Water-oxidizing Complex Research Articles

Innovative Insights into Water-Oxidation Mechanism: Investigating Birnessite's Reaction with Cerium(IV) Ammonium Nitrate.

Developing Mn-based water-oxidation reaction (WOR) catalysts is key for renewable energy storage, utilizing Mn's abundance, cost-effectiveness, and natural role. Cerium(IV) ammonium nitrate (CAN) has been widely utilized as a sacrificial oxidant in the exploration of WOR catalysts. In this study, advanced techniques, such as X-ray absorption spectroscopy (XAS), in situ Raman spectroscopy, and in situ electron paramagnetic resonance (EPR), to delve into the WOR facilitated by CAN and birnessite were employed. XANES analysis has demonstrated that the average oxidation states (AOSs) of Mn in birnessite, a birnessite/CAN mixture, and in the birnessite/CAN mixture postwater addition are 3.7, 3.8, and 3.9, respectively. In situ Raman spectroscopy performed in the presence of birnessite and CAN revealed a distinct peak at 784 cm-1, which is attributed to Mn(IV)═O. A shift of this peak to 769 cm-1 in H218O confirms its association with Mn(IV)═O. No change in this peak was observed in D2O, further supporting the notion that it is linked to Mn(IV)═O rather than Mn-OH (D). Furthermore, EPR spectroscopy shows the presence of Mn(IV). It is suggested that the WOR mechanism initiates with the oxidation of birnessite by CAN, which enhances the concentration of Mn(IV) sites in the birnessite structure. Under acidic conditions, birnessite, enriched in Mn(IV), facilitates oxygen evolution and subsequently transitions into a form with reduced Mn(IV) levels. This process highlights the critical function of the Mn (hydr)oxide structure, similar to its role in the water-oxidizing complex of Photosystem II, where it serves as charge storage for oxidizing equivalents from CAN, paving the way for a four-electron reaction that drives the WOR.

A Reappraisal of the S2 State of Nature's Water Oxidizing Complex in Its Low and High Spin Forms.

Density functional theory calculated 14N hyperfine couplings are obtained for the Mn1 ligated π-N of residue His332 of the photosystem 2 water oxidizing complex. An open cubane, O4H, model closely matches the experimental coupling obtained for the high spin S = 5/2 form of the S2 state, supporting an open cubane structure for this state. We also investigate the unusual geometric features for the S2 state obtained by X-ray free electron laser structure determinations and rationalize it as an equilibrium occurring at room temperature between W1/O4 deprotonated and protonated forms of the open cubane structure.

Exceptional Quantum Efficiency Powers Biomass Production in Halotolerant Algae Picochlorum sp.

The green algal genus Picochlorum is of biotechnological interest because of its robust response to multiple environmental stresses. We compared the metabolic performance of P. SE3 and P. oklahomense to diverse microbial phototrophs and observed exceptional performance of photosystem II (PSII) in light energy conversion in both Picochlorum species. The quantum yield (QY) for O2 evolution is the highest of any phototroph yet observed, 32% (20%) by P. SE3 (P. okl) when normalized to total PSII subunit PsbA (D1) protein, and 80% (75%) normalized per active PSII, respectively. Three factors contribute: (1) an efficient water oxidizing complex (WOC) with the fewest photochemical misses of any organism; (2) faster reoxidation of reduced (PQH2)B in P. SE3 than in P. okl. (period-2 Fourier amplitude); and (3) rapid reoxidation of the plastoquinol pool by downstream electron carriers (Cyt b6f/PETC) that regenerates PQ faster in P. SE3. This performance gain is achieved without significant residue changes around the QB site and thus points to a pull mechanism involving faster PQH2 reoxidation by Cyt b6f/PETC that offsets charge recombination. This high flux in P. SE3 may be explained by genomically encoded plastoquinol terminal oxidases 1 and 2, whereas P. oklahomense has neither. Our results suggest two distinct types of PSII centers exist, one specializing in linear electron flow and the other in PSII-cyclic electron flow. Several amino acids within D1 differ from those in the low-light-descended D1 sequences conserved in Viridiplantae, and more closely match those in cyanobacterial high-light D1 isoforms, including changes near tyrosine Yz and a water/proton channel near the WOC. These residue changes may contribute to the exceptional performance of Picochlorum at high-light intensities by increasing the water oxidation efficiency and the electron/proton flux through the PSII acceptors (QAQB).

CAH3 from Chlamydomonas reinhardtii: Unique Carbonic Anhydrase of the Thylakoid Lumen.

CAH3 is the only carbonic anhydrase (CA) present in the thylakoid lumen of the green algae Chlamydomonas reinhardtii. The monomer of the enzyme has a molecular weight of ~29.5 kDa with high CA activity. Through its dehydration activity, CAH3 can be involved either in the carbon-concentrating mechanism supplying CO2 for RuBisCO in the pyrenoid or in supporting the maximal photosynthetic activity of photosystem II (PSII) by accelerating the removal of protons from the active center of the water-oxidizing complex. Both proposed roles are considered in this review, together with a description of the enzymatic parameters of native and recombinant CAH3, the crystal structure of the protein, and the possible use of lumenal CA as a tool for increasing biomass production in higher plants. The identified involvement of lumenal CAH3 in the function of PSII is still unique among green algae and higher plants and can be used to understand the mechanism(s) of the functional interconnection between PSII and the proposed CA(s) of the thylakoid lumen in other organisms.

Effect of Osmolytes on Photoassembly of Functionally Active Mn4CaO5 Cluster in Mn-Depleted Photosystem II Preparations Isolated from Spinach Leaves

The effect of osmolytes (trehalose, sucrose, betaine, D-glucose and hydroxyectoine) on the photoassembly of the functionally active inorganic core of the water-oxidizing complex (Mn4CaO5 cluster) in Mn-depleted PSII preparations (apo-WOC-PSII) was investigated. It was revealed that the efficiency of the photoassembly of the Mn4CaO5 cluster was considerably (three times) increased in the presence of 1 M disaccharides (trehalose or sucrose) in contrast to other osmolytes. It was found that the osmolytes (especially trehalose or sucrose) improved the redox interaction of exogenous Mn2+ with apo-WOC-PSII, enhanced the protective effect of Mn2+ against the photoinhibition of apo-WOC-PSII, protected CaCl2-treated PSII preparations against thermoinactivation, and stabilized the water-oxidizing complex and electron transport from QA to QB in native PSII preparations during heat treatment. It is suggested that the ability of osmolytes to enhance the efficiency of the photoassembly of a Mn4CaO5 cluster depends on their effect on the following key processes: the redox interaction of Mn2+ with apo-WOC-PSII; the stability of apo-WOC-PSII to photoinhibition during the photoactivation procedure; and the stabilization of both the newly assembled functionally active Mn4CaO5 cluster and the electron transfer from QA to QB.

Decomposition of a manganese complex loaded on TiO2 nanoparticles under photochemical reaction

Water splitting, through electrochemical and photochemical methods, is a promising approach for large-scale hydrogen production. However, the efficiency of these methods is hindered by the water-oxidation reaction (WOR). A variety of Mn complexes have been explored as potential models for water-oxidizing complex in Photosystem II. Among different Mn complexes, [H2O(terpy)MnIII(μ-O)2MnIV(terpy)H2O](NO3)3 (1, terpy = 2,2’:6′2″-terpyridine) has been extensively studied under WOR conditions. In this study, the reactivity of 1 is investigated when loaded onto TiO2 nanoparticles and subjected to photochemical conditions. Our main goal was to identify possible products that could arise from the conversion of 1 given the specified conditions. After conducting various analytical methods, it was determined that the reaction yielded MnOx and Mn(II) species as the resulting reaction products. These findings offer valuable insights into the progress of advanced WOR catalysts and the underlying mechanism of efficient water splitting for energy storage.

How chloride functions to enable proton conduction in photosynthetic water oxidation: Time-resolved kinetics of intermediates (S-states) in vivo and bromide substitution

Chloride (Cl−) is essential for O2 evolution during photosynthetic water oxidation. Two chlorides near the water-oxidizing complex (WOC) in Photosystem II (PSII) structures from Thermosynechococcus elongatus (and T. vulcanus) have been postulated to transfer protons generated from water oxidation. We monitored four criteria: primary charge separation flash yield (P* → P+QA−), rates of water oxidation steps (S-states), rate of proton evolution, and flash O2 yield oscillations by measuring chlorophyll variable fluorescence (P* quenching), pH-sensitive dye changes, and oximetry. Br-substitution slows and destabilizes cellular growth, resulting from lower light-saturated O2 evolution rate (−20 %) and proton release (−36 % ΔpH gradient). The latter implies less ATP production. In Br- cultures, protonogenic S-state transitions (S2 → S3 → S0’) slow with increasing light intensity and during O2/water exchange (S0’ → S0 → S1), while the non-protonogenic S1 → S2 transition is kinetically unaffected. As flash rate increases in Cl− cultures, both rate and extent of acidification of the lumen increase, while charge recombination is suppressed relative to Br−. The Cl− advantage in rapid proton escape from the WOC to lumen is attributed to correlated ion-pair movement of H3O+Cl− in dry water channels vs. separated Br− and H+ ion movement through different regions (>200-fold difference in Bronsted acidities). By contrast, at low flash rates a previously unreported reversal occurs that favors Br− cultures for both proton evolution and less PSII charge recombination. In Br− cultures, slower proton transfer rate is attributed to stronger ion-pairing of Br− with AA residues lining the water channels. Both anions charge-neutralize protons and shepherd them to the lumen using dry aqueous channels.

Magnetic and Electronic Structural Properties of the S3 State of Nature's Water Oxidizing Complex: A Combined Study in ELDOR-Detected Nuclear Magnetic Resonance Spectral Simulation and Broken-Symmetry Density Functional Theory.

ELDOR-detected nuclear magnetic resonance (EDNMR) spectral simulations combined with broken-symmetry density functional theory (BS-DFT) calculations are used to obtain and to assign the 55Mn hyperfine coupling constants (hfcs) for modified forms of the water oxidizing complex in the penultimate S3 state of the water oxidation cycle. The study shows that an open cubane form of the core Mn4CaO6 cluster explains the magnetic properties of the dominant S = 3 species in all cases studied experimentally with no need to invoke a closed cubane intermediate possessing a distorted pentacoordinate Mn4 ion as recently suggested. EDNMR simulations found that both the experimental bandwidth and multinuclear transitions may alter relative EDNMR peak intensities, potentially leading to incorrect assignment of hfcs. The implications of these findings for the water oxidation mechanism are discussed.

How Nature Makes O2: an Electronic Level Mechanism for Water Oxidation in Photosynthesis.

In this paper, we combine broken symmetry density functional calculations and electron paramagnetic resonance analysis to obtain the electronic structure of the penultimate S3 state of nature’s water-oxidizing complex and determine the electronic pathway of O–O bond formation. Analysis of the electronic structure changes along the reaction path shows that two spin crossovers, facilitated by the geometry and magnetism of the water-oxidizing complex, are used to provide a unique low-energy pathway. The pathway is facilitated via the formation and stabilization of the [O2]3– ion. This ion is formed between ligated deprotonated substrate waters, O5 and O6, and is stabilized by antiferromagnetic interaction with the Mn ions of the complex. Combining the computational, crystallographic, and spectroscopic data, we show that an equilibrium exists between the O5 oxo and O6 hydroxo forms with an S = 3 spin state and a deprotonated O6 form containing a two-center one-electron bond in [O5O6]3– which we identify as the form detected using crystallography. This form corresponds to an S = 6 spin state which we demonstrate gives rise to a low-intensity EPR spectrum compared with the accompanying S = 3 state, making its detection via EPR difficult and overshadowed by the S = 3 form. Simulations using 70% of the S = 6 component give rise to a superior fit to the experimental W-band EPR spectral envelope compared with an S = 3 only form. Analyses of the most recent X-ray emission spectroscopy first moment changes for solution and time-resolved crystal data are also shown to support the model. The computational, crystallographic, and spectroscopic data are shown to coalesce to the same picture of a predominant S = 6 species containing the first one-electron oxidation product of two water molecules, that is, [O5O6]3–. Progression of this form to the two-electron-oxidized peroxo and three-electron-oxidized superoxo forms, leading eventually to the evolution of triplet O2, is proposed to be the pathway nature adopts to oxidize water. The study reveals the key electronic, magnetic, and structural design features of nature’s catalyst which facilitates water oxidation to O2 under ambient conditions.

Dinuclear Cobalt Complexes for Homogeneous Water Oxidation: Tuning Rate and Overpotential through the Non-Innocent Ligand.

In this study, dinuclear cobalt complexes (1 and 2) featuring bis(benzimidazole)pyrazolide-type ligands (H2 L and Me2 L) were prepared and evaluated as molecular electrocatalysts for water oxidation. Notably, 1 bearing a non-innocent ligand (H2 L) displayed faster catalytic turnover than 2 under alkaline conditions, and the base dependence of water oxidation and kinetic isotope effect analysis indicated that the reaction mediated by 1 proceeded by a different mechanism relative to 2. Spectroelectrochemical, cold-spray ionization mass spectrometric and computational studies found that double deprotonation of 1 under alkaline conditions cathodically shifted the catalysis-initiating potential and further altered the turnover-limiting step from nucleophilic water attack on (H2 L)CoIII 2 (superoxo) to deprotonation of (L)CoIII 2 (OH)2 . The rate-overpotential analysis and catalytic Tafel plots showed that 1 exhibited a significantly higher rate than previously reported Ru-based dinuclear electrocatalysts at similar overpotentials. These observations suggest that using non-innocent ligands is a valuable strategy for designing effective metal-based molecular water oxidation catalysts.

Candidate for Catalyst during Water-Oxidation Reaction in the Presence of Manganese Compounds, from Nanosized Particles to Impurities: Sleep with One Eye Open.

Water-oxidation reaction (WOR) catalysts are critical for energy conversion. WOR is a four-electron oxidation and sluggish reaction. WOR needs a high thermodynamic driving force; it is also a kinetically slow reaction. Different compounds have been used for WOR; among these compounds, Mn materials have proven to be interesting because Mn is low-cost and also nontoxic, at least compared to many transition metals. Naturally, it has also been used in the biological water-oxidizing complex (WOC). Indeed, WOR has occurred on a huge scale in natural photosynthesis.For a long time, efforts have been made to design and synthesize various ligands and generate Mn compounds toward WOR catalysts. However, the addition or removal of electrons inside Mn compounds during harsh WOR conditions can lead to the formation or the breakage of bonds and result in the conversion of a precatalyst to a catalyst.Here, our findings on the conversion of Mn compounds to catalysts during WOR are presented. Many Mn compounds have been claimed to be catalysts for WOR in the presence of various chemical oxidants or under electrophotochemical conditions. Currently, the advances in characterization techniques and different spectroscopic methods have enabled a better understanding of catalysts. Different conversions such as that of the Mn complex to Mn oxide and Mn salts to Mn oxide during WOR have been explained. Indeed, the morphology and size of the Mn oxide formed depend on several factors such as the origin compounds, pH, ligands, and conditions. Thus, different Mn compounds show different activities toward WOR. The biomimetic models with Mn-Ca clusters are also decomposed during WOR. On the other hand, stable Mn complexes such as Mn phthalocyanines, which are very stable in the absence of potential, are easily decomposed during WOR. It is noted that for many of these Mn compounds, two steps result in the formation of Mn oxide during WOR: (i) Mn(II) or (III) leaching into the electrolyte and (ii) deposition of the leached Mn ions into the solution.Considering these steps, it can be seen that challenges remain in the area of Mn compounds, given the fact that even in the catalytic cycle at low oxidation numbers no Mn(II) or (III) should be leached to the electrolyte.

Macromolecular conformational changes in photosystem II: interaction between structure and function.

Conformational changes play an important role in the functioning of proteins and their complexes. This is also true for the pigment-protein super-complex of photosystem II (PSII). The data testify about the pH-induced macromolecular conformational changes in the water-oxidizing complex (WOC) on the donor side of PSII, the interaction between the spatial structure of WOC proteins and the distribution of cytochrome b559 redox-forms, and the electron transfer efficiency between QA and QB on the acceptor side of PSII. Changes in the protein environment near QA and QB can be observed after the removal of the bicarbonate ion associated with non-heme Fe or after the addition of herbicides binding to the QB site, which results in the suppression of the electron transfer in this site. The "locking" of the de novo assembled PSII in an inactive state until WOC activation is also accompanied by strong structural perturbations on the PSII acceptor and donor sides with the participation of Psb28 and Psb27 proteins. The triggers for degradation and replacement of damaged PSII proteins are structural changes induced by their oxidative modification and aggregation. Macromolecular changes in the antenna proteins underlie the activation of photoprotective non-photochemical quenching, which are induced by protonation of the lumenal residues of PsbS or/and Lhcsr3, as well as the phosphorylation of antenna proteins. Besides this, many smaller-scale conformational changes may occur in PSII. This review summarizes current knowledge about the possible conformational changes in proteins in the PSII super-complex and describes their proposed influence on PSII function.

Evidence for a robust photosystem II in the photosynthetic amoeba Paulinella.

Paulinella represents the only known case of an independent primary plastid endosymbiosis, outside Archaeplastida, that occurred c. 120 (million years ago) Ma. These photoautotrophs grow very slowly in replete culture medium with a doubling time of 6-7 d at optimal low light, and are highly sensitive to photodamage under moderate light levels. We used genomic and biophysical methods to investigate the extreme slow growth rate and light sensitivity of Paulinella, which are key to photosymbiont integration. All photosystem II (PSII) genes except psb28-2 and all cytochrome b6 f complex genes except petM and petL are present in Paulinella micropora KR01 (hereafter, KR01). Biophysical measurements of the water oxidation complex, variable chlorophyll fluorescence, and photosynthesis-irradiance curves show no obvious evidence of PSII impairment. Analysis of photoacclimation under high-light suggests that although KR01 can perform charge separation, it lacks photoprotection mechanisms present in cyanobacteria. We hypothesize that Paulinella species are restricted to low light environments because they are deficient in mitigating the formation of reactive oxygen species formed within the photosystems under peak solar intensities. The finding that many photoprotection genes have been lost or transferred to the host-genome during endosymbiont genome reduction, and may lack light-regulation, is consistent with this hypothesis.

Heterogenization of Molecular Water Oxidation Catalysts in Electrodes for (Photo)Electrochemical Water Oxidation

Water oxidation is still one of the most important challenges to develop efficient artificial photosynthetic devices. In recent decades, the development and study of molecular complexes for water oxidation have allowed insight into the principles governing catalytic activity and the mechanism as well as establish ligand design guidelines to improve performance. However, their durability and long-term stability compromise the performance of molecular-based artificial photosynthetic devices. In this context, heterogenization of molecular water oxidation catalysts on electrode surfaces has emerged as a promising approach for efficient long-lasting water oxidation for artificial photosynthetic devices. This review covers the state of the art of strategies for the heterogenization of molecular water oxidation catalysts onto electrodes for (photo)electrochemical water oxidation. An overview and description of the main binding strategies are provided explaining the advantages of each strategy and their scope. Moreover, selected examples are discussed together with the the differences in activity and stability between the homogeneous and the heterogenized system when reported. Finally, the common design principles for efficient (photo)electrocatalytic performance summarized.

XAS and EPR in Situ Observation of Ru(V) Oxo Intermediate in a Ru Water Oxidation Complex

AbstractInvited for this month's cover picture are the Rüdiger‐DeBeer‐Lloret groups. The cover shows a periodic table and the complementary XAS and EPR obtained by in situ spectroelectrochemistry to confirm the participation of the Ru(V) oxo in the catalytic water oxidation by this Ru molecular catalyst. Read the full text of the Communication at 10.1002/celc.202101271.

XAS and EPR in Situ Observation of Ru(V) Oxo Intermediate in a Ru Water Oxidation Complex.

In this study, we combine in situ spectroelectrochemistry coupled with electron paramagnetic resonance (EPR) and X‐ray absorption spectroscopies (XAS) to investigate a molecular Ru‐based water oxidation catalyst bearing a polypyridinic backbone [RuII(OH2)(Py2Metacn)]2+ . Although high valent key intermediate species arising in catalytic cycles of this family of compounds have remain elusive due to the lack of additional anionic ligands that could potentially stabilize them, mechanistic studies performed on this system proposed a water nucleophilic attack (WNA) mechanism for the O−O bond formation. Employing in situ experimental conditions and complementary spectroscopic techniques allowed to observe intermediates that provide support for a WNA mechanism, including for the first time a Ru(V) oxo intermediate based on the Py2Metacn ligand, in agreement with the previously proposed mechanism.

Isolation and Identification of Pseudo Seven-Coordinate Ru(III) Intermediate Completing the Catalytic Cycle of Ru-bda Type of Water Oxidation Catalysts

Isolation and Identification of Pseudo Seven-Coordinate Ru(III) Intermediate Completing the Catalytic Cycle of Ru-bda Type of Water Oxidation Catalysts

S3 State Models of Nature's Water Oxidizing Complex: Analysis of Bonding and Magnetic Exchange Pathways, Assessment of Experimental Electron Paramagnetic Resonance Data, and Implications for the Water Oxidation Mechanism.

Broken symmetry density functional theory (BS-DFT) calculations on large models of Nature's water oxidizing complex (WOC) are used to investigate the electronic structure and associated magnetic interactions of this key intermediate state. The electronic origins of the ferromagnetic and antiferromagnetic couplings between neighboring Mn ions are investigated and illustrated by using corresponding orbital transformations. Protonation of the O4 and/or O6 atoms leads to large variation in the distribution of spin around the complex with associated changes in its magnetic resonance properties. Models for Sr2+ exchange and methanol addition indicate minor perturbations reflected in slightly altered spin projection coefficients for the Mn1 and Mn2 ions. These are shown to account for the observed changes observed experimentally via electron paramagnetic resonance methods and suggest a reinterpretation of the experimental findings. By comparison with experimental determinations, we show that the spin projections and resulting calculated 55Mn hyperfine couplings support the open cubane form of an oxo (O5)-hydroxo (O6) cluster in all cases with no need to invoke a closed cubane intermediate. The implications of these findings for the water oxidation mechanism are discussed.

Switching the O–O bond-formation mechanism by controlling water activity

Switching the O–O bond-formation mechanism by controlling water activity

Involvement of Carbonic Anhydrase CAH3 in the Structural and Functional Stabilization of the Water-Oxidizing Complex of Photosystem II from Chlamydomonas reinhardtii.

The involvement of carbonic anhydrases (CA) and CA activity in the functioning of photosystem II (PSII) has been studied for a long time and has been shown in many works. However, so far only for CAH3 from Chlamydomonas reinhardtii there is evidence for its association with the donor side of PSII, where the CA activity of CAH3 can influence the functioning of the water-oxidizing complex (WOC). Our results suggest that CAH3 is also involved in the organization of the native structure of WOC independently of its CA activity. It was shown that in PSII preparations from wild type (WT) the high O2-evolving activity of WOC was observed up to 100 mM NaCl in the medium and practically did not decrease with increasing incubation time with NaCl. At the same time, the WOC function in PSII preparations from CAH3-deficient mutant cia3 is significantly inhibited already at NaCl concentrations above 35 mM, reaching 50% at 100 mM NaCl and increased incubation time. It is suggested that the absence of CAH3 in PSII from cia3 causes disruption of the native structure of WOC, allowing more pronounced conformational changes of its proteins and, consequently, suppression of the WOC active center function, when the ionic strength of the medium is increased. The results of Western blot analysis indicate a more difficult removal of PsbP protein from PSII of cia3 at higher NaCl concentrations, apparently due to the changes in the intermolecular interactions between proteins of WOC in the absence of CAH3. At the same time, the values of the maximum quantum yield of PSII did not practically differ between preparations from WT and cia3, indicating no effect of CAH3 on the photoinduced electron transfer in the reaction center of PSII. The obtained results indicate the involvement of the CAH3 protein in the native organization of the WOC and, as a consequence, in the stabilization of its functional state in PSII from C. reinhardtii.