Dataset Information

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

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 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.

SUBMITTER: Hussein R

PROVIDER: S-EPMC8585918 | biostudies-literature | 2021 Nov

REPOSITORIES: biostudies-literature

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Publications

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

Hussein Rana R Ibrahim Mohamed M Bhowmick Asmit A Simon Philipp S PS Chatterjee Ruchira R Lassalle Louise L Doyle Margaret M Bogacz Isabel I Kim In-Sik IS Cheah Mun Hon MH Gul Sheraz S de Lichtenberg Casper C Chernev Petko P Pham Cindy C CC Young Iris D ID Carbajo Sergio S Fuller Franklin D FD Alonso-Mori Roberto R Batyuk Alex A Sutherlin Kyle D KD Brewster Aaron S AS Bolotovsky Robert R Mendez Derek D Holton James M JM Moriarty Nigel W NW Adams Paul D PD Bergmann Uwe U Sauter Nicholas K NK Dobbek Holger H Messinger Johannes J Zouni Athina A Kern Jan J Yachandra Vittal K VK Yano Junko J

Nature communications 20211111 1

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 w ...[more]

PMID: 34764256

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Project description:One of the reasons for the high efficiency and selectivity of biological catalysts arise from their ability to control the pathways of substrates and products using protein channels, and by modulating the transport in the channels using the interaction with the protein residues and the water/hydrogen-bonding network. This process is clearly demonstrated in Photosystem II (PS II), where its light-driven water oxidation reaction catalyzed by the Mn4CaO5 cluster occurs deep inside the protein complex and thus requires the transport of two water molecules to and four protons from the metal center to the bulk water. Based on the recent advances in structural studies of PS II from X-ray crystallography and cryo-electron microscopy, in this review we compare the channels that have been proposed to facilitate this mass transport in cyanobacteria, red and green algae, diatoms, and higher plants. The three major channels (O1, O4, and Cl1 channels) are present in all species investigated; however, some differences exist in the reported structures that arise from the different composition and arrangement of membrane extrinsic subunits between the species. Among the three channels, the Cl1 channel, including the proton gate, is the most conserved among all photosynthetic species. We also found at least one branch for the O1 channel in all organisms, extending all the way from Ca/O1 via the 'water wheel' to the lumen. However, the extending path after the water wheel varies between most species. The O4 channel is, like the Cl1 channel, highly conserved among all species while having different orientations at the end of the path near the bulk. The comparison suggests that the previously proposed functionality of the channels in T. vestitus (Ibrahim et al., Proc Natl Acad Sci USA 117:12624-12635, 2020; Hussein et al., Nat Commun 12:6531, 2021) is conserved through the species, i.e. the O1-like channel is used for substrate water intake, and the tighter Cl1 and O4 channels for proton release. The comparison does not eliminate the potential role of O4 channel as a water intake channel. However, the highly ordered hydrogen-bonded water wire connected to the Mn4CaO5 cluster via the O4 may strongly suggest that it functions in proton release, especially during the S0 → S1 transition (Saito et al., Nat Commun 6:8488, 2015; Kern et al., Nature 563:421-425, 2018; Ibrahim et al., Proc Natl Acad Sci USA 117:12624-12635, 2020; Sakashita et al., Phys Chem Chem Phys 22:15831-15841, 2020; Hussein et al., Nat Commun 12:6531, 2021).

Dataset Information

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

Publications

Structural dynamics in the water and proton channels of photosystem II during the S<sub>2</sub> to S<sub>3</sub> transition.

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