Monomeric Spin Density Distribution in the Primary Donor of Photosystem I as Determined by Electron Magnetic Resonance:  Functional and Thermodynamic Implications

Abstract

The primary electron donor (P700) in Photosystem I (PSI) has been shown to be a dimeric chlorophyll a species. Electron magnetic resonance studies of the cation radical have clearly established that the unpaired electron is delocalized asymmetrically over this dimer; however, the extent to which this asymmetry exists remains ambiguous. Comprehensive electron nuclear double resonance (ENDOR) and electron spin−echo envelope modulation (ESEEM) experiments combined with isotopic substitution and numerical simulations have been used to determine the electronic structure of P700 + . This approach utilizes the strengths of each spectroscopy to elucidate the electron nuclear hyperfine and nuclear quadrupole coupling constants for the nitrogen nuclei in P700 + . These assignments are then confirmed by performing numerical simulations of the ESEEM data. Further confirmation of these values is obtained by performing the spin−echo experiments at multiple microwave frequencies. The same set of hyperfine and quadrupole coupling constants is used to simulate all of the ESEEM data for P700 + containing either natural abundance 14N or isotopically enriched with 15N. These simulations indicate that the unpaired spin is localized over only one of the chlorophylls that make up the special pair. The ramifications of this monomeric spin density on the function and thermodynamics of electron transfer in PSI are discussed.

Redox Potential of Quinones in Both Electron Transfer Branches of Photosystem I

“…This model is in agreement with ENDOR and ESEEM studies from which a largely asymmetric spin density distribution was de-duced (30 -34). In a more recent combination of ENDOR and ESEEM experiments (35) it was found that the spin density distribution is completely localized on P700 B . Measurements on P700 where the axial ligands of both Chl monomers in the P700 dimer were mutated from histidine to Gln or Ser for P700 A and to Gln, Gly, Asn, or Cys for P700 B demonstrated that the replacement of the axial ligand on the B-branch had a much stronger impact on the redox potential and the spin density distribution of P700 (36).…”

Exploring hyperfine interactions in spin-correlated radical pairs from photosynthetic proteins: High-frequency ENDOR and quantum beat oscillations

“…Previous studies, based on 15N ENDOR and electron spin echo envelope modulation (ESEEM) experiments, favor a dimeric electronic structure [53]. More recent ESEEM and ENDOR results, obtained in combination with specific isotope labelling, suggest a monomeric character for P7+oo [54].…”

Structural organization in photosynthetic proteins as studied by high-field EPR of spin-correlated radical pair states

“…Precise knowledge of these hyperfine interactions may help in elucidating the electronic structure of P C 700 , which is still the subject of numerous discussions. 44,45 …”