BBA - Bioenergetics (v.1503, #1-2)

Photosynthetic water oxidation by Jonathan Nugent (1).

Remembering Melvin P. Klein (1921–2000) by R.David Britt; Kenneth Sauer; Vittal K Yachandra (2-6).

The mechanism by which the Mn-containing oxygen evolving complex (OEC) produces oxygen from water has been of great interest for over 40 years. This review focuses on how X-ray spectroscopy has provided important information about the structure of this Mn complex and its intermediates, or S-states, in the water oxidation cycle. X-ray absorption near-edge structure spectroscopy and high-resolution Mn Kβ X-ray emission spectroscopy experiments have identified the oxidation states of the Mn in the OEC in each of the intermediate S-states, while extended X-ray absorption fine structure experiments have shown that 2.7 Å Mn–Mn di-μ-oxo and 3.3 Å Mn–Mn mono-μ-oxo motifs are present in the OEC. X-ray spectroscopy has also been used to probe the two essential cofactors in the OEC, Ca2+ and Cl, and has shown that Ca2+ is an integral component of the OEC and is proximal to Mn. In addition, dichroism studies on oriented PS II membranes have provided angular information about the Mn–Mn and Mn–Ca vectors. Based on these X-ray spectroscopy data, refined models for the structure of the OEC and a mechanism for oxygen evolution by the OEC are presented.
Keywords: Photosystem II; Oxygen evolving complex; Extended X-ray absorption fine structure; X-ray absorption near-edge structure; Electron paramagnetic resonance; S-states; Oxygen evolution; X-ray emission spectroscopy;

Using X-ray absorption spectroscopy (XAS), relevant information on structure and oxidation state of the water-oxidizing Mn complex of photosystem II has been obtained for all four semi-stable intermediate states of its catalytic cycle. We summarize our recent XAS results and discuss their mechanistic implications. The following aspects are covered: (a) information content of X-ray spectra (pre-edge feature, edge position, extended X-ray absorption fine-structure (EXAFS), dichroism in the EXAFS of partially oriented samples); (b) S1-state structure; (c) X-ray edge results on oxidation state changes; (d) EXAFS results on structural changes during the S-state cycle; (e) a structural model for the Mn complex in its S3-state; (f) XAS-based working model for the S2–S3 transition; (g) XAS-based working model for the S0–S1 transition; (h) potential role of hydrogen atom abstraction by the Mn complex. Finally, we present a specific hypothesis on the mechanism of dioxygen formation during the S3–(S4)–S0 transition. According to this hypothesis, water oxidation is facilitated by manganese reduction that is coupled to proton transfer from a substrate water to bridging oxides.
Keywords: Bioinorganic chemistry; Extended X-ray absorption fine-structure; Oxygen-evolving complex; Photosynthesis; Water oxidation;

A new hypothetical mechanism is proposed for photoassembly of the (Mn)4-cluster of the photosynthetic oxygen evolving complex (OEC). In this process, a neutral radical of YZ tyrosine plays a role in oxidizing Mn2+ associated with an apo-OEC, and also in abstracting a proton from a water molecule bound to the Mn2+ ion, together with D1-His190. This is in a similar fashion to the metallo-radical mechanism proposed for photosynthetic water oxidation by the (Mn)4-cluster. The model insists that a common mechanism participates in the photoassembly of the (Mn)4-cluster and the photosynthetic water oxidation.
Keywords: Photosystem II; Oxygen evolution; Photoactivation; Mn-cluster; Proton abstraction; YZ tyrosine;

The inorganic biochemistry of photosynthetic oxygen evolution/water oxidation by G.M Ananyev; L Zaltsman; C Vasko; G.C Dismukes (52-68).
At the request of the organizer of this special edition, we have attempted to do several things in this manuscript: (1) we present a mini-review of recent, selected, works on the light-induced inorganic biogenesis (photoactivation), composition and structure of the inorganic core responsible for photosynthetic water oxidation; (2) we summarize a new proposal for the evolutionary origin of the water oxidation catalyst which postulates a key role for bicarbonate in formation of the inorganic core; (3) we summarize published studies and present new results on what has been learned from studies of ‘inorganic mutants’ in which the endogenous cofactors (Mn n+, Ca 2+, Cl) are substituted; (4) the first ΔpH changes measured during the photoactivation process are reported and used to develop a model for the stepwise photo-assembly process; (5) a comparative analysis is given of data in the literature on the kinetics of substrate water exchange and peroxide binding/dismutation which support a mechanistic model for water oxidation in general; (6) we discuss alternative interpretations of data in the literature with a view to forecast new avenues where progress is needed.

Vibrational spectroscopy of the oxygen-evolving complex and of manganese model compounds by Hsiu-An Chu; Warwick Hillier; Neil A Law; Gerald T Babcock (69-82).
A number of molecularly specific models for the oxygen-evolving complex in photosystem II (PSII) and of manganese–substrate water intermediates that may occur in this process have been proposed recently. We summarize this work briefly. Fourier transform infrared techniques have emerged as fruitful tools to study the molecular structures of YZ and the manganese complex. We discuss recent work in which mid-IR (1000–2000 cm−1) methods have been used in this effort. The low-frequency IR region (<1000 cm−1) has been more difficult to access for technical reasons, but good progress has been made in overcoming these obstacles. We update recent low-frequency work on PSII and then present a detailed summary of relevant manganese model compounds that will be of importance in understanding the emerging biological data.
Keywords: Fourier transform infrared spectroscopy; Photosystem II; Manganese cluster; Tyrosyl radical; Oxygen-evolving complex;

Comparative studies of the S0 and S2 multiline electron paramagnetic resonance signals from the manganese cluster in Photosystem II by Paulina Geijer; Sindra Peterson; Karin A Åhrling; Zsuzsanna Deák; Stenbjörn Styring (83-95).
Electron paramagnetic resonance (EPR) spectroscopy is one of the major techniques used to analyse the structure and function of the water oxidising complex (WOC) in Photosystem II. The discovery of an EPR signal from the S0 state has opened the way for new experiments, aiming to characterise the S0 state and elucidate the differences between the different S states. We present a review of the biochemical and biophysical characterisation of the S0 state multiline signal that has evolved since its discovery, and compare these results to previous and recent data from the S2 multiline signal. We also present some new data from the S2 state reached on the second turnover of the enzyme.
Keywords: Oxygen evolution; Photosystem II; Electron paramagnetic resonance; Multiline signal; S state;

Electron paramagnetic resonance (EPR) spectroscopy has often played a crucial role in characterizing the various cofactors and processes of photosynthesis, and photosystem II and its oxygen evolving chemistry is no exception. Until recently, the application of EPR spectroscopy to the characterization of the oxygen evolving complex (OEC) has been limited to the S2-state of the Kok cycle. However, in the past few years, continuous wave-EPR signals have been obtained for both the S0- and S1-state as well as for the S2–Y Z-state of a number of inhibited systems. Furthermore, the pulsed EPR technique of electron spin echo electron nuclear double resonance spectroscopy has been used to directly probe the 55Mn nuclei of the manganese cluster. In this review, we discuss how the EPR data obtained from each of these states of the OEC Kok cycle are being used to provide insight into the physical and electronic structure of the manganese cluster and its interaction with the key tyrosine, YZ.
Keywords: Photosynthesis; Photosystem II; Electron paramagnetic resonance; Electron nuclear double resonance; Oxygen evolution; Manganese;

The parallel polarization electron paramagnetic resonance (EPR) method has been applied to investigate manganese EPR signals of native S1 and S3 states of the water oxidizing complex (WOC) in photosystem (PS) II. The EPR signals in both states were assigned to thermally excited states with S=1, from which zero-field interaction parameters D and E were derived. Three kinds of signals, the doublet signal, the singlet-like signal and g=11–15 signal, were detected in Ca2+-depleted PS II. The g=11–15 signal was observed by parallel and perpendicular modes and assigned to a higher oxidation state beyond S2 in Ca2+-depleted PS II. The singlet-like signal was associated with the g=11–15 signal but not with the YZ (the tyrosine residue 161 of the D1 polypeptide in PS II) radical. The doublet signal was associated with the YZ radical as proved by pulsed electron nuclear double resonance (ENDOR) and ENDOR-induced EPR. The electron transfer mechanism relevant to the role of YZ radical was discussed.
Keywords: S3 state; Ca2+-depleted photosystem II; Parallel electron paramagnetic resonance; Pulsed electron nuclear double resonance; Mn cluster; YZ;

Results from a variety of experimental techniques which have been used to define the oxidation levels of Mn and other components in the S states of the water oxidising complex in Photosystem II are reviewed. A self-consistent interpretation of Mn X-ray absorption near edge spectroscopy, UV-visible and near infrared spectroscopic data suggests that Mn oxidation occurs only on the S0→S1 transition, and that all four Mn centres have formal oxidation state III thereafter. Ligand oxidation occurs on the transitions to S2 and S3. This is supported by high level quantum chemical calculations and an analysis of the kinetics of substrate water exchange, as recently determined by Wydrzynski et al. (this journal). One type of model for the catalytic site structure and water oxidation mechanism, consistent with these conclusions, is discussed. This model invokes magnetically separate oxo bridged dimers with water oxidation occurring by a concerted 2H+/2e transfer mechanism, with one H transfer to a bridge oxygen on each dimer.
Keywords: Photosystem II; Oxidation state; Computational chemistry; Manganese; Electron paramagnetic resonance; OEC;

Photosynthetic water oxidation: towards a mechanism by Jonathan H.A Nugent; Anne M Rich; Michael C.W Evans (138-146).
This mini-review outlines the current theories on the mechanism of electron transfer from water to P680, the location and structure of the water oxidising complex and the role of the manganese cluster. We discuss how our data fit in with current theories and put forward our ideas on the location and mechanism of water oxidation.
Keywords: Photosynthesis; Oxygen evolution; Photosystem II; Water oxidation; Tyrosine; Manganese;

The combination of site-directed mutagenesis, isotopic labeling, new magnetic resonance techniques and optical spectroscopic methods have provided new insights into cofactor coordination and into the mechanism of electron transport and proton-coupled electron transport in photosystem II. Site-directed mutations in the D1 polypeptide of this photosystem have implicated a number of histidine and carboxylate residues in the coordination and assembly of the manganese cluster, responsible for photosynthetic water oxidation. Many of these are located in the carboxy-terminal region of this polypeptide close to the processing site involved in its maturation. This maturation is a required precondition for cluster assembly. Recent proposals for the mechanism of water oxidation have directly implicated redox-active tyrosine YZ in this mechanism and have emphasized the importance of the coupling of proton and electron transfer in the reduction of YZ by the Mn cluster. The interaction of both homologous redox-active tyrosines YZ and YD with their respective homologous proton acceptors is discussed in an effort to better understand the significance of such coupling.
Keywords: Photosystem II; Redox-active tyrosine; Oxygen evolution; Manganese; Proton-coupled electron transport; Site-directed mutagenesis;

The catalytic site for photosynthetic water oxidation is embedded in a protein matrix consisting of nearly 30 different polypeptides. Residues from several of these polypeptides modulate the properties of the tetrameric Mn cluster and the redox-active tyrosine residue, YZ, that are located at the catalytic site. However, most or all of the residues that interact directly with YZ and the Mn cluster appear to be contributed by the D1 polypeptide. This review summarizes our knowledge of the environments of YZ and the Mn cluster as obtained from the introduction of site-directed, deletion, and other mutations into the photosystem II polypeptides of the cyanobacterium Synechocystis sp. PCC 6803 and the green alga Chlamydomonas reinhardtii.
Keywords: Photosynthesis; Tyrosyl radical; Oxygen evolution; Electron transfer; Site-directed mutagenesis;

It is well established that bicarbonate stimulates electron transfer between the primary and secondary electron acceptors, QA and QB, in formate-inhibited photosystem II; the non-heme Fe between QA and QB plays an essential role in the bicarbonate binding. Strong evidence of a bicarbonate requirement for the water-oxidizing complex (WOC), both O2 evolving and assembling from apo-WOC and Mn2+, of photosystem II (PSII) preparations has been presented in a number of publications during the last 5 years. The following explanations for the involvement of bicarbonate in the events on the donor side of PSII are considered: (1) bicarbonate serves as an electron donor (alternative to water or as a way of involvement of water molecules in the oxidative reactions) to the Mn-containing O2 center; (2) bicarbonate facilitates reassembly of the WOC from apo-WOC and Mn2+ due to formation of the complexes Mn(HCO3)+ and Mn(HCO3)2 leading to an easier oxidation of Mn2+ with PSII; (3) bicarbonate is an integral component of the WOC essential for its function and stability; it may be considered a direct ligand to the Mn cluster; (4) the WOC is stabilized by bicarbonate through its binding to other components of PSII.
Keywords: Photosystem II; Water-oxidizing complex; Manganese; Bicarbonate; Formate;

The mechanism for photosynthetic O2 evolution by photosystem II is currently a topic of intense debate. Important questions remain as to what is the nature of the binding sites for the substrate water and how does the O–O bond form. Recent measurements of the 18O exchange between the solvent water and the photogenerated O2 as a function of the S-state cycle have provided some surprising insights to these questions (W. Hillier, T. Wydrzynski, Biochemistry 39 (2000) 4399–4405). The results show that one substrate water molecule is bound at the beginning of the catalytic sequence, in the S0 state, while the second substrate water molecule binds in the S3 state or possibly earlier. It may be that the second substrate water molecule only enters the catalytic sequence following the formation of the S3 state. Most importantly, comparison of the observed exchange rates with oxygen ligand exchange in various metal complexes reveal that the two substrate water molecules are most likely bound to separate MnIII ions, which do not undergo metal-centered oxidations through to the S3 state. The implication of this analysis is that in the S1 state, all four Mn ions are in the +3 oxidation state. This minireview summarizes the arguments for this proposal.
Keywords: O2 evolution; Photosystem II; Manganese cluster; Water exchange; Substrate binding;

Keywords: Photosystem II; Water oxidizing complex; Hydrogen bond network; Redox isomerism;

A mechanism for photosynthetic water oxidation is proposed based on a structural model of the oxygen-evolving complex (OEC) and its placement into the modeled structure of the D1/D2 core of photosystem II. The structural model of the OEC satisfies many of the geometrical constraints imposed by spectroscopic and biophysical results. The model includes the tetranuclear manganese cluster, calcium, chloride, tyrosine Z, H190, D170, H332 and H337 of the D1 polypeptide and is patterned after the reversible O2-binding diferric site in oxyhemerythrin. The mechanism for water oxidation readily follows from the structural model. Concerted proton-coupled electron transfer in the S2→S3 and S3→S4 transitions forms a terminal Mn(V)O moiety. Nucleophilic attack on this electron-deficient Mn(V)O by a calcium-bound water molecule results in a Mn(III)–OOH species, similar to the ferric hydroperoxide in oxyhemerythrin. Dioxygen is released in a manner analogous to that in oxyhemerythrin, concomitant with reduction of manganese and protonation of a μ-oxo bridge.
Keywords: Calcium; Chloride; Manganese; Oxygen-evolving complex; Photosystem II; Tyrosyl radical; Water oxidation;

Coupling of electron and proton transfer in the photosynthetic water oxidase by Fabrice Rappaport; Jérôme Lavergne (246-259).
According to current estimates, the photosynthetic water oxidase functions with a quite restricted driving force. This emphasizes the importance of the catalytic mechanisms in this enzyme. The general problem of coupling electron and proton transfer is discussed from this viewpoint and it is argued that ‘weak coupling’ is preferable to ‘strong coupling’. Weak coupling can be achieved by facilitating deprotonation either before (proton-first path) or after (electron-first path) the oxidation step. The proton-first path is probably relevant to the oxidation of tyrosine YZ by P-680. Histidine D1–190 is believed to play a key role as a proton acceptor facilitating YZ deprotonation. The pK a of an efficient proton acceptor is submitted to conflicting requirements, since a high pK a favors proton transfer from the donor, but also from the medium. H-bonding between YZ and His, together with the Coulombic interaction between negative tyrosinate and positive imidazolium, are suggested to play a decisive role in alleviating these constraints. Current data and concepts on the coupling of electron and proton transfer in the water oxidase are discussed.
Keywords: Proton-coupled electron transfer; Photosystem II; Water oxidation; Redox active tyrosine;