title: Alternating electron and proton transfer steps in photosynthetic water oxidation.
abstract: Water oxidation by cyanobacteria, algae, and plants is pivotal in oxygenic photosynthesis, the process that powers life on Earth, and is the paradigm for engineering solar fuel-production systems. Each complete reaction cycle of photosynthetic water oxidation requires the removal of four electrons and four protons from the catalytic site, a manganese-calcium complex and its protein environment in photosystem II. In time-resolved photothermal beam deflection experiments, we monitored apparent volume changes of the photosystem II protein associated with charge creation by light-induced electron transfer (contraction) and charge-compensating proton relocation (expansion). Two previously invisible proton removal steps were detected, thereby filling two gaps in the basic reaction-cycle model of photosynthetic water oxidation. In the S(2) → S(3) transition of the classical S-state cycle, an intermediate is formed by deprotonation clearly before electron transfer to the oxidant (Y Z OX). The rate-determining elementary step (τ, approximately 30 µs at 20 °C) in the long-distance proton relocation toward the protein-water interface is characterized by a high activation energy (E(a) = 0.46 ± 0.05 eV) and strong H/D kinetic isotope effect (approximately 6). The characteristics of a proton transfer step during the S(0) → S(1) transition are similar (τ, approximately 100 µs; E(a) = 0.34 ± 0.08 eV; kinetic isotope effect, approximately 3); however, the proton removal from the Mn complex proceeds after electron transfer to . By discovery of the transient formation of two further intermediate states in the reaction cycle of photosynthetic water oxidation, a temporal sequence of strictly alternating removal of electrons and protons from the catalytic site is established.
authors.affiliation: Physics Department, Freie Universität Berlin, 14195 Berlin, Germany.
authors.forename: André
authors.initials: A
authors.lastname: Klauss
authors.forename: Michael
authors.initials: M
authors.lastname: Haumann
authors.forename: Holger
authors.initials: H
authors.lastname: Dau
mesh_terms: D001692:Biological Transport; D004579:Electron Transport; D007700:Kinetics; D008954:Models, Biological; D010084:Oxidation-Reduction; D010788:Photosynthesis / Q000502:physiology*; D045332:Photosystem II Protein Complex / Q000378:metabolism*; D011522:Protons; D013057:Spectrum Analysis / Q000379:methods; D018724:Spinacia oleracea; D014867:Water / Q000737:chemistry*
chemical_list: D045332:Photosystem II Protein Complex; D011522:Protons; D014867:Water