Magnetic resonance of ultrafast chemical reactions

Abstract

Using e.s.e. (electron spin-echo), RYDMR (reaction-yield-detected magnetic resonance) and e.s.r. (electron spin resonance) in protein single crystals, we have investigated the cation, the triplet and the initial radical pair associated with the process of photoinduced charge separation in photosynthesis. The initial charge separation of bacterial photosynthesis occurs in a few picoseconds within in a reaction-centre protein containing eight electron-transfer components, namely four bacterial chlorophylls, two bacteriopheophytins and two quinones. Two bacteriochlorophylls, BChl₂, form the primary donor and one bacteriopheophytin serves as the primary acceptor. E.s.e. determination of the anisotropic ¹⁵N hyperfine interactions have shown that the primary donor cation resides symmetrically in two of the four BChls in the form of a special pair of bacterial chlorophylls, BChl⁺₂. In direct contrast, our e.s.r. studies on the triplet state of the primary donor in single crystals of reaction centres suggest that the triplet state resides asymmetrically in BChl₂, where the triplet is highly asymmetrical in R. viridis but is much more symmetrical (C₂) in R. sphaeroides. RYDMR studies of the initial radical pair formed indicate that the extra bacteriochlorophyll molecule, BChl_B, that is between the special pair donor cation and the primary acceptor bacteriopheophytin anion is not involved in a discrete electron-transfer step in bacterial reaction centres. By combining the results of our magnetic-resonance experiments with X-ray structural information, the following description emerges: (1) the ground-state, primary donor is a supermolecule dimer with approximately C₂ symmetry; (2) the bridging BChl_B molecule probably functions as a superexchange site for rapid transfer of electrons from the primary donor to the primary acceptor but with negligible back reaction; (3) the special pair, BChl₂, is lower in energy than the bridging molecule, BChl_B, such that the initial radical pair is formed via super-exchange between the distant (10 Å edge-to-edge) special pair BChl₂ and the bacteriopheophytin.