A central question in biological water splitting concerns the oxidation states of the manganese ions that comprise the oxygen-evolving complex of photosystem II. Understanding the nature and order of ...oxidation events that occur during the catalytic cycle of five S
states (
= 0-4) is of fundamental importance both for the natural system and for artificial water oxidation catalysts. Despite the widespread adoption of the so-called "high-valent scheme"-where, for example, the Mn oxidation states in the S
state are assigned as III, IV, IV, IV-the competing "low-valent scheme" that differs by a total of two metal unpaired electrons (
III, III, III, IV in the S
state) is favored by several recent studies for the biological catalyst. The question of the correct oxidation state assignment is addressed here by a detailed computational comparison of the two schemes using a common structural platform and theoretical approach. Models based on crystallographic constraints were constructed for all conceivable oxidation state assignments in the four (semi)stable S states of the oxygen evolving complex, sampling various protonation levels and patterns to ensure comprehensive coverage. The models are evaluated with respect to their geometric, energetic, electronic, and spectroscopic properties against available experimental EXAFS, XFEL-XRD, EPR, ENDOR and Mn K pre-edge XANES data. New 2.5 K
Mn ENDOR data of the S
state are also reported. Our results conclusively show that the entire S state phenomenology can only be accommodated within the high-valent scheme by adopting a single motif and protonation pattern that progresses smoothly from S
(III, III, III, IV) to S
(IV, IV, IV, IV), satisfying all experimental constraints and reproducing all observables. By contrast, it was impossible to construct a consistent cycle based on the low-valent scheme for all S states. Instead, the low-valent models developed here may provide new insight into the over-reduced S states and the states involved in the assembly of the catalytically active water oxidizing cluster.
Inspired by the period-four oscillation in flash-induced oxygen evolution of photosystem II discovered by Joliot in 1969, Kok performed additional experiments and proposed a five-state kinetic model ...for photosynthetic oxygen evolution, known as Kok's S-state clock or cycle
. The model comprises four (meta)stable intermediates (S
, S
, S
and S
) and one transient S
state, which precedes dioxygen formation occurring in a concerted reaction from two water-derived oxygens bound at an oxo-bridged tetra manganese calcium (Mn
CaO
) cluster in the oxygen-evolving complex
. This reaction is coupled to the two-step reduction and protonation of the mobile plastoquinone Q
at the acceptor side of PSII. Here, using serial femtosecond X-ray crystallography and simultaneous X-ray emission spectroscopy with multi-flash visible laser excitation at room temperature, we visualize all (meta)stable states of Kok's cycle as high-resolution structures (2.04-2.08 Å). In addition, we report structures of two transient states at 150 and 400 µs, revealing notable structural changes including the binding of one additional 'water', Ox, during the S
→S
state transition. Our results suggest that one water ligand to calcium (W3) is directly involved in substrate delivery. The binding of the additional oxygen Ox in the S
state between Ca and Mn1 supports O-O bond formation mechanisms involving O5 as one substrate, where Ox is either the other substrate oxygen or is perfectly positioned to refill the O5 position during O
release. Thus, our results exclude peroxo-bond formation in the S
state, and the nucleophilic attack of W3 onto W2 is unlikely.
Knowledge of the manganese oxidation states of the oxygen-evolving Mn₄CaO₅ cluster in photosystem II (PSII) is crucial toward understanding the mechanism of biological water oxidation. There is a 4 ...decade long debate on this topic that historically originates from the observation of a multiline electron paramagnetic resonance (EPR) signal with effective total spin of S = 1/2 in the singly oxidized S₂ state of this cluster. This signal implies an overall oxidation state of either Mn(III)₃Mn(IV) or Mn(III)Mn(IV)₃ for the S₂ state. These 2 competing assignments are commonly known as “low oxidation (LO)” and “high oxidation (HO)” models of the Mn₄CaO₅ cluster. Recent advanced EPR and Mn K-edge X-ray spectroscopy studies converge upon the HO model. However, doubts about these assignments have been voiced, fueled especially by studies counting the number of flash-driven electron removals required for the assembly of an active Mn₄CaO₅ cluster starting from Mn(II) and Mn-free PSII. This process, known as photoactivation, appeared to support the LO model since the first oxygen is reported to evolve already after 7 flashes. In this study, we improved the quantum yield and sensitivity of the photoactivation experiment by employing PSII microcrystals that retained all protein subunits after complete manganese removal and by oxygen detection via a custom built thin-layer cell connected to a membrane inlet mass spectrometer. We demonstrate that 9 flashes by a nanosecond laser are required for the production of the first oxygen, which proves that the HO model provides the correct description of the Mn₄CaO₅ cluster’s oxidation states.
Protonation states of water ligands and oxo bridges are intimately involved in tuning the electronic structures and oxidation potentials of the oxygen evolving complex (OEC) in Photosystem II, ...steering the mechanistic pathway, which involves at least five redox state intermediates S(n) (n = 0-4) resulting in the oxidation of water to molecular oxygen. Although protons are practically invisible in protein crystallography, their effects on the electronic structure and magnetic properties of metal active sites can be probed using spectroscopy. With the twin purpose of aiding the interpretation of the complex electron paramagnetic resonance (EPR) spectroscopic data of the OEC and of improving the view of the cluster at the atomic level, a complete set of protonation configurations for the S(2) state of the OEC were investigated, and their distinctive effects on magnetic properties of the cluster were evaluated. The most recent X-ray structure of Photosystem II at 1.9 Å resolution was used and refined to obtain the optimum structure for the Mn(4)O(5)Ca core within the protein pocket. Employing this model, a set of 26 structures was constructed that tested various protonation scenarios of the water ligands and oxo bridges. Our results suggest that one of the two water molecules that are proposed to coordinate the outer Mn ion (Mn(A)) of the cluster is deprotonated in the S(2) state, as this leads to optimal experimental agreement, reproducing the correct ground state spin multiplicity (S = 1/2), spin expectation values, and EXAFS-derived metal-metal distances. Deprotonation of Ca(2+)-bound water molecules is strongly disfavored in the S(2) state, but dissociation of one of the two water ligands appears to be facile. The computed isotropic hyperfine couplings presented here allow distinctions between models to be made and call into question the assumption that the largest coupling is always attributable to Mn(III). The present results impose limits for the total charge and the proton configuration of the OEC in the S(2) state, with implications for the cascade of events in the Kok cycle and for the water splitting mechanism.
Light-driven oxidation of water into dioxygen, catalysed by the oxygen-evolving complex (OEC) in photosystem II, is essential for life on Earth and provides the blueprint for devices for producing ...fuel from sunlight. Although the structure of the OEC is known at atomic level for its dark-stable state, the mechanism by which water is oxidized remains unsettled. Important mechanistic information was gained in the past two decades by mass spectrometric studies of the H2(18)O/H2(16)O substrate-water exchange in the four (semi) stable redox states of the OEC. However, until now such data were not attainable in the transient states formed immediately before the O-O bond formation. Using modified photosystem II complexes displaying up to 40-fold slower O2 production rates, we show here that in the transient S3YZ state the substrate-water exchange is dramatically slowed as compared with the earlier S states. This further constrains the possible sites for substrate-water binding in photosystem II.
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•Fe2O3 films were studied for electrocatalytic OER in 0.5 M H2SO4.•The OER performances of the films are polymorph-dependent.•Mixed-polymorph film of γ-Fe2O3 and α-Fe2O3 is highly ...active and stable for OER.•Electronic properties due to polymorph crystal structure affect the OER performance.
Stable and efficient oxygen evolution reaction (OER) catalysts for the oxidation of water to dioxygen in highly acidic media are currently limited to expensive noble metal (Ir and Ru) oxides since presently known OER catalysts made of inexpensive earth-abundant materials generally suffer anodic corrosion at low pH. In this study, we report that a mixed-polymorph film comprising maghemite and hematite, prepared using spray pyrolysis deposition followed by low-temperature annealing, showed a sustained OER rate (>24 h) corresponding to a current density of 10 mA cm−2 at an initial overpotential of 650 mV, with a Tafel slope of only 56 mV dec−1 and near-100% Faradaic efficiency in 0.5 M H2SO4 (pH 0.3). This performance is remarkable, since iron (III) oxide films comprising only maghemite were found to exhibit a comparable intrinsic activity, but considerably lower stability for OER, while films of pure hematite were OER-inactive. These results are explained by the differences in the polymorph crystal structures, which cause different electrical conductivity and surface interactions with water molecules and protons. Our findings not only reveal the potential of iron (III) oxide as acid-stable OER catalyst, but also highlight the important yet hitherto largely unexplored effect of crystal polymorphism on electrocatalytic OER performance.
Abstract The Mn 4 CaO 5(6) cluster in photosystem II catalyzes water splitting through the S i state cycle ( i = 0–4). Molecular O 2 is formed and the natural catalyst is reset during the final S 3 → ...(S 4 ) → S 0 transition. Only recently experimental breakthroughs have emerged for this transition but without explicit information on the S 0 -state reconstitution, thus the progression after O 2 release remains elusive. In this report, our molecular dynamics simulations combined with density functional calculations suggest a likely missing link for closing the cycle, i.e., restoring the first catalytic state. Specifically, the formation of closed-cubane intermediates with all hexa-coordinate Mn is observed, which would undergo proton release, water dissociation, and ligand transfer to produce the open-cubane structure of the S 0 state. Thereby, we theoretically identify the previously unknown structural isomerism in the S 0 state that acts as the origin of the proposed structural flexibility prevailing in the cycle, which may be functionally important for nature’s water oxidation catalysis.
Abstract
Light-driven oxidation of water to molecular oxygen is catalyzed by the oxygen-evolving complex (OEC) in Photosystem II (PS II). This multi-electron, multi-proton catalysis requires the ...transport of two water molecules to and four protons from the OEC. A high-resolution 1.89 Å structure obtained by averaging all the S states and refining the data of various time points during the S
2
to S
3
transition has provided better visualization of the potential pathways for substrate water insertion and proton release. Our results indicate that the O1 channel is the likely water intake pathway, and the Cl1 channel is the likely proton release pathway based on the structural rearrangements of water molecules and amino acid side chains along these channels. In particular in the Cl1 channel, we suggest that residue D1-E65 serves as a gate for proton transport by minimizing the back reaction. The results show that the water oxidation reaction at the OEC is well coordinated with the amino acid side chains and the H-bonding network over the entire length of the channels, which is essential in shuttling substrate waters and protons.
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