Electronic Structure of the Primary Electron Donor in Photosystem I Studied by Multifrequency HYSCORE Spectroscopy at X- and Q-Band.

The primary electron donor of the photosystem I (I) is a heterodimer consisting of two chlorophyll molecules. A series of electron-transfer events immediately following the initial light excitation leads to a stabilization of the positive charge by its cation radical form, . The electronic structure of and, in particular, its asymmetry with respect to the two chlorophyll monomers is of fundamental interest and is not fully understood up to this date. Here, we apply multifrequency X- (9 GHz) and Q-band (35 GHz) hyperfine sublevel correlation (HYSCORE) spectroscopy to investigate the electron spin density distribution in the cation radical of I from a thermophilic cyanobacterium . Six N and two H distinct nuclei have been resolved in the HYSCORE spectra and parameters of the corresponding nuclear hyperfine and quadrupolar hyperfine interactions were obtained by combining the analysis of HYSCORE spectral features with direct numerical simulations. Based on a close similarity of the nuclear quadrupole tensor parameters, all of the resolved N nuclei were assigned to six out of total eight available pyrrole ring nitrogen atoms (i.e., four in each of the chlorophylls), providing direct evidence of spin density delocalization over the both monomers in the heterodimer. Using the obtained experimental values of the N electron-nuclear hyperfine interaction parameters, the upper limit of the electron spin density asymmetry parameter is estimated as = 7.7 ± 0.5, while a tentative assignment of N observed in the HYSCORE spectra yields = 3.1 ± 0.5.