title: Ammonia binding to the oxygen-evolving complex of photosystem II identifies the solvent-exchangeable oxygen bridge (μ-oxo) of the manganese tetramer.
abstract: The assignment of the two substrate water sites of the tetra-manganese penta-oxygen calcium (Mn4O5Ca) cluster of photosystem II is essential for the elucidation of the mechanism of biological O-O bond formation and the subsequent design of bio-inspired water-splitting catalysts. We recently demonstrated using pulsed EPR spectroscopy that one of the five oxygen bridges (μ-oxo) exchanges unusually rapidly with bulk water and is thus a likely candidate for one of the substrates. Ammonia, a water analog, was previously shown to bind to the Mn4O5Ca cluster, potentially displacing a water/substrate ligand [Britt RD, et al. (1989) J Am Chem Soc 111(10):3522-3532]. Here we show by a combination of EPR and time-resolved membrane inlet mass spectrometry that the binding of ammonia perturbs the exchangeable μ-oxo bridge without drastically altering the binding/exchange kinetics of the two substrates. In combination with broken-symmetry density functional theory, our results show that (i) the exchangable μ-oxo bridge is O5 {using the labeling of the current crystal structure [Umena Y, et al. (2011) Nature 473(7345):55-60]}; (ii) ammonia displaces a water ligand to the outer manganese (MnA4-W1); and (iii) as W1 is trans to O5, ammonia binding elongates the MnA4-O5 bond, leading to the perturbation of the μ-oxo bridge resonance and to a small change in the water exchange rates. These experimental results support O-O bond formation between O5 and possibly an oxyl radical as proposed by Siegbahn and exclude W1 as the second substrate water.
authors.affiliation: Max-Planck-Institut für Chemische Energiekonversion, D-45470 Mülheim an der Ruhr, Germany.
authors.forename: Montserrat
authors.initials: M
authors.lastname: Pérez Navarro
authors.forename: William M
authors.initials: WM
authors.lastname: Ames
authors.forename: Håkan
authors.initials: H
authors.lastname: Nilsson
authors.forename: Thomas
authors.initials: T
authors.lastname: Lohmiller
authors.forename: Dimitrios A
authors.initials: DA
authors.lastname: Pantazis
authors.forename: Leonid
authors.initials: L
authors.lastname: Rapatskiy
authors.forename: Marc M
authors.initials: MM
authors.lastname: Nowaczyk
authors.forename: Frank
authors.initials: F
authors.lastname: Neese
authors.forename: Alain
authors.initials: A
authors.lastname: Boussac
authors.forename: Johannes
authors.initials: J
authors.lastname: Messinger
authors.forename: Wolfgang
authors.initials: W
authors.lastname: Lubitz
authors.forename: Nicholas
authors.initials: N
authors.lastname: Cox
mesh_terms: D000641:Ammonia / Q000378:metabolism*; D004583:Electrons; D008024:Ligands; D009682:Magnetic Resonance Spectroscopy; D008345:Manganese / Q000378:metabolism*; D010100:Oxygen / Q000378:metabolism*; D045332:Photosystem II Protein Complex / Q000737:chemistry / Q000378:metabolism*; D012997:Solvents / Q000378:metabolism*; D013113:Spin Labels; D014867:Water
chemical_list: D008024:Ligands; D045332:Photosystem II Protein Complex; D012997:Solvents; D013113:Spin Labels; D014867:Water; D008345:Manganese; D000641:Ammonia; D010100:Oxygen
keywords: Mn cluster; OEC; PSII; water oxidizing complex; water-oxidation
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