X-ray Free Electron Laser Radiation Damage through the S-State Cycle of the Oxygen-Evolving Complex of Photosystem II

The oxygen-evolving complex (OEC) catalyzes water-splitting through a reaction mechanism that cycles the OEC through the "S-state" intermediates. Understanding structure/function relationsships of the S-states is crucial for elucidating the water-oxidation mechanism. Serial femtosecond X-ray crystallography has been used to obtain radiation damage-free structures. However, it remains to be established whether "diffraction-before-destruction" is actually accomplished or if significant changes are produced by the high-intensity X-ray pulses during the femtosecond scattering measurement. Here, we use ab initio molecular dynamics simulations to estimate the extent of structural changes induced on the femtosecond time scale. We found that the radiation damage is dependent on the bonding and charge of each atom in the OEC, in a manner that may provide lessons for XFEL studies of other metalloproteins. The maximum displacement of Mn and oxygen centers is 0.25 and 0.39 Å, respectively, during the 50 fs pulse, which is significantly smaller than the uncertainty given the 1.9 Å resolution of the current PSII crystal structures. However, these structural changes might be detectable when comparing isomorphous Fourier differences of electron density maps of the different S-states. One conclusion is that pulses shorter than 15 fs should be used to avoid significant radiation damage.