The vibrational spectrum of the secondary electron acceptor, A1, in photosystem I

Photosystem I (PSI) is a multisubunit protein complex which carries out light-induced, transmembrane charge separation in oxygenic photosynthesis. In PSI, the electron-transfer pathway consists of chlorophyll and phylloquinone molecules, as well as iron-sulfur clusters. There are two phylloquinone molecules, which are located in structurally symmetric positions in the reaction center. It has been proposed that both phylloquinone molecules are active as the A1 secondary electron acceptor in bidirectional electron-transfer reactions. The PSI A1 acceptors are of interest because they have the lowest reduction potential of any quinone found in nature. In this work using light-induced FT-IR spectroscopy, isotope-edited spectra are presented, which attribute vibrational bands to the carbonyl stretching vibrations of A1 and A1- and the quinoid ring stretching vibration of A1. Bands are assigned by comparison with hybrid Hartee-Fock density functional calculations, which predict vibrational frequencies, amplitudes, and isotope shifts for the phylloquinone singlet and radical anion states. The results are consistent with an environmental interaction increasing the frequency of the singlet CO vibration and decreasing the frequency of the anion radical CO vibration, relative to model compounds. This environmental interaction may be the asymmetric hydrogen bond to A1/A1-, electrostatic interactions with charged amino acid side chains, or a pi-pi interaction with the indole ring of a nearby tryptophan. Such differential effects on the structure of A1 and A1- may be associated with a destabilization of the anion radical. These studies give novel information concerning the effect of the protein matrix on the PSI electron-transfer cofactor.