Binding site influence on the electronic structure and electron paramagnetic resonance properties of the phyllosemiquinone free radical of photosystem I.

Electronic structure calculations are performed on models of the phyllosemiquinone (PhSQ) free radical in the A(1A) and A(1B) sites of photo system I. Partial geometry optimization of each site is performed, and from the resultant geometry spin densities and hyperfine couplings are calculated. We exploit the ONIOM methodology to progressively build up a model of the A(1A) site and monitor the effect on the spin density distribution of the PhSQ and its hyperfine couplings. For the A(1A) site, we show that while the O1 atom of the PhSQ is not involved in direct hydrogen bonding, the (17)O anisotropic hyperfine coupling for this position is sensitive to interactions with neighboring groups, especially Trp A697 and Phe A689. The results obtained are in agreement with experimental determinations which indicate small differences in (17)O hyperfine couplings for both oxygen atoms. Good agreement between calculated and experimental (1)H and (13)C hyperfine couplings is also found. In addition, we find that a significant (14)N isotropic coupling of 1.4 MHz is calculated for the peptide NH group of Leu A722. The (14)N isotropic hyperfine coupling obtained for the indole nitrogen atom of Trp A697 is calculated to be zero in disagreement with a previous experimental assignment. The spin density distribution of the PhSQ in the A(1B) site is calculated to be very similar to that in the A(1A) site. The presence of just one relatively weak hydrogen bond to the photo system I quinone is proposed to contribute substantially to its relatively low redox potential when compared with the more strongly hydrogen bonded quinone acceptors present in type II reaction centers.