Electronic Structure of the Quinone Radical Anion A1•−of Photosystem I Investigated by Advanced Pulse EPR and ENDOR Techniques

Abstract

Vitamin K1 (VK1) is an important cofactor of the electron-transfer chain in photosystem I (PS I), referred to as A1. The special properties of this quinone result from its unique interaction(s) with the protein surrounding. In particular, a single H-bond to neutral A1 was identified previously in the X-ray crystal structure of PS I. During light-induced electron transfer in PS I, A1 is transiently reduced to the radical anion A1*-. In this work, we characterized the electron spin density distribution of A1*- with the aim of understanding the influence of the protein surrounding on it. We studied the light-induced spin-polarized radical pair P700*+A1*- and the photoaccumulated radical anion A1*-, using advanced pulse EPR, ENDOR, and TRIPLE techniques at Q-band (34 GHz). Exchange with fully deuterated quinone in the A1 binding site allowed differentiation between proton hyperfine couplings from the quinone and from the protein surrounding. In addition, DFT calculations on a model of the A1 site were performed and provided proton hyperfine couplings that were in close agreement with the ones determined experimentally. This combined approach allowed the assignment of proton hyperfine coupling tensors to molecular positions, thereby yielding a picture of the spin density distribution in A1*-. Comparison with VK1*- in organic solvents (Epel et al. J. Phys. Chem. B 2006, 110, 11549.) leads to the conclusion that the single H-bond present in both the radical pair P700*+A1*- and the photoaccumulated radical anion A1*- is, indeed, the crucial factor that governs the electronic structure of A1*-.