Identifying carboxylate ligand vibrational modes in photosystem II with QM/MM methods.

The light-driven oxidation of water in photosystem II (PSII) produces nearly all of the molecular oxygen on Earth and drives the production of nearly all of Earth’s biomass. Determining the mechanism of O2 formation in PSII is one of the hottest topics in photosynthesis and has stimulated much interest in the development of artificial photosynthesis. The catalytic water-oxidizing center (WOC) consists of aMn4CaO5 cluster, nearby amino acid residues, and numerous surrounding water molecules (Fig. 1). Rapid progress in understanding the mechanism of O2 formation has been made in the last 5 years because of developments in crystallography (e.g., the development of free electron laser sources) and the interplay between new structural information, computational studies, and advanced biophysical methods such as pulsed EPR spectroscopy, X-ray absorbance spectroscopy, and membrane inlet mass spectrometry (1–4). FTIR spectroscopy is an additional biophysical method that has the advantage of being sensitive to the amino acid residues and water molecules that surround the Mn4CaO5 cluster. However, the interpretation ofmuch of the FTIR literature on PSII has been hampered by an inability to assign spectral features to specific residues or functional groups. In PNAS, Nakamura and Noguchi (5) address this problem by simulating FTIR difference spectra of the WOC in the symmetric carboxylate stretching region on the basis of quantum mechanics/molecular mechanics (QM/MM) methods. PSII is located in the thylakoid membranes of plants, algae, and cyanobacteria. It is a homodimer in vivo, having a total molecular weight of ∼700 kDa with each monomer containing at least 20 different subunits and nearly 60 organic and inorganic cofactors. The largest membrane-spanning subunits include CP47 (56 kDa), CP43 (52 kDa), D2 (39 kDa), and D1 (38 kDa). The Mn4CaO5 cluster is ligated by six carboxylate groups, one histidine side chain, and four water molecules. The histidine residue (H332) and five of the six carboxylate groups (D170, E189, E333,D342, and theC terminus at A344) are from D1, and one (E354) is from CP43. Recent 1.9and 1.95-Å crystallographic structures of PSII show that the Mn4CaO5 cluster is arranged as a distorted Mn3CaO4 cube that is linked to a fourth “dangling” Mn ion (denoted Mn4) by two oxo bridges (6, 7). Two water molecules (W1 and W2) coordinate to Mn4, and two (W3 and W4) coordinate to the Ca ion. Networks of hydrogen bonds in the Mn4CaO5 cluster’s environment efficiently transport protons away from the cluster and permit the access of water. Light-induced separations of charge within PSII drive the accumulation of oxidizing equivalents on the Mn4CaO5 cluster. During each catalytic cycle, the cluster accumulates four oxidizing equivalents, cycling through five oxidation states termed Sn, where “n” denotes the number of oxidizing Fig. 1. The Mn4CaO5 cluster and its ligation environment from the 1.95-Å X-ray crystallographic structure (7) (Protein Data Bank ID code 4UB6). For clarity, only selected residues are shown. Except as noted otherwise, all residues are from the D1 polypeptide. Purple spheres, manganese ions; yellow sphere, calcium; large red spheres, μ-oxo bridges; blue sphere, chloride; small red spheres, water molecules including the four water molecules bound to Mn4 (W1 andW2) and Ca (W3 andW4).