Water oxidation mechanism in photosystem II, including oxidations, proton release pathways, O―O bond formation and O2 release ☆
TL;DR: The present status of DFT studies on water oxidation in photosystem II is described and it is argued that a full understanding of all steps is close.
About: This article is published in Biochimica et Biophysica Acta.The article was published on 2013-08-01 and is currently open access. It has received 329 citations till now. The article focuses on the topics: Oxygen-evolving complex & P680.
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TL;DR: It is suggested that future advances in solar fuels science will be accelerated by the development of new methods for materials synthesis and characterization, along with in-depth investigations of redox mechanisms at catalytic surfaces.
Abstract: Water oxidation is a key chemical transformation for the conversion of solar energy into chemical fuels Our review focuses on recent work on robust earth-abundant heterogeneous catalysts for the oxygen-evolving reaction (OER) We point out that improvements in the performance of OER catalysts will depend critically on the success of work aimed at understanding reaction barriers based on atomic-level mechanisms We highlight the challenge of obtaining acid-stable OER catalysts, with proposals for elements that could be employed to reach this goal We suggest that future advances in solar fuels science will be accelerated by the development of new methods for materials synthesis and characterization, along with in-depth investigations of redox mechanisms at catalytic surfaces
1,159 citations
TL;DR: A ‘radiation-damage-free’ structure of PSII from Thermosynechococcus vulcanus in the S1 state is reported, and it is expected that this structure will provide a blueprint for the design of artificial catalysts for water oxidation.
Abstract: Photosynthesis converts light energy into biologically useful chemical energy vital to life on Earth. The initial reaction of photosynthesis takes place in photosystem II (PSII), a 700-kilodalton homodimeric membrane protein complex which catalyses photo-oxidation of water into dioxygen through an S-state cycle of the oxygen evolving complex (OEC). The structure of PSII has been solved by X-ray diffraction (XRD) at 1.9-angstrom (A) resolution, which revealed that the OEC is a Mn4CaO5-cluster coordinated by a well-defined protein environment1. However, extended X-ray absorption fine structure (EXAFS) studies showed that the manganese cations in the OEC are easily reduced by X-ray irradiation2, and slight differences were found in the Mn–Mn distances between the results of XRD1, EXAFS3–7 and theoretical studies8–14. Here we report a ‘radiation-damage-free’ structure of PSII from Thermosynechococcus vulcanus in the S1 state at a resolution of 1.95 A using femtosecond X-ray pulses of the SPring-8 angstrom compact free-electron laser (SACLA) and a huge number of large, highly isomorphous PSII crystals. Compared with the structure from XRD, the OEC in the X-ray free electron laser structure has Mn–Mn distances that are shorter by 0.1–0.2 A. The valences of each manganese atom were tentatively assigned as Mn1D(III), Mn2C(IV), Mn3B(IV) and Mn4A(III), based on the average Mn–ligand distances and analysis of the Jahn–Teller axis on Mn(III). One of the oxo-bridged oxygens, O5, has significantly longer Mn–O distances in contrast to the other oxo-oxygen atoms, suggesting that it is a hydroxide ion instead of a normal oxygen dianion and therefore may serve as one of the substrate oxygen atoms. These findings provide a structural basis for the mechanism of oxygen evolution, and we expect that this structure will provide a blueprint for design of artificial catalysts for water oxidation.
978 citations
TL;DR: The overall structure of PSII is provided followed by detailed descriptions of the specific structure of the Mn4CaO5 cluster and its surrounding protein environment, based on the geometric organization revealed by the crystallographic analysis.
Abstract: Oxygenic photosynthesis forms the basis of aerobic life on earth by converting light energy into biologically useful chemical energy and by splitting water to generate molecular oxygen. The water-splitting and oxygen-evolving reaction is catalyzed by photosystem II (PSII), a huge, multisubunit membrane-protein complex located in the thylakoid membranes of organisms ranging from cyanobacteria to higher plants. The structure of PSII has been analyzed at 1.9-A resolution by X-ray crystallography, revealing a clear picture of the Mn4CaO5 cluster, the catalytic center for water oxidation. This article provides an overview of the overall structure of PSII followed by detailed descriptions of the specific structure of the Mn4CaO5 cluster and its surrounding protein environment. Based on the geometric organization of the Mn4CaO5 cluster revealed by the crystallographic analysis, in combination with the results of a vast number of experimental studies involving spectroscopic and other techniques as well as various theoretical studies, the article also discusses possible mechanisms for water splitting that are currently under consideration.
508 citations
Cites background from "Water oxidation mechanism in photos..."
...ELDOR: electron-electron double resonance experiments; and theoretical calculations (6, 117, 142)....
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TL;DR: The most often encountered reaction of the Fe(III)−O2 species is an electrophilic attack on an electron-rich (co)substrate that yields an Fe(II) intermediate with a peroxide bridge between the ferrous ion and an organic molecule (Figure 57).
Abstract: ing a hydrogen atom from substrates with relatively weak X−H bonds (Figure 56). Such a situation was found in the catalytic cycle of ACCO, where cleavage of the N−H bond is facilitated by the ferrous ion capable of (partly) reducing the resulting N-based radical to an anion. In the catalytic cycle of HEPD and in the reaction of HppE with an enantiomer of the native substrate, a C−H bond at the carbon hosting a deprotonated alcohol group is severed by the superoxide. In these cases transfer of a hydrogen atom to the superoxide is coupled to one-electron reduction of Fe(III) to Fe(II), which yields aldehyde or ketone products. In a similar way a thioaldehyde is produced during the initial steps of the IPNS catalytic cycle. Figure 53. Reaction catalyzed by NDO. Figure 54. X-ray structure of the non-heme iron cofactor in the NDO active site (PDB 1O7G). Figure 55. Reaction mechanism for the dihydroxylation reaction catalyzed by NDO suggested on the basis of the results of a DFT study. Relative energy values in kilocalories per mole are given beneath the structures shown and above the arrows for the transition states connecting them. Chemical Reviews Review dx.doi.org/10.1021/cr400388t | Chem. Rev. 2014, 114, 3601−3658 3636 The most often encountered reaction of the Fe(III)−O2 species is an electrophilic attack on an electron-rich (co)substrate that yields an Fe(II) intermediate with a peroxide bridge between the ferrous ion and an organic molecule (Figure 57). In all examples shown in the figure the reactive spin state is a quintet with high-spin Fe(III) antiferromagnetically coupled to the superoxide radical. This particular electronic structure allows for a smooth two-electron reaction, leading to a ferrous intermediate featuring a high-spin Fe(II) ion, i.e., also lying on a quintet PES. When the substrates are easily one-electron-oxidized, as, for example, carotenoids or catecholates, already the ternary enzyme−dioxygen−organic substrate complex may contain an organic radical along with the superoxide anion stabilized by coordination to the metal (Figure 58). With proper (antiferromagnetic) alignment of the spins of the unpaired electrons on the two radicals, direct coupling between them proceeds with a straightforward formation of a new C−O bond. With the O2 ligand already protonated, several different reaction scenarios are usually plausible, and one of them, arguably the simplest, involves a transfer of the HOO group from the metal ion to the organic substrate (Figure 59). In the reaction of HEPD, it is the distal, i.e., originally protonated, oxygen atom that attacks the aldehyde group and the proton is transferred to the second (proximal) oxygen atom with the help of a phosphonic group of the substrate. In this reaction HOO acts as a nucleophile. In the case of HGD, the HOO ligand has a partial radical character, and hence, in its attack on the aromatic ring, it behaves as an electrophilic reagent. Moreover, in the HGD and ACO cases, it is the proximal oxygen atom that is directly transferred from the metal ion to the organic radical, i.e., the proton remains on the same oxygen atom throughout the reaction. When a catalytic reaction involves a homolytic O−O bond cleavage, one end of the peroxo group is in contact with the metal ion, and it is reduced to HO− or RO− when the O−O bond breaks (Figure 60). The electron required for the reduction is provided usually by the ferrous ion; in intradiol dioxygenases, which host Fe(III) in the active site, a tyrosinate ligand can serve as a reductant. Heterolytic cleavage of the O−O bond typically yields highvalent iron(IV)−oxo species, and such a reaction requires Fe(II), a deprotonated proximal oxygen atom, and usually also that the distal oxygen atom has a chance to develop a second covalent bond when the O−O gets broken (Figure 61). The bonding partner for the distal oxygen can be a hydrogen (PDHs, IPNS, ACCO) or a (co)substrate’s carbon (αKAOs, ACO, Dke1) atom. Heterolysis to Fe(IV)O usually proceeds on the quintet PES. Finally, heterolytic O−O bond cleavage may proceed without changing the oxidation state of the metal but instead with coupled two-electron oxidation of an organic substrate (Figure Figure 56. Examples of Fe(II)/Fe(III)−O2 reactions involving hydrogen atom abstraction. Only the most relevant fragment of the substrate is shown. Figure 57. Examples of Fe(III)−O2 reactions involving electrophilic attack and two-electron oxidation of an organic (co)substrate. Figure 58. Examples of Fe(II)/Fe(III)−O2 reactions involving radical coupling between the superoxide and an organic radical. Only the most relevant fragment of the substrate is shown. Chemical Reviews Review dx.doi.org/10.1021/cr400388t | Chem. Rev. 2014, 114, 3601−3658 3637 62). In both cases depicted in the figure, a hydroperoxo group is bound to high-spin Fe(III), and when theO−Obond cleaves, the OH group remains on iron and the other oxygen atom forms two covalent bonds with the organic substrate. This kind of heterolytic O−O cleavage requires that the donor orbital of the organic substrate, i.e., the one that provides two electrons for reduction of the peroxo group, has a good overlap with the O−O σ* orbital. 5.2. Dinuclear Non-Heme Iron Enzymes 5.2.1. Methane Monooxygenase. MMO is an enzyme which inserts one oxygen from O2 into methane to form methanol. The active site of the soluble form of MMO is shown in Figure 63. It contains an iron dimer complex linked by oxygen-derived ligands and has four glutamates and two histidines. Due to the presence of a well-resolved X-ray structure, and the technical importance of the reaction catalyzed, this was actually the first redox-active enzymemechanism that was treated with the cluster model using modern DFT functionals in 1997. Several groups were active at an early stage, and the most essential parts of the reaction mechanism were determined more than a decade ago. A comprehensive review of this development was written by Friesner et al. In short, the active species (compound Q) has a diamond core structure with two bridging oxo groups and is in an Fe2(IV,IV) state, one of themost oxidized species in nature. One of the oxo groups of compound Q activates nethane by an abstraction of one hydrogen atom. The TS is linear in C···H···O to form an Fe2(III,IV) state and amethyl radical. The loss of entropy at the TS is a large part of the barrier. In the second step, the methyl radical recombines with the bridging hydroxide formed in the first step. The TS for this step was first located by Basch et al. This rebound mechanism was criticized by interpretations of radical clock experiments, which appeared to show that there could not be a sufficiently long-lived alkyl radical to be consistent with a two-step mechanism. A concerted mechanism with simultaneous cleavage of the C−H bond and formation of the C−O bond was therefore suggested. Several explanations were suggested to resolve this apparent discrepancy between experiment and theory. In one of them, it was concluded that the radical clock probe molecules Figure 59. Examples of HOO transfer reactions. Only the most relevant fragment of the substrate is shown. Figure 60. Examples of O−O bond homolysis facilitated by oneelectron reduction of the proximal oxygen atom. Only the most relevant fragment of the substrate is shown. Figure 61. Examples of heterolytic O−O bond cleavage yielding iron(IV)−oxo species. Figure 62. Examples of heterolytic O−Obond cleavage proceeding with direct two-electron oxidation of the organic molecule. Chemical Reviews Review dx.doi.org/10.1021/cr400388t | Chem. Rev. 2014, 114, 3601−3658 3638 were chemically so different from methane that different mechanisms were likely. The probes are much easier to ionize and could form cations instead of radicals. Another suggestion was a so-called two-channel mechanism of the dynamics involving a bound radical intermediate. A third possibility could be something analogous to the two-state reactivity mechanism suggested for P450 to explain similar discrepancies in that case, but this has not been tested. In summary, a concerted mechanism, as suggested by the experiments, has never been found in DFT modeling calculations for methane hydroxylation by MMO, at least when reasonable models have been tried, and the suggestion has therefore not survived. In the initial phase of the MMO studies, there were problems converging to proper electronic states. These problems were solved by Friesner et al., who were able to obtain the correct antiferromagnetic coupling of compound Q with two high-spin irons. A state of key importance is also the first intermediate after Q, with an electronic structure characterized as Fe2(III,IV)− O•, discussed further below in connection with mixedMn−Fe dimers. It was found that already at the TS for hydrogen abstraction the iron dimer is in an Fe2(III,IV) state as it is in the product of this step. The bridging oxygen radical would then act as a hydrogen atom abstractor. At the TS, the spins are divided between a bridging oxo ligand and the methyl, while the iron spins stay essentially constant from the Fe2(III,IV)−O state to the product. The O−O bond cleavage to reach compound Q is also a significant step in the catalytic cycle. Again, several groups were involved in studying this step at an early stage. There was essential agreement among these studies on the mechanism. First, a peroxide (compound P) is formed between the two irons in an Fe2(III,III) state. Several different structures of P are nearly degenerate. In the TS for the O−O cleavage, the oxygens are symmetric, but only one of the irons is redox-active. In the final Figure 63. Active site of methane monooxygenase. Figure 64. R1 and R2 proteins in RNR. Chemical Reviews Review dx.doi.org/10.1021/cr400388t | Chem. Rev. 2014, 114, 3601−3658 3639 stage, the other iron also changes its oxidation state to IV, and compound Q is formed. In the study by Friesner et al.,
457 citations
TL;DR: The structural changes in PSII induced by two-flash illumination at room temperature at a resolution of 2.35 Å are described, providing a mechanism for the O=O bond formation consistent with that proposed previously.
Abstract: Photosystem II (PSII) is a huge membrane-protein complex consisting of 20 different subunits with a total molecular mass of 350 kDa for a monomer. It catalyses light-driven water oxidation at its catalytic centre, the oxygen-evolving complex (OEC). The structure of PSII has been analysed at 1.9 A resolution by synchrotron radiation X-rays, which revealed that the OEC is a Mn4CaO5 cluster organized in an asymmetric, 'distorted-chair' form. This structure was further analysed with femtosecond X-ray free electron lasers (XFEL), providing the 'radiation damage-free' structure. The mechanism of O=O bond formation, however, remains obscure owing to the lack of intermediate-state structures. Here we describe the structural changes in PSII induced by two-flash illumination at room temperature at a resolution of 2.35 A using time-resolved serial femtosecond crystallography with an XFEL provided by the SPring-8 angstrom compact free-electron laser. An isomorphous difference Fourier map between the two-flash and dark-adapted states revealed two areas of apparent changes: around the QB/non-haem iron and the Mn4CaO5 cluster. The changes around the QB/non-haem iron region reflected the electron and proton transfers induced by the two-flash illumination. In the region around the OEC, a water molecule located 3.5 A from the Mn4CaO5 cluster disappeared from the map upon two-flash illumination. This reduced the distance between another water molecule and the oxygen atom O4, suggesting that proton transfer also occurred. Importantly, the two-flash-minus-dark isomorphous difference Fourier map showed an apparent positive peak around O5, a unique μ4-oxo-bridge located in the quasi-centre of Mn1 and Mn4 (refs 4,5). This suggests the insertion of a new oxygen atom (O6) close to O5, providing an O=O distance of 1.5 A between these two oxygen atoms. This provides a mechanism for the O=O bond formation consistent with that proposed previously
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TL;DR: In this article, a semi-empirical exchange correlation functional with local spin density, gradient, and exact exchange terms was proposed. But this functional performed significantly better than previous functionals with gradient corrections only, and fits experimental atomization energies with an impressively small average absolute deviation of 2.4 kcal/mol.
Abstract: Despite the remarkable thermochemical accuracy of Kohn–Sham density‐functional theories with gradient corrections for exchange‐correlation [see, for example, A. D. Becke, J. Chem. Phys. 96, 2155 (1992)], we believe that further improvements are unlikely unless exact‐exchange information is considered. Arguments to support this view are presented, and a semiempirical exchange‐correlation functional containing local‐spin‐density, gradient, and exact‐exchange terms is tested on 56 atomization energies, 42 ionization potentials, 8 proton affinities, and 10 total atomic energies of first‐ and second‐row systems. This functional performs significantly better than previous functionals with gradient corrections only, and fits experimental atomization energies with an impressively small average absolute deviation of 2.4 kcal/mol.
87,732 citations
TL;DR: The crystal structure of photosystem II is reported, finding that five oxygen atoms served as oxo bridges linking the five metal atoms, and that four water molecules were bound to the Mn4CaO5 cluster; some of them may therefore serve as substrates for dioxygen formation.
Abstract: Photosystem II is the site of photosynthetic water oxidation and contains 20 subunits with a total molecular mass of 350 kDa. The structure of photosystem II has been reported at resolutions from 3.8 to 2.9 angstrom. These resolutions have provided much information on the arrangement of protein subunits and cofactors but are insufficient to reveal the detailed structure of the catalytic centre of water splitting. Here we report the crystal structure of photosystem II at a resolution of 1.9 angstrom. From our electron density map, we located all of the metal atoms of the Mn(4)CaO(5) cluster, together with all of their ligands. We found that five oxygen atoms served as oxo bridges linking the five metal atoms, and that four water molecules were bound to the Mn(4)CaO(5) cluster; some of them may therefore serve as substrates for dioxygen formation. We identified more than 1,300 water molecules in each photosystem II monomer. Some of them formed extensive hydrogen-bonding networks that may serve as channels for protons, water or oxygen molecules. The determination of the high-resolution structure of photosystem II will allow us to analyse and understand its functions in great detail.
3,325 citations
01 Jan 1996
3,277 citations
"Water oxidation mechanism in photos..." refers methods in this paper
...The hybrid functional B3LYP* [44,45] was used with polarized basis sets for the geometries (lacvp*), large basis sets for energies (cc-pvtz(-f)), and a surrounding dielectric medium with dielectric constant equal to 6.0 (basis lacvp*)....
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...The hybrid functional B3LYP* [44,45] was used with polarized basis sets for the geometries (lacvp*), large basis sets for energies (cc-pvtz(-f)), and a surrounding dielectric medium with dielectric constant equal to 6....
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TL;DR: The data strongly suggest that the OEC contains a cubane-like Mn3CaO4 cluster linked to a fourth Mn by a mono-μ-oxo bridge, and the details of the surrounding coordination sphere of the metal cluster and the implications for a possible oxygen-evolving mechanism are discussed.
Abstract: Photosynthesis uses light energy to drive the oxidation of water at an oxygen-evolving catalytic site within photosystem II (PSII). We report the structure of PSII of the cyanobacterium Thermosynechococcus elongatus at 3.5 angstrom resolution. We have assigned most of the amino acid residues of this 650-kilodalton dimeric multisubunit complex and refined the structure to reveal its molecular architecture. Consequently, we are able to describe details of the binding sites for cofactors and propose a structure of the oxygen-evolving center (OEC). The data strongly suggest that the OEC contains a cubane-like Mn 3 CaO 4 cluster linked to a fourth Mn by a mono-μ-oxo bridge. The details of the surrounding coordination sphere of the metal cluster and the implications for a possible oxygen-evolving mechanism are discussed.
3,112 citations
"Water oxidation mechanism in photos..." refers methods in this paper
...Using the information of the mechanism obtained [12] combined with the X-ray back-bone structure of the London structure [1] and the suggested ligand arrangements from the Berlin structure [2], a new structure was obtained, which has since...
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TL;DR: The uniformity with which B2-PLYP improves for a wide range of chemical systems emphasizes the need of (virtual) orbital-dependent terms that describe nonlocal electron correlation in accurate exchange-correlation functionals.
Abstract: A new hybrid density functional for general chemistry applications is proposed. It is based on a mixing of standard generalized gradient approximations GGAs for exchange by Becke B and for correlation by Lee, Yang, and Parr LYP with Hartree-Fock HF exchange and a perturbative second-order correlation part PT2 that is obtained from the Kohn-Sham GGA orbitals and eigenvalues. This virtual orbital-dependent functional contains only two global parameters that describe the mixture of HF and GGA exchange ax and of the PT2 and GGA correlation c, respectively. The parameters are obtained in a least-squares-fit procedure to the G2/97 set of heat of formations. Opposed to conventional hybrid functionals, the optimum ax is found to be quite large 53% with c=27% which at least in part explains the success for many problematic molecular systems compared to conventional approaches. The performance of the new functional termed B2-PLYP is assessed by the G2/97 standard benchmark set, a second test suite of atoms, molecules, and reactions that are considered as electronically very difficult including transition-metal compounds, weakly bonded complexes, and reaction barriers and comparisons with other hybrid functionals of GGA and meta-GGA types. According to many realistic tests, B2-PLYP can be regarded as the best general purpose density functional for molecules e.g., a mean absolute deviation for the two test sets of only 1.8 and 3.2 kcal/mol compared to about 3 and 5 kcal/mol, respectively, for the best other density functionals. Very importantly, also the maximum and minium errors outliers are strongly reduced by about 10‐20 kcal/mol. Furthermore, very good results are obtained for transition state barriers but unlike previous attempts at such a good description, this definitely comes not at the expense of equilibrium properties. Preliminary calculations of the equilibrium bond lengths and harmonic vibrational frequencies for diatomic molecules and transition-metal complexes also show very promising results. The uniformity with which B2-PLYP improves for a wide range of chemical systems emphasizes the need of virtual orbital-dependent terms that describe nonlocal electron correlation in accurate exchange-correlation functionals. From a practical point of view, the new functional seems to be very robust and it is thus suggested as an efficient quantum chemical method of general purpose. © 2006 American Institute of Physics. DOI: 10.1063/1.2148954
2,704 citations
"Water oxidation mechanism in photos..." refers methods in this paper
...Dispersion effects were added using the empirical formula of Grimme [49]....
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