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

Rana Hussein ,R Alonso‐Mori ,Kyle D Sutherlin ,Franklin D Fuller ,Vittal K Yachandra ,Holger Dobbek ,Cindy C Pham ,In-Sik Kim ,Sergio Carbajo ,Robert Bolotovsky ,Mun Hon Cheah ,Mohamed Ibrahim ,Paul D Adams ,Philipp S Simon ,Asmit Bhowmick ,Johannes Messinger ,Petko Chernev ,James M Holton ,Athina Zouni ,Margaret Doyle ,Jan Kern ,Derek Mendez ,Aaron S Brewster ,Louise Lassalle ,Casper De Lichtenberg ,Ruchira Chatterjee ,Sheraz Gul ,Uwe Bergmann ,Nigel W Moriarty ,I.d Young ,Alex Batyuk ,Isabel Bogacz ,Nicholas K Sauter ,Junko Yano

doi:10.1038/s41467-021-26781-z

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.

Highlights

A high-resolution dataset was generated by merging more than one hundred thousand high-quality diffraction images collected at room temperature (RT) from PS II crystals in various illumination states and a structure was refined to a resolution of 1.89 Å (Supplementary Table 2)
We evaluate the motion of waters and amino acid residues along the channels using the RT crystallography data collected for the S2 (200 ms after one flash (1 F)) and the S3 state (200 ms after the 2nd flash (2 F)), and four-time points (50, 150, 250, and 400 μs after the 2nd flash) during the S2 to S3 transition (Supplementary Table 2), where both a proton release and water insertion occur
Our study investigates the motion of waters and surrounding amino acid residues using snapshots of the RT crystal structures of PS II to identify substrate water and proton release channels

Summary

Introduction

With static methods (for example, using standard software packages like CAVER or MOLE to map cavities and channels). The ability to take snapshots of the structure at the various time points at RT during the reaction allows for the investigation of water movements and changes in hydrogenbonding networks in proteins[12]. These studies can provide new insights into the reaction mechanism in PS II by potentially identifying water and proton pathways. They provide starting models for MD simulations, using RT structures that are the catalytically relevant and functional states, along a reaction trajectory. There was no indication of the suggested rearrangement of the cluster between an “opencubane” and a “closed-cubane” structure[31]

Methods

Results

Conclusion