posted on 2024-06-04, 17:36authored byJinchan Liu, Ke R. Yang, Zhuoran Long, William H. Armstrong, Gary W. Brudvig, Victor S. Batista
Understanding how water ligands regulate the conformational
changes
and functionality of the oxygen-evolving complex (OEC) in photosystem
II (PSII) throughout the catalytic cycle of oxygen evolution remains
a highly intriguing and unresolved challenge. In this study, we investigate
the effect of water insertion (WI) on the redox state of the OEC by
using the molecular dynamics (MD) and quantum mechanics/molecular
mechanics (QM/MM) hybrid methods. We find that water binding significantly
reduces the free energy change for proton-coupled electron transfer
(PCET) from Mn to YZ•, underscoring the
important regulatory role of water binding, which is essential for
enabling the OEC redox-leveling mechanism along the catalytic cycle.
We propose a water binding mechanism in which WI is thermodynamically
favored by the closed-cubane form of the OEC, with water delivery
mediated by Ca2+ ligand exchange. Isomerization from the
closed- to open-cubane conformation at three post-WI states highlights
the importance of the location of the MnIII center in the
OEC and the orientation of its Jahn–Teller axis to conformational
changes of the OEC, which might be critical for the formation of the
O–O bond. These findings reveal a complex interplay between
conformational changes in the OEC and the ligand environment during
the activation of the OEC by YZ•. Analogous
regulatory effects due to water ligand binding are expected to be
important for a wide range of catalysts activated by redox state transitions
in aqueous environments.