97D functional (PDF)

  • QM/MM-optimized atomic coordinates of TyrD-O• and His189-N• (TXT)

The authors declare no competing financial interest.

Supplementary Material

pg2c00019_si_001.pdf (85KB, pdf)
pg2c00019_si_002.txt (74.9KB, txt)

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