Light-Dependent Production of Dioxygen in Photosynthesis

Oxygen, that supports all aerobic life, is abundant in the atmosphere because of its constant regeneration by photosynthetic water oxidation, which is catalyzed by a Mn₄CaO₅ cluster in photosystem II (PS II), a multi subunit membrane protein complex. X-ray and other spectroscopy studies of the electronic and geometric structure of the Mn₄CaO₅ cluster as it advances through the intermediate states have been important for understanding the mechanism of water oxidation. The results and interpretations, especially from X-ray spectroscopy studies, regarding the geometric and electronic structure and the changes as the system proceeds through the catalytic cycle will be summarized in this review. This review will also include newer methodologies in time-resolved X-ray diffraction and spectroscopy that have become available since the commissioning of the X-ray free electron laser (XFEL) and are being applied to study the oxygen-evolving complex (OEC). The femtosecond X-ray pulses of the XFEL allows us to outrun X-ray damage at room temperature, and the time-evolution of the photo-induced reaction can be probed using a visible laser-pump followed by the X-ray-probe pulse. XFELs can be used to simultaneously determine the light-induced protein dynamics using crystallography and the local chemistry that occurs at the catalytic center using X-ray spectroscopy under functional conditions. Membrane inlet mass spectrometry has been important for providing direct information about the exchange of substrate water molecules, which has a direct bearing on the mechanism of water oxidation. Moreover, it has been indispensable for the time-resolved X-ray diffraction and spectroscopy studies and will be briefly reviewed in this chapter. Given the role of PS II in maintaining life in the biosphere and the future vision of a renewable energy economy, understanding the structure and mechanism of the photosynthetic water oxidation catalyst is an important goal for the future

Computational insights into the O2-evolving complex of photosystem II

Mechanistic investigations of the water-splitting reaction of the oxygen-evolving complex (OEC) of photosystem II (PSII) are fundamentally informed by structural studies. Many physical techniques have provided important insights into the OEC structure and function, including X-ray diffraction (XRD) and extended X-ray absorption fine structure (EXAFS) spectroscopy as well as mass spectrometry (MS), electron paramagnetic resonance (EPR) spectroscopy and Fourier transform infrared spectroscopy applied in conjunction with mutagenesis studies. However, experimental studies have yet to yield consensus as to the exact configuration of the catalytic metal cluster and its ligation scheme. Computational modeling studies, including density functional (DFT) theory combined with quantum mechanics/molecular mechanics (QM/MM) hybrid methods for explicitly including the influence of the surrounding protein, have proposed chemically satisfactory models of the fully ligated OEC within PSII that are maximally consistent with experimental results. The inorganic core of these models is similar to the crystallographic model upon which they were based but comprises important modifications due to structural refinement, hydration and proteinaceous ligation which improve agreement with a wide range of experimental data. The computational models are useful for rationalizing spectroscopic and crystallographic results and for building a complete structure-based mechanism of water-splitting in PSII as described by the intermediate oxidation states of the OEC. This review summarizes these recent advances in QM/MM modeling of PSII within the context of recent experimental studies