title: Mono-manganese mechanism of the photosystem II water splitting reaction by a unique Mn4Ca cluster.
abstract: The molecular mechanism of the water oxidation reaction in photosystem II (PSII) of green plants remains a great mystery in life science. This reaction is known to take place in the oxygen evolving complex (OEC) incorporating four manganese, one calcium and one chloride cofactors, that is light-driven to cycle four intermediates, designated S(0) through S(4), to produce four protons, five electrons and lastly one molecular oxygen, for indispensable resources in biosphere. Recent advancements of X-ray crystallography models established the existence of a catalytic Mn(4)Ca cluster ligated by seven protein amino acids, but its functional structure is not yet resolved. The (18)O exchange rates of two substrate water molecules were recently measured for four S(i)-state samples (i=0-3) leading to (34)O(2) and (36)O(2) formations, revealing asymmetric substrate binding sites significantly depending on the S(i)-state. In this paper, we present a chemically complete model for the Mn(4)Ca cluster and its surrounding enzyme field, which we found out from some possible models by using the hybrid density functional theoretic geometry optimization method to confirm good agreements with the 3.0 A resolution PSII model [B. Loll, J. Kern, W. Saenger, A. Zouni , J. Biesiadka, Nature 438 (2005) 1040-1044] and the S-state dependence of (18)O exchange rates [W. Hillier and T. Wydrzynski, Phys. Chem. Chem. Phys. 6 (2004) 4882-4889]. Furthermore, we have verified that two substrate water molecules are bound to asymmetric cis-positions on the terminal Mn ion being triply bridged (mu-oxo, mu-carboxylato, and a hydrogen bond) to the Mn(3)CaO(3)(OH) core, by developing a generalized theory of (18)O exchange kinetics in OEC to obtain an experimental evidence for the cross exchange pathway from the slow to the fast exchange process. Some important experimental data will be discussed in terms of this model and its possible tautomers, to suggest that a cofactor, Cl(-) ion, may be bound to CP43-Arg357 nearby Ca(2+) ion and that D1-His337 may be used to trap a released proton only in the S(2)-state.
authors.affiliation: Department of Physics, School of Science and Technology, Meiji University, Tama-ku, Kawasaki, Kanagawa 214-8571, Japan. kusunoki@isc.meiji.ac.jp
authors.forename: Masami
authors.initials: M
authors.lastname: Kusunoki
mesh_terms: D001665:Binding Sites; D004578:Electron Spin Resonance Spectroscopy; D007700:Kinetics; D008345:Manganese / Q000737:chemistry / Q000378:metabolism*; D008956:Models, Chemical; D010084:Oxidation-Reduction; D010100:Oxygen / Q000737:chemistry / Q000378:metabolism; D010103:Oxygen Isotopes / Q000737:chemistry; D010788:Photosynthesis / Q000502:physiology; D045332:Photosystem II Protein Complex / Q000737:chemistry / Q000378:metabolism*; D013237:Stereoisomerism; D014867:Water / Q000737:chemistry / Q000378:metabolism*
chemical_list: D010103:Oxygen Isotopes; D045332:Photosystem II Protein Complex; D014867:Water; D008345:Manganese; D010100:Oxygen