S 3 State of the O 2 ‐ Evolving Complex of Photosystem II : Insights from 2 QM / MM , EXAFS , and Femtosecond X ‐ ray Di ff raction

19 P II (PSII) is a protein−pigment complex found 20 in the thylakoid membranes of the higher plants and 21 internal membranes of cyanobacteria. During the light period of 22 photosynthesis, PSII performs water oxidation with oxygen 23 evolution. The reaction is triggered by the photochemical 24 oxidation of the chlorophyll a species P680 that induces 25 electron−hole separation at the reaction center. The electron 26 hole is transferred from P680 to the redox-active tyrosine, YZ, 27 which in turn oxidizes the CaMn4O5 cluster of the oxygen28 evolving complex (OEC). The high efficiency and low 29 overpotentials make the OEC a prototype for development 30 of artificial water-oxidation catalysts. However, the structural 31 changes of the OEC responsible for efficiency and functionality, 32 along the catalytic cycle, have yet to be established at the 33 molecular level. 34 In each turn of the cycle, the OEC evolves through five 35 “storage” states, Sn (n = 0−4), with S0 and S4 being the most 36 reduced and oxidized forms, respectively. After the S4 state is 37 formed, O2 is spontaneously released and the S0 state is 38 restored, completing the catalytic cycle. Structural models for 39 the S0−S2 states have been found to be consistent with 40 femtosecond X-ray diffraction (XRD) and high-resolution 41 extended X-ray absorption fine structure (EXAFS) data. 42 However, the structure of the OEC cluster in the S3 state 43 remains controversial. 44 W-Band electron paramagnetic resonance (EPR) spectros45 copy has determined that the OEC in the S3 state has Mn(IV) 46 centers with octahedral environments. It is established that 47 the S2 → S3 conversion involves binding of a water molecule 48 (Wx) to the OEC, although the coordination site remains 49 uncertain. Ammonia binding to the S2 state 16−20 provided 50 valuable insights because water and ammonia are electronic and 51 structural analogues. On the basis of EPR and FTIR