Perturbing the Water Cavity Surrounding the Manganese Cluster by Mutating the Residue D1-Valine 185 Has a Strong Effect on the Water Oxidation Mechanism of Photosystem II

In oxygenic photosynthesis, light-driven oxidation of water to molecular oxygen is carried out by the oxygen-evolving complex (OEC) in photosystem II (PS II). Recently, we reported the room-temperature structures of PS II in the four (semi)stable S-states, S1, S2, S3, and S0, showing that a water molecule is inserted during the S2→ S3transition, as a new bridging O(H)-ligand between Mn1 and Ca. To understand the sequence of events leading to the formation of this last stable intermediate state before O2formation, we recorded diffraction and Mn X-ray emission spectroscopy (XES) data at several time points during the S2→ S3transition. At the electron acceptor site, changes due to the two-electron redox chemistry at the quinones, QAand QB, are observed. At the donor site, tyrosine YZand His190 H-bonded to it move by 50 µs after the second flash, and Glu189 moves away from Ca. This is followed by Mn1 and Mn4 moving apart, and the insertion of OX(H) at the open coordination site of Mn1. This water, possibly a ligand of Ca, could be supplied via a “water wheel”-like arrangement of five waters next to the OEC that is connected by a large channel to the bulk solvent. XES spectra show that Mn oxidation (τ of ∼350 µs) during the S2→ S3transition mirrors the appearance of OXelectron density. This indicates that the oxidation state change and the insertion of water as a bridging atom between Mn1 and Ca are highly correlated.

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Electron, proton and hydrogen–atom transfers in photosynthetic water oxidation

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2002.1135 ◽

2002 ◽

Vol 357 (1426) ◽

pp. 1383-1394 ◽

Cited By ~ 25

Author(s):

Cecilia Tommos

Keyword(s):

Photosystem Ii ◽

Proton Transfer ◽

Water Oxidation ◽

Oxidation Mechanism ◽

Bulk Solution ◽

Hydrogen Atoms ◽

Redox Active ◽

Hydrogen Atom Transfers ◽

Reduce Carbon Dioxide ◽

Photosynthetic Water Oxidation

When photosynthetic organisms developed so that they could use water as an electron source to reduce carbon dioxide, the stage was set for efficient proliferation. Algae and plants spread globally and provided the foundation for our atmosphere and for O 2 –based chemistry in biological systems. Light–driven water oxidation is catalysed by photosystem II, the active site of which contains a redox–active tyrosine denoted Y Z , a tetramanganese cluster, calcium and chloride. In 1995, Gerald Babcock and co–workers presented the hypothesis that photosynthetic water oxidation occurs as a metallo–radical catalysed process. In this model, the oxidized tyrosine radical is generated by coupled proton/electron transfer and re–reduced by abstracting hydrogen atoms from substrate water or hydroxide–ligated to the manganese cluster. The proposed function of Y Z requires proton transfer from the tyrosine site upon oxidation. The oxidation mechanism of Y Z in an inhibited and O 2 –evolving photosystem II is discussed. Domino–deprotonation from Y Z to the bulk solution is shown to be consistent with a variety of data obtained on metal–depleted samples. Experimental data that suggest that the oxidation of Y Z in O 2 –evolving samples is coupled to proton transfer in a hydrogen–bonding network are described. Finally, a dielectric–dependent model for the proton release that is associated with the catalytic cycle of photosystem II is discussed.

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The exchange of the fast substrate water in the S2 state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism

Chemical Science ◽

10.1039/d1sc02265b ◽

2021 ◽

Author(s):

Casper de Lichtenberg ◽

Christopher J. Kim ◽

Petko Chernev ◽

Richard J Debus ◽

Johannes Messinger

Keyword(s):

Photosystem Ii ◽

Molecular Oxygen ◽

Water Oxidation ◽

Oxidation Mechanism ◽

Bulk Water ◽

Oxygen Species ◽

S2 State ◽

Oxo Bridge

The molecular oxygen we breathe is produced from water-derived oxygen species bound to the Mn4CaO5 cluster in photosystem II (PSII). Present research points to the central oxo-bridge O5 as the...

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The mechanism for proton–coupled electron transfer from tyrosine in a model complex and comparisons with Y Z oxidation in photosystem II

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2002.1142 ◽

2002 ◽

Vol 357 (1426) ◽

pp. 1471-1479 ◽

Cited By ~ 39

Author(s):

Martin Sjödin ◽

Stenbjörn Styring ◽

Björn Åkermark ◽

Licheng Sun ◽

Leif Hammarström

Keyword(s):

Electron Transfer ◽

Photosystem Ii ◽

Water Oxidation ◽

Oxidation Mechanism ◽

Model System ◽

Proton Coupled Electron Transfer ◽

Tyrosine Oxidation ◽

Model Complex ◽

Primary Donor ◽

Mn Cluster

In the water–oxidizing reactions of photosystem II (PSII), a tyrosine residue plays a key part as an intermediate electron–transfer reactant between the primary donor chlorophylls (the pigment P 680 ) and the water–oxidizing Mn cluster. The tyrosine is deprotonated upon oxidation, and the coupling between the proton reaction and electron transfer is of great mechanistic importance for the understanding of the water–oxidation mechanism. Within a programme on artificial photosynthesis, we have made and studied the proton–coupled tyrosine oxidation in a model system and been able to draw mechanistic conclusions that we use to interpret the analogous reactions in PSII.

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Water oxidation chemistry of photosystem II

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2002.1136 ◽

2002 ◽

Vol 357 (1426) ◽

pp. 1395-1405 ◽

Cited By ~ 31

Author(s):

John S. Vrettos ◽

Gary W. Brudvig

Keyword(s):

Photosystem Ii ◽

Water Oxidation ◽

Ion Selectivity ◽

Bound Water ◽

Nucleophilic Attack ◽

Manganese Cluster ◽

Bond Forming ◽

Proton Coupled Electron Transfer ◽

Tyrosine Z ◽

Oxidation Chemistry

The O 2 –evolving complex of photosystem II catalyses the light–driven four–electron oxidation of water to dioxygen in photosynthesis. In this article, the steps leading to photosynthetic O 2 evolution are discussed. Emphasis is given to the proton–coupled electron–transfer steps involved in oxidation of the manganese cluster by oxidized tyrosine Z (Y Z ), the function of Ca 2+ and the mechanism by which water is activated for formation of an O–O bond. Based on a consideration of the biophysical studies of photosystem II and inorganic manganese model chemistry, a mechanism for photosynthetic O 2 evolution is presented in which the O–O bond–forming step occurs via nucleophilic attack on an electron–deficient Mn V =O species by a calcium–bound water molecule. The proposed mechanism includes specific roles for the tetranuclear manganese cluster, calcium, chloride, Y Z and His190 of the D1 polypeptide. Recent studies of the ion selectivity of the calcium site in the O 2 –evolving complex and of a functional inorganic manganese model system that test key aspects of this mechanism are also discussed.

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Amino acid residues involved in the coordination and assembly of the manganese cluster of photosystem II. Proton-coupled electron transport of the redox-active tyrosines and its relationship to water oxidation

Biochimica et Biophysica Acta (BBA) - Bioenergetics ◽

10.1016/s0005-2728(00)00220-6 ◽

2001 ◽

Vol 1503 (1-2) ◽

pp. 147-163 ◽

Cited By ~ 122

Author(s):

Bruce A Diner

Keyword(s):

Amino Acid ◽

Electron Transport ◽

Photosystem Ii ◽

Water Oxidation ◽

Amino Acid Residues ◽

Manganese Cluster ◽

Redox Active

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Water oxidation chemistry of photosystem II

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2007.2217 ◽

2007 ◽

Vol 363 (1494) ◽

pp. 1211-1219 ◽

Cited By ~ 153

Author(s):

Gary W Brudvig

Keyword(s):

Photosystem Ii ◽

Water Oxidation ◽

Oxidation Mechanism ◽

Intermediate Species ◽

X Ray ◽

Redox Active ◽

Ca Ions ◽

Oxidation Chemistry ◽

Chemical Problem ◽

Mechanism Of The Reaction

Photosystem II (PSII) uses light energy to split water into protons, electrons and O 2 . In this reaction, nature has solved the difficult chemical problem of efficient four-electron oxidation of water to yield O 2 without significant amounts of reactive intermediate species such as superoxide, hydrogen peroxide and hydroxyl radicals. In order to use nature's solution for the design of artificial catalysts that split water, it is important to understand the mechanism of the reaction. The recently published X-ray crystal structures of cyanobacterial PSII complexes provide information on the structure of the Mn and Ca ions, the redox-active tyrosine called Y Z and the surrounding amino acids that comprise the O 2 -evolving complex (OEC). The emerging structure of the OEC provides constraints on the different hypothesized mechanisms for O 2 evolution. The water oxidation mechanism of PSII is discussed in the light of biophysical and computational studies, inorganic chemistry and X-ray crystallographic information.

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What does the Sr-substituted 2.1 Å resolution crystal structure of photosystem II reveal about the water oxidation mechanism?

Chemical Communications ◽

10.1039/c3cc49324e ◽

2014 ◽

Vol 50 (24) ◽

pp. 3187-3190 ◽

Cited By ~ 19

Author(s):

Richard Terrett ◽

Simon Petrie ◽

Ron J. Pace ◽

Robert Stranger

Keyword(s):

Crystal Structure ◽

Photosystem Ii ◽

Water Oxidation ◽

Density Functional ◽

Oxidation Mechanism ◽

Functional Study ◽

Density Functional Study ◽

X Ray

The structure of the water oxidising complex in the Sr-substituted X-ray crystal structure of photosystem II and its differences relative to the Ca-containing system, have been rationalized by a density functional study.

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