Exploring hyperfine interactions in spin-correlated radical pairs from photosynthetic proteins: High-frequency ENDOR and quantum beat oscillations

Abstract

Electron paramagnetic resonance (EPR) and related spectroscopic toots remain among the most important probes of structure and function of natural photosynthetic systems. Indeed, the challenging questions in the study of photosynthesis have to a great extent dictated the directions taken in the development of EPR and associated spectroscopies. In this overview we demonstrate, with recent examples from our laboratories, the potential of high-frequency and time-resolved EPR spectroscopy to reveal unique inforrnation about electron transfer processes and the structure of photosynthetic systems. A common feature of these experiments is that they probe hyperfine interactions of the spincorrelated radical pair. Thus, [he analysis of the results requires consideration of three interacting spins: two correlated eteetron spins with one nuclear spin. The results illustrate the importance of resolving nuclear hyperfŸ structure for obtaining details of structure-function relationships in photosynthetic electron transfer.

Exploring the Electron Transfer Pathways in Photosystem I by High-Time-Resolution Electron Paramagnetic Resonance: Observation of the B-Side Radical Pair P700+A1B– in Whole Cells of the Deuterated Green Alga Chlamydomonas reinhardtii at Cryogenic Temperatures

“…Hyperfine interactions in the radical pair were approximated by considering five equivalent 14 N nuclei ( a N = 0.060 mT) in P 700 + and four equivalent 2 H nuclei ( a D = 0.055 mT) in A 1 – . The resultant second moments are in agreement with published hyperfine parameters for P 700 + , and A 1 – . , Inhomogeneous broadening was considered by convolution with a Gaussian. The homogeneous spin–spin relaxation time has been estimated from the decay of the out-of-phase electron spin echo of P 700 + A 1B – in the nondeuterated PsaA-M684H mutant …”

“…The fixed magnetic parameters, used in the computer fit of the two-dimensional EPR experiment, are summarized elsewhere (see the Supporting Information, Table S1). The g tensor components − and the parameters of the hyperfine interaction − are the same as those employed in the case of the deuterated mutant. However, as we consider both radical pair intermediates P 700 + A 1A – and P 700 + A 1B – , two sets of spin–spin coupling parameters, D A , J A and D B , J B , are now required in the analysis …”

“…We therefore conclude that g tensor orientation I is correct. This conclusion confirms the previous assignment in time-resolved high-frequency and multifrequency EPR studies on deuterated and 15 N-substituted cyanobacteria. − ,, …”

“…This conclusion confirms the previous assignment in time-resolved high-frequency and multifrequency EPR studies on deuterated and 15 N-substituted cyanobacteria. [49][50][51]53,58 Using g tensor orientation I, we obtain the three-dimensional structure of P 700 + A 1A − in the photosynthetic membrane, as shown in Figure 8b. The structural model is based on the assumption that the major part of the unpaired electron spin in P 700 + is on the chlorophyll a species coordinated by the PsaB protein subunit.…”