What you get out of high-time resolution electron paramagnetic resonance: example from photosynthetic bacteria

Abstract

The primary energy conversion steps of natural photosynthesis proceed via light-induced radical ion pairs as short-lived intermediates. Time-resolved electron paramagnetic resonance (EPR) experiments of photosynthetic reaction centers monitor the key charge separated state between the oxidized primary electron donor and reduced quinone acceptor, e.g., P(+)(865)Q(-)(A) of purple photosynthetic bacteria. The time-resolved EPR spectra of P(+)(865)Q(-)(A) are indicative of a spin-correlated radical pair that is created from the excited singlet state of P(865) in an ultra-fast photochemical reaction. Importantly, the spin-correlated radical pair nature of the charge separated state is a common feature of all photosynthetic reaction centers, which gives rise to several interesting spin phenomena such as quantum oscillations, observed at short delay times after optical excitation. In this review, we describe details of the quantum oscillation phenomenon and present a complete analysis of the data obtained from the charge separated state of purple bacteria, P(+)(865)Q(-)(A). The analysis and simulation of the quantum oscillations yield the three-dimensional structure of P(+)(865)Q(-)(A) in the photosynthetic membrane on a nanosecond time scale after light-induced charge separation. Comparison with crystallographic data reveals that the position of Q(-)(A) is essentially the same as in the X-ray structure. However, the head group of Q(-)(A) has undergone a 60° rotation in the ring plane relative to its orientation in the crystal structure. The results are discussed within the framework of the previously suggested conformational gating mechanism for electron transfer from Q(-)(A) to the secondary quinone acceptor Q(B).

Charge Transfer Processes in OPV Materials as Revealed by EPR Spectroscopy

“…Therefore, EPR spectroscopy has extensively been used in the research of photosynthesis and molecular donor-acceptor systems where light-induced electron transfer processes and recombination reactions take place. [64][65][66][67][68][69][70][71] EPR at various frequencies allowed the spectral separation of distinct radicals as well as the determination of g-tensors and hyperfine tensors. Advanced pulsed methods provided insight into hyperfine interactions and relaxation phenomena.…”

“…EPR spectroscopy has extensively been used in the research of photochemical transformations as a valuable method for studying time-dependent charge and spin dynamics. [64][65][66][67][68][69][70][71]125] The time resolution of EPR is much lower than ultrafast optical techniques. The conventional X-band EPR operates at 9-10 GHz frequency with a typical time-response of 100s of ns (see Introduction).…”

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

“…Under these conditions, the model predicts the formation of electron spin oscillations whose frequency ω ZQ sensitively depends on the orientation Ω of the radical pair in the laboratory frame, x, y, z, with B 0 along the z axis. Generally, ω ZQ (Ω) can be written as 24,25,37,38 where D zz (Ω), g i zz (Ω), and a ij are the zz component of the dipolar coupling tensor, the zz component of the g tensor of radical i, and the isotropic hyperfine coupling between nucleus j and radical i. Inspection of eq 2 reveals that the frequency of the electron spin oscillations is determined by the spin−spin interactions of the radical pair and the difference in the Zeeman and hyperfine interactions of the constituent radicals.…”

“…The crucial parameter is the position of A 1A − (A 1B − ) in the photosynthetic membrane. 24,52 We assume that a shift of A 1A − (A 1B − ) relative to the position of A 1A (A 1B ) in the X-ray structure beyond the error limits of the Q-band study is unlikely to occur. 61 Using the quinone position as a selection criterion, one can eliminate seven of the eight degenerate geometries.…”

EPR Spectroscopy

“…Due to space limitations only a selected range of systems can be covered. Recent good reviews exist about EPR spectroscopic studies on photosynthesis [20][21][22] and metalloproteins [23][24][25][26]. Strongly physics-related application fields, such as quantum computing [27], electrically detected [28] and optically [29] detected EPR spectroscopy of dopants and defects in solids are left out.…”