Magnetic-field-induced orientation of photosynthetic reaction centers as revealed by time-resolved W-band EPR of spin-correlated radical pairs: development of a molecular model

Spin-correlated radical pairs are the short-lived intermediates of the primary energy conversion steps of photosynthesis. In this paper, we develop a comprehensive model for the spin-polarized electron paramagnetic resonance (EPR) spectra of these systems. Particular emphasis is given to a proper treatment of the alignment of the photosynthetic bacteria by the field of the EPR spectrometer. The model is employed to analyze time-resolved W-band (94 GHz) EPR spectra of the secondary radical pair P(700)(+)A(1)(-) in photosystern I formed by photoexcitation of the deuterated and N-15- substituted cyanobacterium Synechococcus lividus. Computer simulations of the angular-dependent EPR spectra of P(700)(+)A(1)(-) provide values for the order parameter of the cyanobacterial cells and for the orientation of the membrane normal in a molecular reference system. The order parameter from EPR compares favorably with corresponding data from electron microscopy obtained for the S. lividus cells under similar experimental conditions. It is shown that high-field EPR of a magnetically aligned sample in combination with the study of quantum beat oscillations represents a powerful structural tool for the short-lived radical pair intermediates of photosynthesis.