Invited Paper HC+SS-FrM3
Water Oxidation Reaction in Natural Photosynthesis

Friday, October 25, 2019, 9:00 am, Room A213

Many of the catalytic reactions in inorganic systems and natural enzymes involve multiple electrons, and proceed through several intermediate steps. For example, photosynthetic water oxidation in nature is catalyzed by the metal center that consists of oxo-bridged four Mn and one Ca atoms, which is located in multi-subunit membrane protein, Photosystem II (PSII). This is one of the most important, life-sustaining chemical processes occurring in the biosphere. The oxygen-evolving complex (OEC) in PSII, which contains the heteronuclear Mn₄CaO₅ cluster, catalyses the reaction

2H₂O → O₂ + 4e- + 4H+

that couples the four-electron oxidation of water with the one-electron photochemistry occurring at the PSII reaction center. The OEC cycles through five intermediate S-states (S₀ to S₄) that corresponds to the abstraction of four successive electrons from the OEC (Fig. 1). Once four oxidizing equivalents are accumulated (S₄-state), a spontaneous reaction occurs that results in the release of O₂ and the formation of the S₀-state.

Recently, the development of X-ray Free Electron Lasers (XFELs) has opened up opportunities for studying the dynamics of biological systems. Intense XFEL pulses enable us to apply both X-ray diffraction and X-ray spectroscopic techniques to dilute systems or small protein crystals. By taking advantage of ultra-bright femtosecond X-ray pulses, one can also collect the data under functional conditions of temperature and pressure, in a time-resolved manner, after initiating reactions, and follow the chemical dynamics during catalytic reactions and electron transfer. Such an approach is particularly beneficial for biological materials and aqueous solution samples that are susceptible to X-ray radiation damage.

We have developed spectroscopy and diffraction techniques necessary to fully utilize the capability of the XFEL x-rays for a wide-variety of metalloenzymes, like Photosystem II, and to study their chemistry under functional conditions. One of such methods is simultaneous data collection for x-ray crystallography and x-ray spectroscopy, to look at overall structural changes of proteins and chemical changes at metal catalytic sites. We have used the above techniques to study the water oxidation reaction of Photosystem II, in which the Mn₄CaO₅ cluster catalyzes the reaction. The current status of this research and the mechanistic understanding of the water oxidation reaction based on the X-ray techniques is presented.