Structural dynamics in the water and proton channels of photosystem II during the S2 to S3 transition

AbstractLight-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 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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Untangling the sequence of events during the S2→ S3transition in photosystem II and implications for the water oxidation mechanism

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2000529117 ◽

2020 ◽

Vol 117 (23) ◽

pp. 12624-12635 ◽

Cited By ~ 20

Author(s):

Mohamed Ibrahim ◽

Thomas Fransson ◽

Ruchira Chatterjee ◽

Mun Hon Cheah ◽

Rana Hussein ◽

...

Keyword(s):

Photosystem Ii ◽

Water Oxidation ◽

Donor Site ◽

Oxidation Mechanism ◽

Oxygenic Photosynthesis ◽

Acceptor Site ◽

Oxygen Evolving Complex ◽

Ps Ii ◽

Sequence Of Events ◽

Large Channel

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→ S3transition, 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 O2formation, we recorded diffraction and Mn X-ray emission spectroscopy (XES) data at several time points during the S2→ S3transition. At the electron acceptor site, changes due to the two-electron redox chemistry at the quinones, QAand QB, are observed. At the donor site, tyrosine YZand 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 of Mn1. This water, possibly a ligand of Ca, could be supplied via a “water wheel”-like arrangement of five waters next to the OEC that is connected by a large channel to the bulk solvent. XES spectra show that Mn oxidation (τ of ∼350 µs) during the S2→ S3transition mirrors the appearance of OXelectron density. This indicates that the oxidation state change and the insertion of water as a bridging atom between Mn1 and Ca are highly correlated.

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Hydration of Amino Acid Side Chains: Nonpolar and Electrostatic Contributions Calculated from Staged Molecular Dynamics Free Energy Simulations with Explicit Water Molecules

The Journal of Physical Chemistry B ◽

10.1021/jp048502c ◽

2004 ◽

Vol 108 (42) ◽

pp. 16567-16576 ◽

Cited By ~ 164

Author(s):

Yuqing Deng ◽

Benoît Roux

Keyword(s):

Molecular Dynamics ◽

Free Energy ◽

Amino Acid ◽

Water Molecules ◽

Side Chains ◽

Amino Acid Side Chains ◽

Energy Simulations ◽

Explicit Water

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Photosystem II oxygen-evolving complex photoassembly displays an inverse H/D solvent isotope effect under chloride-limiting conditions

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1910231116 ◽

2019 ◽

Vol 116 (38) ◽

pp. 18917-18922 ◽

Cited By ~ 10

Author(s):

David J. Vinyard ◽

Syed Lal Badshah ◽

M. Rita Riggio ◽

Divya Kaur ◽

Annaliesa R. Fanguy ◽

...

Keyword(s):

Amino Acid ◽

Photosystem Ii ◽

Isotope Effect ◽

Water Oxidation ◽

Oxygenic Photosynthesis ◽

Oxygen Evolving Complex ◽

Solvent Isotope Effect ◽

Solvent Isotope ◽

Oxygen Evolving ◽

Protein Environment

Photosystem II (PSII) performs the solar-driven oxidation of water used to fuel oxygenic photosynthesis. The active site of water oxidation is the oxygen-evolving complex (OEC), a Mn4CaO5 cluster. PSII requires degradation of key subunits and reassembly of the OEC as frequently as every 20 to 40 min. The metals for the OEC are assembled within the PSII protein environment via a series of binding events and photochemically induced oxidation events, but the full mechanism is unknown. A role of proton release in this mechanism is suggested here by the observation that the yield of in vitro OEC photoassembly is higher in deuterated water, D2O, compared with H2O when chloride is limiting. In kinetic studies, OEC photoassembly shows a significant lag phase in H2O at limiting chloride concentrations with an apparent H/D solvent isotope effect of 0.14 ± 0.05. The growth phase of OEC photoassembly shows an H/D solvent isotope effect of 1.5 ± 0.2. We analyzed the protonation states of the OEC protein environment using classical Multiconformer Continuum Electrostatics. Combining experiments and simulations leads to a model in which protons are lost from amino acid that will serve as OEC ligands as metals are bound. Chloride and D2O increase the proton affinities of key amino acid residues. These residues tune the binding affinity of Mn2+/3+ and facilitate the deprotonation of water to form a proposed μ-hydroxo bridged Mn2+Mn3+ intermediate.

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Predicting the Strength of Stacking Interactions Between Heterocycles and Aromatic Amino Acid Side Chains

10.26434/chemrxiv.7628939.v2 ◽

2019 ◽

Author(s):

Andrea N. Bootsma ◽

Analise C. Doney ◽

Steven Wheeler

Keyword(s):

Amino Acid ◽

Binding Sites ◽

Aromatic Amino Acid ◽

Aromatic Amino Acids ◽

Biologically Active ◽

Side Chains ◽

Stacking Interactions ◽

Inhibitor Binding ◽

Protein Binding Sites ◽

Amino Acid Side Chains

Despite the ubiquity of stacking interactions between heterocycles and aromatic amino acids in biological systems, our ability to predict their strength, even qualitatively, is limited. Based on rigorous ab initio data, we have devised a simple predictive model of the strength of stacking interactions between heterocycles commonly found in biologically active molecules and the amino acid side chains Phe, Tyr, and Trp. This model provides rapid predictions of the stacking ability of a given heterocycle based on readily-computed heterocycle descriptors. We show that the values of these descriptors, and therefore the strength of stacking interactions with aromatic amino acid side chains, follow simple predictable trends and can be modulated by changing the number and distribution of heteroatoms within the heterocycle. This provides a simple conceptual model for understanding stacking interactions in protein binding sites and optimizing inhibitor binding in drug design.

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A Strategy for Thioamide Incorporation During Fmoc Solid-Phase Peptide Synthesis with Robust Stereochemical Integrity

10.26434/chemrxiv.8206247.v1 ◽

2019 ◽

Cited By ~ 1

Author(s):

luis camacho III ◽

Bryan J. Lampkin ◽

Brett VanVeller

Keyword(s):

Amino Acid ◽

Functional Groups ◽

Peptide Synthesis ◽

Solid Phase ◽

Solid Phase Peptide Synthesis ◽

Side Chains ◽

Amino Acid Side Chains ◽

Peptide Elongation

We describe a method to protect the sensitive stereochemistry of the thioamide—in analogy to the protection of the functional groups of amino acid side chains—in order to preserve the thioamide moiety during peptide elongation.

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