Chemistry Colloquium

The solar water-splitting protein complex, photosystem II (PSII), catalyzes one of the most energetically demanding reactions in Nature by using light energy to drive the catalytic oxidation of water. Proton-coupled electron transfer (PCET) reactions, which are exquisitely tuned by smart protein matrix effects, are central to this water-splitting chemistry. PSII contains two symmetrically placed tyrosine residues, YD and YZ, one on each subunit of the heterodimeric core. The functions of these symmetry-related tyrosines are quite distinct, a versatility provided by their distinct local environments in PSII. YZ is kinetically competent and has been proposed to be directly involved in the PCET reactions of water oxidation. In contrast, the YD PCET redox poises the catalytic Mn4 cluster and may electrostatically tune the adjacent monomeric redox-active chlorophyll and -carotene in the secondary ET pathway of PSII. We have developed novel EPR methods for the study of powder and oriented PSII complexes to elucidate the geometry of the Mn4 cluster and the redox-active tyrosine, YZ, in the S2YZ• intermediate state of PSII. The structural model from these studies indicates proton-coupled electron-transfer between YZ and a water ligand to the Mn4 cluster. We are developing pulsed X-band (9 GHz) and high-frequency D-band (130 GHz) electron paramagnetic resonance (EPR) and electron-nuclear double resonance (ENDOR) methods to disentangle the individual steps of photo-induced PCET that leads to the formation of the redox-active tyrosyl radicals, YD• and YZ•, in PSII. We provide direct ‘snapshots’ of functional PCET intermediates and, for the first time, make it possible to detail the mechanism of PCET in photosystem II.

*This research is supported by U. S. Department of Energy, Basic Energy Sciences, Solar Energy Utilization Program (DE-FG02-0ER06-15).