Light-generated nuclear quantum beats: a signature of photosynthesis.

Abstract

Light-induced radical pairs in deuterated and deuterated plus 15N-substituted Synechococcus lividus cyanobacteria have been studied by transient EPR following pulsed laser excitation. Nuclear quantum beats are observed in the transverse electron magnetization at lower temperatures. Model calculations for the time profiles, evaluated at the high-field emissive maximum of the spectrum, indicate assignment of these coherences to nitrogen nuclei in the primary donor. Thorough investigation of the nuclear modulation patterns can provide detailed information on the electronic structure of the primary donor, providing insight into the mechanism of the primary events of plant photosynthesis. THEORYIn this section we briefly summarize a model for transient EPR of spin-correlated radical pairs and define the model parameters (16, 21-23). Specifically, we consider a sudden lightinduced generation of the radical pair with a spatially fixed geometry. Particular emphasis is given to the nuclear spin interactions, essential for the modeling of nuclear quantum beats.The total spin Hamiltonian, H(fl, t), depends on the orientation, Q, of the radical pair and can be divided into seven parts:H(fQ, t) = Hz(fQ) + HR(fl, t) + HEX + HD(Q)Spin-correlated radical pairs (1-7) are generated as short-lived intermediates in the primary energy conversion steps of natural photosynthesis (1,(5)(6)(7)(8)(9)(10)(11)(12)(13)(14). If the initial configuration of the radical pair is not an eigenstate of the corresponding spin Hamiltonian, the radical pair starts out in a coherent superposition of spin states (15)(16)(17)(18)(19), which can manifest itself as quantum beats in an EPR experiment with adequate time resolution (20)(21)(22)(23)(24). In the following we report transient EPR studies of light-induced radical pairs in plant photosystem I (PSI) with particular reference to nuclear spin coherences generated by a laser pulse. The primary electron transfer process in PSI involves the primary chlorophyll donor P700 and a series of protein-bound acceptors, Ao, A1, Fx, FA, and FB (25). Although the PSI reaction center has been crystallized, its x-ray structure is not known with great detail (26). Yet there is substantial evidence that two chlorophyll molecules, the special pair (27), form the primary donor (26, 28). Furthermore, current evidence suggests that Ao is a chlorophyll species and Fx, FA, and FB are iron-sulfur (FeS) centers. A1 has been identified as vitamin K1 (29). Thus, existing information points to the following chain of electron transfer steps, initiated by photoexcitation of the donor P700 (25, 29):A light-induced EPR signal with characteristic e/a/e polarization (e = emissive, a = absorptive) was observed in PSI a number of years ago (30,31). Yet the identity of this signal remained unclear. Recent work proves a direct assignment of the polarized spectrum to the secondary radical pair, P4o0A-(29, 32). Here we report observation of nuclear quantum beats for P7OAj in deuterated and deuterated plus 15N-substituted Synechococ...

Electron Transfer in Cyanobacterial Photosystem I

“…This shift is very well reproduced in numerical simulations (Fig. 6, bottom) of the P 700 ϩ A 1 Ϫ spectrum based on the spin-correlated radical pair model (23,26) in which the signal decay is assumed to be negligibly slow. Thus, it is clear that P 700 ϩ A 1 Ϫ dominates the early spectra.…”

Time-Resolved High-Frequency and Multifrequency EPR Studies of Spin-Correlated Radical Pairs in Photosynthetic Reaction Center Proteins

“…In addition, there are coherences between the eigenstates of the radical pair. Analysis reveals that zero quantum electron (Salikhov et at., 1990;Bittl and Kothe, 1991;Kothe et at., 1998;Zwanenburg and Hore, 1993;Kothe et at., 1994a;Kothe et at., 1994b;Bittl et at., 1994;Kiefer et at., 1999;Link et at., 2001;Heinen et at., 2002) and single quantum nuclear coherences (Kothe et at., 1998;Weber et at., 1995;Weber et at., 1997;Jeschke, 1997) are involved.…”

The quantum mitochondrion and optimal health

“…In essence, the energy in light can be harvested very efficiently and transferred using wavelike resonance. There is thus a ‘goldilocks zone’ to optimize efficiency; in effect, just the right amount of ‘noise’ can result in enhanced ‘coherence’ and ‘tunnelling’ due to stimulating particular vibrational modes in proteins–so called exciton-vibrational coupling (vibronic coupling) [41–44]. For example, tubulin contains chromophoric aromatics molecules such as tryptophan, and thus may play a role in coherent energy transfer; key in this maybe their free pi electrons [45,46].…”