Proton egress pathway during the S1–S2 transition of the Oxygen Evolving Complex of Photosystem II (original) (raw)
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Nature Communications
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 S2 to S3 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 ...
Redox Potential of the Oxygen-Evolving Complex in the Electron Transfer Cascade of Photosystem II
The Journal of Physical Chemistry Letters, 2019
In photosystem II (PSII), water oxidation occurs in the Mn 4 CaO 5 cluster with the release of electrons via the redox-active tyrosine (TyrZ) to the reaction-center chlorophylls (P D1 /P D2). Using a quantum mechanical/molecular mechanical approach, we report the redox potentials (E m) of these cofactors in the PSII protein environment. The E m values suggest that the Mn 4 CaO 5 cluster, TyrZ, and P D1 /P D2 form a downhill electron transfer pathway. E m for the first oxidation step, E m (S 0 /S 1), is uniquely low (730 mV) and is ∼100 mV lower than that for the second oxidation step, E m (S 1 /S 2) (830 mV) only when the O4 site of the Mn 4 CaO 5 cluster is protonated in S 0. The O4-water chain, which directly forms a low-barrier H-bond with the Mn 4 CaO 5 cluster and mediates protoncoupled electron transfer in the S 0 to S 1 transition, explains why the second lowest oxidation state, S 1 , is the most stable and S 0 is converted to S 1 even in the dark.
Electrostatics and proton transfer in photosynthetic water oxidation
Philosophical Transactions of the Royal Society B: Biological Sciences, 2002
Photosystem II (PSII) oxidizes two water molecules to yield dioxygen plus four protons. Dioxygen is released during the last out of four sequential oxidation steps of the catalytic centre (S 0 ⇒ S 1 , S 1 ⇒ S 2 , S 2 ⇒ S 3 , S 3 ⇒ S 4 → S 0 ). The release of the chemically produced protons is blurred by transient, highly variable and electrostatically triggered proton transfer at the periphery (Bohr effect). The extent of the latter transiently amounts to more than one H ϩ /e Ϫ under certain conditions and this is understood in terms of electrostatics. By kinetic analyses of electron-proton transfer and electrochromism, we discriminated between Bohr-effect and chemically produced protons and arrived at a distribution of the latter over the oxidation steps of 1 : 0 : 1 : 2. During the oxidation of tyr-161 on subunit D1 (Y Z ), its phenolic proton is not normally released into the bulk. Instead, it is shared with and confined in a hydrogenbonded cluster. This notion is difficult to reconcile with proposed mechanisms where Y Z acts as a hydrogen acceptor for bound water. Only in manganese (Mn) depleted PSII is the proton released into the bulk and this changes the rate of electron transfer between Y Z and the primary donor of PSII P ϩ 680 from electron to proton controlled. D1-His190, the proposed centre of the hydrogen-bonded cluster around Y Z , is probably further remote from Y Z than previously thought, because substitution of D1-Glu189, its direct neighbour, by Gln, Arg or Lys is without effect on the electron transfer from Y Z to P ϩ 680 (in nanoseconds) and from the Mn cluster to Y ox Z .
ACS Energy Letters
Photosystem II (PSII) oxidizes water to produce oxygen through a four-step photocatalytic cycle. Understanding PSII structure−function relations is important for the development of biomimetic photocatalytic systems. The quantum mechanics/molecular mechanics (QM/MM) analysis of substrate water binding to the oxygen-evolving complex (OEC) has suggested a rearrangement of water ligands in a carousel mechanism around a key Mn center. Here, we find that the most recently reported X-ray free-electron laser (XFEL) crystallographic data obtained for the dark-stable S 1 state and the doubly flashed S 3 state at 2.25 Å resolution support the carousel mechanism. The features in the XFEL data and QM/MM model-simulated difference Fourier maps suggest that water displacement may occur from the so-called "narrow" channel, resulting in binding of a new water molecule to the OEC, and thus provide new insights into the nature of rearrangements of water ligands along the catalytic cycle before OO bond formation.
Tracing the Pathways of Waters and Protons in Photosystem II and Cytochrome c Oxidase
Inorganics, 2019
Photosystem II (PSII) uses water as the terminal electron donor, producing oxygen in the Mn4CaO5 oxygen evolving complex (OEC), while cytochrome c oxidase (CcO) reduces O2 to water in its heme–Cu binuclear center (BNC). Each protein is oriented in the membrane to add to the proton gradient. The OEC, which releases protons, is located near the P-side (positive, at low-pH) of the membrane. In contrast, the BNC is in the middle of CcO, so the protons needed for O2 reduction must be transferred from the N-side (negative, at high pH). In addition, CcO pumps protons from N- to P-side, coupled to the O2 reduction chemistry, to store additional energy. Thus, proton transfers are directly coupled to the OEC and BNC redox chemistry, as well as needed for CcO proton pumping. The simulations that study the changes in proton affinity of the redox active sites and the surrounding protein at different states of the reaction cycle, as well as the changes in hydration that modulate proton transfer p...
Proceedings of the National Academy of Sciences
In oxygenic photosynthesis, light-driven oxidation of water to molecular oxygen is carried out by the oxygen-evolving complex (OEC) in photosystem II (PS II). Recently, we reported the room-temperature structures of PS II in the four (semi)stable S-states, S1, S2, S3, and S0, showing that a water molecule is inserted during the S2 → S3 transition, as a new bridging O(H)-ligand between Mn1 and Ca. To understand the sequence of events leading to the formation of this last stable intermediate state before O2 formation, we recorded diffraction and Mn X-ray emission spectroscopy (XES) data at several time points during the S2 → S3 transition. At the electron acceptor site, changes due to the two-electron redox chemistry at the quinones, QA and QB, are observed. At the donor site, tyrosine YZ and His190 H-bonded to it move by 50 µs after the second flash, and Glu189 moves away from Ca. This is followed by Mn1 and Mn4 moving apart, and the insertion of OX(H) at the open coordination site o...
Biochimica et Biophysica Acta (BBA) - Bioenergetics, 2004
The pulsed electron paramagnetic resonance (EPR) methods of electron spin echo envelope modulation (ESEEM) and electron spin echoelectron nuclear double resonance (ESE-ENDOR) are used to investigate the structure of the Photosystem II oxygen-evolving complex (OEC), including the paramagnetic manganese cluster and its immediate surroundings. Recent unpublished results from the pulsed EPR laboratory at UC-Davis are discussed, along with aspects of recent publications, with a focus on substrate and cofactor interactions. New data on the proximity of exchangeable deuterons around the Mn cluster poised in the S 0 -state are presented and interpreted. These pulsed EPR results are used in an evaluation of several recently proposed mechanisms for PSII water oxidation. We strongly favor mechanistic models where the substrate waters bind within the OEC early in the S-state cycle. Models in which the OUO bond is formed by a nucleophilic attack by a Ca 2 + -bound water on a strong S 4 -state electrophile provide a good match to the pulsed EPR data. D
Oxygen evolving complex in Photosystem II: Better than excellent
The Oxygen Evolving Complex in photosystem II, which is responsible for the oxidation of water to oxygen in plants, algae and cyanobacteria, contains a cluster of one calcium and four manganese atoms. This cluster serves as a model for the splitting of water by energy obtained from sunlight. The recent published data on the mechanism and the structure of photosystem II provide a detailed architecture of the oxygen-evolving complex and the surrounding amino acids. Biomimetically, we expect to learn some strategies from this natural system to synthesize an efficient catalyst for water oxidation, that is necessary for artificial photosynthesis.
Structural Changes of the Oxygen-evolving Complex in Photosystem II during the Catalytic Cycle
Journal of Biological Chemistry, 2013
Background: Mn 4 CaO 5 cluster catalyzes water oxidation in photosystem II. Results: Mn-Mn/Ca/ligand distances and changes in the structure of the Mn 4 CaO 5 cluster are determined for the intermediate states in the reaction using x-ray spectroscopy. Conclusion: Position of one bridging oxygen and related geometric changes may be critical during catalysis. Significance: Knowledge about structural changes during catalysis is crucial for understanding the O-O bond formation mechanism in PSII.