Short Hydrogen Bond between Redox-Active Tyrosine Y_Zand D1-His190 in the Photosystem II Crystal Structure

Abstract

The crystal structure of photosystem II (PSII) analyzed at a resolution of 1.9 Å revealed a remarkably short H-bond between redox-active tyrosine Y(Z) and D1-His190 (2.46 Å donor-acceptor distance). Using large-scale quantum mechanical/molecular mechanical (QM/MM) calculations with the explicit PSII protein environment, we were able to reproduce this remarkably short H-bond in the original geometry of the crystal structure in the neutral [Y(Z)O···H···N(ε)-His-N(δ)H···O═Asn] state, but not in the oxidized states, indicating that the neutral state was the one observed in the crystal structure. In addition to the appropriate redox/protonation state of Y(Z) and D1-His190, we found that the presence of a cluster of water molecules played a key role in shortening the distance between Y(Z) and D1-His190. The orientations of the water molecules in the cluster were energetically stabilized by the highly polarized PSII protein environment, where the Ca ion of the oxygen-evolving complex (OEC) and the OEC ligand D1-Glu189 were also involved.

Mechanism of tyrosine D oxidation in Photosystem II

“…The atomic charges of Chla, pheophytin a, and quinones were taken from our previous studies on PSII (47). We considered the Mn 4 CaO 5 cluster as the (O4) 2− (O5)H − model (26) in the S1 state.…”

“…We used the QSite (48) program code as utilized in previous studies (26). Owing to the large system size of PSII, we considered residues and cofactors in only subunits D1, D2, CP47, and CP43 as the protein environment.…”

“…S1). The results indicated that the cluster of waters near TyrZ was responsible for tuning the crucial pK a values (26) . In contrast, the corresponding H-bond between TyrD and D2-His189 is of standard length: 2.74 Å (for TyrD-OH and TyrD-O • ).…”

“…In the 1.9-Å crystal structure (1), the H-bond from TyrZ-OH to D1-His190 (O TyrZ −N D1-His190 ) is unusually short, 2.46 Å. QM/MM calculations have reproduced the O TyrZ −N D1-His190 distance (2.47 Å) (26). Remarkably, the potential-energy profile indicated that this H-bond is a barrier-less, single-well (ionic) H-bond, an unusually short H-bond that can be formed only when the pK a difference between donor and acceptor is nearly zero (27)(28)(29)(30) (Fig.…”

Proton transfer reactions and hydrogen-bond networks in protein environments

“…This indicates that the unusually short H-bond is not stable in the protein environment, in particular if the matching pK a condition for the H-bond donor and acceptor moieties is satisfied only transiently near the protein surface. (For comparison, see also the case of an unusually short H-bond between D1-Tyr161 and D1-His190 in PSII [1,64]; here the matching pK a condition is satisfied easily in the protein inner core, without tuning the original pK a values of the donor and acceptor moieties. Discussed later, see 'Presence of an unusually short, but stable H-bond in redox-active D1-Tyr161 (TyrZ) in photosystem II'.)…”