The function of photosystem I. Quantum chemical insight into the role of tryptophan-quinone interactions

Quantum chemical calculations have provided evidence for the role of tryptophan residues in the electron transfer process of photosystem I (PS-I). The interaction of Trp with quinone acceptors and their radical anions in the A(1) site of PS-I has been modeled by various indole-quinone and indole-semiquinone complexes. MP2 optimizations show that, while neutral quinones and an indole molecule prefer a pi-stacked arrangement, semiquinone radical anions prefer a T-stacked conformation with significant N-H...pi hydrogen bonding interactions. Comparison of density functional calculations of electronic g-tensors with electron paramagnetic resonance data strongly suggests that hydrogen-bonded T-shaped arrangements occur upon reduction of quinone acceptors without an extended side chain (e.g., duroquinone or naphthoquinone), when reconstituted into the phylloquinone-depleted A(1) site of PS-I. In contrast, for the native phylloquinone (vitamin K(1), Q(K)), reorientation of the semiquinone radical anion is prevented by side chain-protein interactions. For a fixed pi-stacked arrangement, the extent of the intermolecular interaction is reduced upon one-electron reduction. This corresponds to a lowering of the redox potential of the P(700)(+)*Q(K)(-)* radical pair, due to interactions of Q(K) with a tryptophan. Together with the comparably weak hydrogen bonding in PS-I, the proposed model explains the very negative redox potential of the A(1) site, needed for forward electron transfer. T-stacking hydrogen bonds to semiquinones may also have to be considered in many other electron transfer processes in living organisms.