Electron spin polarization of photosynthetic reactants

Abstract

Photosynthesis is the conversion of the quantum energy of light into the chemical energy of complex organic molecules and organized cellular structures in plants and in some bacteria. The processes of photosynthesis span the time domain of subpicoseconds to the millennia of slow-growing trees, its study brings together such diverse disciplines as photophysics, biochemistry, botany and ecology. In the last few decades tremendous progress has been made in understanding the multivarious chemical reactions that ultimately lead to the fixation of carbon dioxide into organic substance, yet the basic mechanism underlying the conversion of photon energy into chemical energy still remains very much an enigma. These so-called primary reactions which transduce the excitation energy of excited chlorophyll pigments into the potential energy of stabilized, separated charges on electron donor and electron acceptor molecules have been studied with a variety of physical techniques, among which fast optical spectroscopy and electron paramagnetic resonance (EPR) are prominent. This review will highlight one intriguing aspect of EPR, namely that of electron spin polarization (ESP).† It will be shown that ESP of photosynthetic primary reactants offers a unique tool to gain insight in the electrostatic and magnetic interactions that make photosynthesis work. Moreover, it will become apparent that ESP in photosynthesis has several unique traits not (yet) found in ESP of photochemical reactions in vitro. As such, it may serve as a paradigma of ESP phenomena and will present an absorbing spectacle also for EPR spectroscopists outside photosynthesis.

Primary photochemistry of reaction centers from the photosynthetic purple bacteria

“…Since the time the first reaction center was isolated from the purple bacterium Rhodobacter sphaeroides [122] (formerly Rhodopseudomonas sphaeroides [65]), an enormous literature has grown on the properties of bacterial reaction centers (see general reviews [56,106,112,114]). This review will focus on the primary charge separation process in reaction centers isolated from the purple photosynthetic bacteria.…”

Nanosecond-Flash 15N Photo-CIDNP MAS NMR on Reaction Centers of Rhodobacter sphaeroides R26

“…The radical pair is born in a pure electronic singlet state S 0 , which evolves coherently into a triplet state T 0 , while the other two triplet states (T ?1 and T -1 ) are not populated at high magnetic fields. This high electron polarization delocalized in the S 0 -T 0 manifold is detected as photochemically induced dynamic electron polarization [17,18]. In this context, electron polarization of the radical pair corresponds to selective population of the two noneigenstates having the magnetic quantum number m = 0 and being in the S 0 -T 0 manifold.…”

Magnetic Interactions Between Photosynthetic Reactants

“…Low temperature polarized signals of PS I of orientated and unorientated material were observed by a number of authors (reviewed in Hoff, 1984). The ESP spectrum of unorientated PSI particles, which is very much like the low temperature ESP signal of bacteria, was simulated by Gast (1982;Gast et al, 1983) following the suggestions of Pedersen (1979) on ESP in a multiple acceptor system.…”

“…As has been pointed out above, this is probably not a good approximation for the distances of the radicals encountered in the RC. Previous attempts to include in lineshape simulations of polarized signals an axial dipolar interaction were not satisfactory (McCracken, 1983;McCracken and Sauer, 1983;Hoff, 1984) but recently Hore et al (1986) presented a transparent treatment of this problem. They showed that for random samples and the type of radicals found in the RC (D', A;, A;) D plays only a role in the transfer of polarization from A; to A;, because only A, has a significantly anisotropic g-term.…”

“…That anisotropic (dipolar) interactions play a role was clearly indicated by the work of McCracken et al (1982) who established that orientated PS I particles at cryogenic temperatures exhibited an orientation dependence of the ESP pattern that could not be explained solely by g-anisotropy of (one of) the acceptors as earlier assumed by Friesner et al (1979). An attempt to explain the orientation dependence by a dipolar interaction was unsatisfactory (McCracken, 1983;McCracken and Sauer, 1983;Hoff, 1984). A recent effort was undertaken by P. J. Hore (unpublished results) who tried to simulate the well-resolved Q-band (35 GHz) ESP spectrum at 6 K of deuterated algae from Thurnauer and Gast (1985) following the method of Hore et al (1986).…”