Structural, dynamic, and energetic aspects of long-range electron transfer in photosynthetic reaction centers

Abstract

Intramolecular electron transfer within proteins plays an essential role in biological energy transduction. Electron donor and acceptor cofactors are bound in the protein matrix at specific locations, and protein-cofactor interactions as well as protein conformational changes can markedly influence the electron transfer rates. To assess these effects, we have investigated charge recombination from the primary quinone acceptor to the special pair bacteriochlorophyll dimer in wild-type reaction centers of Rhodobacter sphaeroides and four mutants with widely modified free energy gaps. After light-induced charge separation, the recombination kinetics were measured in the light-and dark-adapted forms of the protein from 10 to 300 K. The data were analyzed by using the spin-boson model, which allowed us to self-consistently determine the electronic coupling energy, the distribution of energy gaps, the spectral density of phonons, and the reorganization energy. The analysis revealed slow changes of the energy gap after charge separation. Interesting correlations of the control parameters governing electron transfer were found and related to structural and dynamic properties of the protein.T he bioenergetic pathways of living systems involve a multitude of electron transfer (ET) reactions. Within large protein-cofactor complexes, electrons tunnel between donor and acceptor sites over substantial distances (5-30 Å). In the weak coupling regime, the ET rate coefficient is obtained from perturbation theory as (1-4)where ប and V denote Planck's constant divided by 2 and the electronic coupling matrix element, respectively. The thermally averaged Franck-Condon factor, FC, represents the probability of forming a resonant complex between donor and acceptor. This quantity can be calculated in various ways, based on classical, semiclassical, or quantum-mechanical theories (4). In the celebrated classical Marcus theory (1),with Boltzmann's constant, k B , and absolute temperature, T. The free energy difference between the reactant and product states, , the nuclear reorganization energy, , and the electronic coupling, V, are the three system parameters that govern the ET rate. From these quantities, only the driving force, , is directly accessible to measurement, e.g., by delayed fluorescence (5), redox titration (6), or voltammetry (7). The other two parameters can be determined only indirectly from kinetic data and are difficult to disentangle in practice. The intrinsic flexibility of proteins adds an interesting dynamic aspect to the ET reaction. Proteins fluctuate thermally among many different conformations and respond to charge rearrangements with structural relaxations on time scales ranging from (below) picoseconds to (at least) seconds. These motions can strongly affect the ET parameters and hence the ET rates (8-10). For studying biological ET, the photosynthetic reaction center (RC) of the purple bacterium Rhodobacter sphaeroides is a superb model system. This membrane-spanning, 120-kDa, protein-pigment complex consists...

Thermoluminescence: theory

“…As a rule, the recombination reaction in PS II or in purple bacterial RCs is not adequately described as a simple monoexponential process. For previous literature on this subject, see for PS II: Bennoun (1970); Lavorel et al (1982); Lavergne and Rappaport (1998);De Wijn et al (2001);De Wijn and Van Gorkom (2002); and Rappaport et al (2005) and for bacterial RCs, see Sebban and Wraight (1989); Schoepp et al (1992); McMahon et al (1998); Kriegl and Nienhaus (2004). Generally, the recombination kinetics can be fitted satisfactorily as a sum of two exponentials; however, this does not warrant a true bipartite heterogeneity and may very well be due to a more broadly distributed kinetic heterogeneity.…”

The manganese complex of photosystem II in its reaction cycle—Basic framework and possible realization at the atomic level

“…This discrepancy is not easily explainable by rate-limitation by a coupled proton-tunneling process because the H/D isotope effect on the rate is small (≤1.4). Protein dynamics involving diffusive motions between numerous conformational substates [240][241][242][243] or specific, 'conducive' protein motions [244,245] may facilitate a significant reorganization of the Mn complex -including proton movements -at low activation enthalpy. We note that such an influence of the protein dynamics could render quantum chemical calculations on the energy profile along putative reaction paths problematic.…”

Phonon Guided Biology. Architecture of Life and Conscious Perception Are Mediated by Toroidal Coupling of Phonon, Photon and Electron Information Fluxes at Discrete Eigenfrequencies.

“…We argue therefore that the induced storage of energy is mediated by toroidal phonon information flux, that imposes a spectrum of Chladni-type of geometric patterns in the cytoplasm. EM fields act as forcers to create phonon-driven non-linear information processing, since phonons conduct acoustic information along protein lattice networks at the speed of sound (Kriegl and Niehaus, 2004). The resulting coherent resonance structures subsequently interact with cell components and contributes to ordering of life processes such as the above second messenger function of Ca2+ ions.…”