O2 evolution electrocatalysis:Electronic, atomic, and nanoscale dynamics matter

In Nature, Mefford, Chueh, and colleagues describe how they investigated the oxygen evolution reaction (OER) in situ at sub-micrometer resolution. Nanoscale variations of current density, geometry, and oxidation states show that the currently emerging and potentially paradigm-shifting picture of redox-active, structurally dynamic catalyst materials might need to include the nanoscale

New aspects of operando Raman spectroscopy applied to electrochemical CO2 reduction on Cu foams

The mechanism of electrochemical CO2 reduction (CO2RR) on copper surfaces is still insufficiently understood. Operando Raman spectroscopy is ideally suited to elucidate the role of adsorbed reaction intermediates and products. For a Cu foam material which has been previously characterized regarding electrochemical properties and product spectrum, 129 operando spectra are reported, covering the spectral range from 250 to 3300 cm−1. (1) The dendritic foam structure facilitates surface-enhanced Raman spectroscopy (SERS) and thus electrochemical operando spectroscopy, without any further surface manipulations. (2) Both Raman enhancement and SERS background depend strongly on the electric potential and the “history” of preceding potential sequences. (3) To restore the plausible intensity dependencies of Raman bands, normalization to the SERS background intensity is proposed. (4) Two distinct types of *CO adsorption modes are resolved. (5) Hysteresis in the potential-dependent *CO desorption supports previous electrochemical analyses; saturating *CO adsorption may limit CO formation rates. (6) HCO3− likely deprotonates upon adsorption so that exclusively adsorbed carbonate is detectable, but with strong dependence on the preceding potential sequences. (7) A variety of species and adsorption modes of reaction products containing C—H bonds were detected and compared to reference solutions of likely reaction products, but further investigations are required for assignment to specific molecular species. (8) The Raman bands of adsorbed reaction products depend weakly or strongly on the preceding potential sequences. In future investigations, suitably designed potential protocols could provide valuable insights into the potential-dependent kinetics of product formation, adsorption, and desorption

Structural models of the manganese complex of photosystem II and mechanistic implications

Photosynthetic water oxidation and O2 formation are catalyzed by a Mn4Ca complex bound to the proteins of photosystem II (PSII). The catalytic site, including the inorganic Mn4CaOnHx core and its protein environment, is denoted as oxygen-evolving complex (OEC). Earlier and recent progress in the endeavor to elucidate the structure of the OEC is reviewed, with focus on recent results obtained by (i) X-ray spectroscopy (specifically by EXAFS analyses), and (ii) X-ray diffraction (XRD, protein crystallography). Very recently, an impressive resolution of 1.9 Å has been achieved by XRD. Most likely however, all XRD data on the Mn4CaOnHx core of the OEC are affected by X-ray induced modifications (radiation damage). Therefore and to address (important) details of the geometric and electronic structure of the OEC, a combined analysis of XRD and XAS data has been approached by several research groups. These efforts are reviewed and extended using an especially comprehensive approach. Taking into account XRD results on the protein environment of the inorganic core of the Mn complex, 12 alternative OEC models are considered and evaluated by quantitative comparison to (i) extended-range EXAFS data, (ii) polarized EXAFS of partially oriented PSII membrane particles, and (iii) polarized EXAFS of PSII crystals. We conclude that there is a class of OEC models that is in good agreement with both the recent crystallographic models and the XAS data. On these grounds, mechanistic implications for the Osingle bondO bond formation chemistry are discussed. This article is part of a Special Issue entitled: Photosystem II

Valinomycin sensitivity proves that light-induced thylakoid voltages result in millisecond phase of chlorophyll fluorescence transients

AbstractUpon sudden exposure of plants to an actinic light of saturating intensity, the yield of chlorophyll fluorescence increases typically by 200–400% of the initial O-level. At least three distinct phases of these O–J–I–P transients can be resolved: O–J (0.05–5 ms), J–I (5–50 ms), and I–P (50–1000 ms). In thylakoid membranes, the J–I increase accounts for ∼30% of the total fluorescence increase; in Photosystem II membranes, the J–I phase is always lacking. In the presence of the ionophore valinomycin, which is known to inhibit specifically the formation of membrane voltages, the magnitude of the J–I phase is clearly diminished; in the presence of valinomycin supplemented by potassium, the J–I phase is fully suppressed. We conclude that the light-driven formation of the thylakoid-membrane voltage results in an increase of the chlorophyll excited-state lifetime, a phenomenon explainable by the electric-field-induced shift of the free-energy level of the primary radical pair [Dau and Sauer, Biochim. Biophys. Acta 1102 (1992) 91]. The assignment of the J–I increase in the fluorescence yield enhances the potential of using O–J–I–P fluorescence transients for investigations on photosynthesis in intact organisms. A putative role of thylakoid voltages in protection of PSII against photoinhibitory damage is discussed

Applicability of Transition State Theory to the (Proton-Coupled) Electron Transfer in Photosynthetic Water Oxidation with Emphasis on the Entropy of Activation

Recent advancements in the study of the protein complex photosystem II have clarified the sequence of events leading to the formation of oxygen during the S3 → S4 → S0 transition, wherein the inorganic Mn4Ca(µ-O)6(OHx)4 cluster finishes photo-catalyzing the water splitting reaction (Greife et al., Nature 2023, 617, 623–628; Bhowmick et al., Nature 2023, 617, 629–636). During this final step, a tyrosine radical (TyrZ), stable for a couple of milliseconds, oxidizes a cluster-bound oxygen while the hydrogen bonding patterns of nearby waters shift a proton away. A treatment of this redox reaction within the context of accepted transition state theories predicts rate constants that are significantly higher than experimentally recovered values (1012 s−1 versus 103 s−1). In an effort to understand this disparity, temperature-dependent experiments have revealed large entropic contributions to the rates with only a moderate enthalpy of activation. We suggest that the entropic source may be related to the observed proton rearrangements, and further possible near isoenergetic variations in the nearby extended H-bonding network delaying the realization of an ‘ideal’ transition state. In the following, we explore this relation in the context of Eyring’s transition state theory and Marcus’ electron transfer theory and evaluate their compatibility with the experimental evidence

Extended protein/water H-bond networks in photosynthetic water oxidation

Oxidation of water molecules in the photosystem II (PSII) protein complex proceeds at the manganese–calcium complex, which is buried deeply in the lumenal part of PSII. Understanding the PSII function requires knowledge of the intricate coupling between the water-oxidation chemistry and the dynamic proton management by the PSII protein matrix. Here we assess the structural basis for long-distance proton transfer in the interior of PSII and for proton management at its surface. Using the recent high-resolution crystal structure of PSII, we investigate prominent hydrogen-bonded networks of the lumenal side of PSII. This analysis leads to the identification of clusters of polar groups and hydrogen-bonded networks consisting of amino acid residues and water molecules. We suggest that long-distance proton transfer and conformational coupling is facilitated by hydrogen-bonded networks that often involve more than one protein subunit. Proton-storing Asp/Glu dyads, such as the D1-E65/D2-E312 dyad connected to a complex water-wire network, may be particularly important for coupling protonation states to the protein conformation. Clusters of carboxylic amino acids could participate in proton management at the lumenal surface of PSII. We propose that rather than having a classical hydrophobic protein interior, the lumenal side of PSII resembles a complex polyelectrolyte with evolutionary optimized hydrogen-bonding networks. This article is part of a Special Issue entitled: Photosynthesis Research for Sustainability: from Natural to Artificial

Alternating electron and proton transfer steps in photosynthetic water oxidation

Water oxidation by cyanobacteria, algae, and plants is pivotal in oxygenic photosynthesis, the process that powers life on Earth, and is the paradigm for engineering solar fuel–production systems. Each complete reaction cycle of photosynthetic water oxidation requires the removal of four electrons and four protons from the catalytic site, a manganese–calcium complex and its protein environment in photosystem II. In time-resolved photothermal beam deflection experiments, we monitored apparent volume changes of the photosystem II protein associated with charge creation by light-induced electron transfer (contraction) and charge-compensating proton relocation (expansion). Two previously invisible proton removal steps were detected, thereby filling two gaps in the basic reaction-cycle model of photosynthetic water oxidation. In the S2 → S3 transition of the classical S-state cycle, an intermediate is formed by deprotonation clearly before electron transfer to the oxidant (Graphic). The rate-determining elementary step (τ, approximately 30 µs at 20 °C) in the long-distance proton relocation toward the protein–water interface is characterized by a high activation energy (Ea = 0.46 ± 0.05 eV) and strong H/D kinetic isotope effect (approximately 6). The characteristics of a proton transfer step during the S0 → S1 transition are similar (τ, approximately 100 µs; Ea = 0.34 ± 0.08 eV; kinetic isotope effect, approximately 3); however, the proton removal from the Mn complex proceeds after electron transfer to Graphic. By discovery of the transient formation of two further intermediate states in the reaction cycle of photosynthetic water oxidation, a temporal sequence of strictly alternating removal of electrons and protons from the catalytic site is established

Copper Carbonate Hydroxide as Precursor of Interfacial CO in CO2 Electroreduction

Copper electrodes are especially effective in catalysis of C2 and further multi-carbon products in the CO2 reduction reaction (CO2RR) and therefore of major technological interest. The reasons for the unparalleled Cu performance in CO2RR are insufficiently understood. Here, the electrode–electrolyte interface was highlighted as a dynamic physical-chemical system and determinant of catalytic events. Exploiting the intrinsic surface-enhanced Raman effect of previously characterized Cu foam electrodes, operando Raman experiments were used to interrogate structures and molecular interactions at the electrode–electrolyte interface at subcatalytic and catalytic potentials. Formation of a copper carbonate hydroxide (CuCarHyd) was detected, which resembles the mineral malachite. Its carbonate ions could be directly converted to CO at low overpotential. These and further experiments suggested a basic mode of CO2/carbonate reduction at Cu electrodes interfaces that contrasted previous mechanistic models: the starting point in carbon reduction was not CO2 but carbonate ions bound to the metallic Cu electrode in form of CuCarHyd structures. It was hypothesized that Cu oxides residues could enhance CO2RR indirectly by supporting formation of CuCarHyd motifs. The presence of CuCarHyd patches at catalytic potentials might result from alkalization in conjunction with local electrical potential gradients, enabling the formation of metastable CuCarHyd motifs over a large range of potentials

Photosynthetic dioxygen formation studied by time-resolved delayed fluorescence measurements — Method, rationale, and results on the activation energy of dioxygen formation

AbstractThe analysis of the time-resolved delayed fluorescence (DF) measurements represents an important tool to study quantitatively light-induced electron transfer as well as associated processes, e.g. proton movements, at the donor side of photosystem II (PSII). This method can provide, inter alia, insights in the functionally important inner-protein proton movements, which are hardly detectable by conventional spectroscopic approaches. The underlying rationale and experimental details of the method are described. The delayed emission of chlorophyll fluorescence of highly active PSII membrane particles was measured in the time domain from 10 μs to 60 ms after each flash of a train of nanosecond laser pulses. Focusing on the oxygen-formation step induced by the third flash, we find that the recently reported formation of an S4-intermediate prior to the onset of O–O bond formation [M. Haumann, P. Liebisch, C. Müller, M. Barra, M. Grabolle, H. Dau, Science 310, 1019–1021, 2006] is a multiphasic process, as anticipated for proton movements from the manganese complex of PSII to the aqueous bulk phase. The S4-formation involves three or more likely sequential steps; a tri-exponential fit yields time constants of 14, 65, and 200 μs (at 20 °C, pH 6.4). We determine that S4-formation is characterized by a sizable difference in Gibbs free energy of more than 90 meV (20 °C, pH 6.4). In the second part of the study, the temperature dependence (−2.7 to 27.5 °C) of the rate constant of dioxygen formation (600/s at 20 °C) was investigated by analysis of DF transients. If the activation energy is assumed to be temperature-independent, a value of 230 meV is determined. There are weak indications for a biphasicity in the Arrhenius plot, but clear-cut evidence for a temperature-dependent switch between two activation energies, which would point to the existence of two distinct rate-limiting steps, is not obtained

Fast structural changes (200–900 ns) may prepare the photosynthetic manganese complex for oxidation by the adjacent tyrosine radical

The Mn complex of photosystem II (PSII) cycles through 4 semi-stable states (S0 to S3). Laser-flash excitation of PSII in the S2 or S3 state induces processes with time constants around 350 ns, which have been assigned previously to energetic relaxation of the oxidized tyrosine (YZox). Herein we report monitoring of these processes in the time domain of hundreds of nanoseconds by photoacoustic (or ‘optoacoustic’) experiments involving pressure-wave detection after excitation of PSII membrane particles by ns- laser flashes. We find that specifically for excitation of PSII in the S2 state, nuclear rearrangements are induced which amount to a contraction of PSII by at least 30 Å3 (time constant of 350 ns at 25 °C; activation energy of 285 +/− 50 meV). In the S3 state, the 350-ns-contraction is about 5 times smaller whereas in S0 and S1, no volume changes are detectable in this time domain. It is proposed that the classical S2 = > S3 transition of the Mn complex is a multi-step process. The first step after YZox formation involves a fast nuclear rearrangement of the Mn complex and its protein–water environment (~ 350 ns), which may serve a dual role: (1) The Mn‐ complex entity is prepared for the subsequent proton removal and electron transfer by formation of an intermediate state of specific (but still unknown) atomic structure. (2) Formation of the structural intermediate is associated (necessarily) with energetic relaxation and thus stabilization of YZox so that energy losses by charge recombination with the QA− anion radical are minimized. The intermediate formed within about 350 ns after YZox formation in the S2-state is discussed in the context of two recent models of the S2 = > S3 transition of the water oxidation cycle. This article is part of a Special Issue entitled: Photosynthesis Research for Sustainability: From Natural to Artificial