Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn ₄ CaO ₅ cluster in photosystem II

Abstract

During photosynthesis, the light-driven oxidation of water performed by photosystem II (PSII) provides electrons necessary to fix CO 2 , in turn supporting life on Earth by liberating molecular oxygen. Recent high-resolution X-ray images of PSII show that the wateroxidizing center (WOC) is composed of an Mn 4 CaO 5 cluster with six carboxylate, one imidazole, and four water ligands. FTIR difference spectroscopy has shown significant structural changes of the WOC during the S-state cycle of water oxidation, especially within carboxylate groups. However, the roles that these carboxylate groups play in water oxidation as well as how they should be properly assigned in spectra are unresolved. In this study, we performed a normal mode analysis of the WOC using the quantum mechanics/ molecular mechanics (QM/MM) method to simulate FTIR difference spectra on the S 1 to S 2 transition in the carboxylate stretching region. By evaluating WOC models with different oxidation and protonation states, we determined that models of high-oxidation states, Mn(III) 2 Mn(IV) 2 , satisfactorily reproduced experimental spectra from intact and Ca-depleted PSII compared with low-oxidation models. It is further suggested that the carboxylate groups bridging Ca and Mn ions within this center tune the reactivity of water ligands bound to Ca by shifting charge via their π conjugation.T he oxidation of water, performed by photosystem II (PSII) in plants and cyanobacteria, is a crucial part of the photosynthesis process, providing a source of electrons used for CO 2 fixation. This process also produces molecular oxygen as a byproduct; this "waste" oxygen is released to the atmosphere, where it plays an essential role in sustaining life on Earth. The catalytic site of water oxidation is a water-oxidizing center (WOC) located in the electron-donor side of PSII (1-3). Recent high-resolution (1.9-1.95 Å) X-ray crystallographic structures of PSII (4, 5) revealed that the WOC core is an Mn 4 CaO 5 cluster fixed to the protein by six carboxylate [D1-D170, D1-E189, D1-E333, D1-D342, D1-A344 (C terminus), and CP43-E354] ligands and one imidazole (D1-H332) ligand. Four water ligands are also bound to Mn 4 (W1 and W2) and Ca (W3 and W4) (Fig. 1B shows numbering of the Mn ions and water ligands); several water molecules also exist around the Mn 4 CaO 5 cluster, forming a hydrogen bond network (Fig. 1A). Because of the absence of the information of hydrogen atoms in the X-ray structures, however, the protonation states of the water and oxo ligands in Mn 4 CaO 5 as well as the structure of the hydrogen bond network remain to be clarified.The water-oxidizing reaction proceeds through a cycle of five intermediates designated as S n states (n = 0−4) (6, 7), where S 1 is the most stable in the dark. Oxidation of the Mn 4 CaO 5 cluster by a Y Z • radical, produced by light-induced charge separation, advances the S n state (n = 0−3) to the S n + 1 state. The S 4 state immediately relaxes to the S 0 state on release of O 2 . The oxidation states of the Mn atoms wi...

On the comparison between differential vibrational spectroscopy spectra and theoretical data in the carboxyl region of photosystem II

“…In particular, we selected two different mutants, one reported as non-influencing mutant (E189Q; Strickler et al 2006) and another as high-influencing mutant (D61A; Debus 2014), regarding the intensities of the differential IR spectra (see Table 2). As comparison and control, we present the double differential spectra of the isotope labeled 13 C-1 A344 (WT* in Table 2, see Figs 5 and 6 for spectra), similarly as what previously reported by another work (Nakamura and Noguchi 2016). In the latter case, as expected, the effect of the isotopic exchange is localized in a relatively small spectral window, modifying mainly the neighborhood of the A344.…”

“…To show the weaknesses and the critical points of the direct calculation of difference spectra, in the present work, we investigated several models of the natural Mn 4 Ca cluster present in PSII. As first, similar to what reported in a recent work (Nakamura and Noguchi ), we considered two different protonation patterns, in which the W2 molecule coordinating the Mn4 ion is present either as hydroxide or water molecule. In agreement with the previous study, we found a dramatic effect of the specific protonation of the W1 and W2 molecules, namely, PP1 (W1 = H 2 O, W2 = OH) and PP2 (W1 = H 2 O, W2 = H 2 O), on the calculated differential spectra (Fig.…”

“…In particular, the protonation pattern for the region surrounding the Mn 4 Ca cluster has been extensively studied by several energetic studies (Galstyan et al , Milikisiyants et al , Pantazis et al , Siegbahn , Shoji et al , Askerka et al , Ugur et al ), establishing PP1 as the most probable pattern. Despite these evidences, the second PP2 pattern is reported to have a better agreement with vibrational spectra (Nakamura and Noguchi , Wilson and Jain ).…”

D1-Asn-298 in photosystem II is involved in a hydrogen-bond network near the redox-active tyrosine YZ for proton exit during water oxidation

“…Characteristic bands at 1450 -1350 cm Ϫ1 are due to the symmetric COO Ϫ stretching vibrations (78, 80 -85), whereas the coupled asymmetric COO Ϫ stretching bands appear at 1600 -1500 cm Ϫ1 , overlapping the amide II bands (NH bending and CN stretching vibrations of backbone amides) (78,82). The changes of these COO Ϫ bands during the S-state cycle are attributed to the structural changes of carboxylate residues around the Mn 4 CaO 5 cluster (80,81,(83)(84)(85). The obtained spectra showed characteristic features depending on the flash number, especially in the symmetric COO Ϫ region around 1400 cm Ϫ1 , reflecting high efficiencies of the S-state transitions.…”

Substrate water exchange in the S2 state of photosystem II is dependent on the conformation of the Mn4Ca cluster

“…The Ca ion and four Mn ions are connected by five oxo-bridges, and Ca and Mn4 bind two terminal water ligands each (W1-W4; W2 may be a hydroxo ligand). [27][28][29][30] The remaining coordination sites of the Mn 4 Ca cluster are completed by bridging carboxy ligands supplied by the D1 and CP43 proteins of PSII (not shown). The only exception is the Mn1 site, which features one histidine ligand and is five-coordinate.…”