Energetics and Mechanism of Primary Charge Separation in Bacterial Photosynthesis. A Comparative Study on Reaction Centers of Rhodobacter sphaeroides and Chloroflexus aurantiacus

Abstract

The high efficiency of charge separation in photosynthetic reaction centers arises from the interplay of energetics, electronic couplings, and reorganization energies relevant for the fast charge separation and slow recombination processes. All these parameters can be determined unambiguously only from magnetic-fielddependent measurements of the recombination dynamics of the intermediate radical pair P + H A -and the lifetime of the recombination product 3 P*. Results obtained on Q A -depleted reaction centers of Chloroflexus aurantiacus are compared with those for the well-characterized reaction centers of Rhodobacter sphaeroides. In contrast to Rb. sphaeroides, the magnetic field dependence of the triplet yield in Cf. aurantiacus has a pronounced resonance structure, allowing the direct determination of the exchange interaction of P + H A -, J ) 21 G. The recombination rate k T is slightly larger for Cf. aurantiacus and shows a different temperature dependence. All these differences can be explained by the free energy of P + H A -, found to be larger by 0.04 eV in Cf. aurantiacus compared to Rb. sphaeroides. We propose that this different energy arises largely from the different amino acid at position L104, which is glutamic acid in the case of Rb. sphaeroides and glutamine in the case of Cf. aurantiacus. The electronic couplings and the reorganization energies, on the other hand, are very similar in both reaction centers. Implications for the mechanism of primary charge separation are discussed. The pronounced nonexponential kinetics of charge separation in Cf. aurantiacus is explained by the energetic inhomogeneity of the primary radical pair P + B A -.

Temperature Dependence of Electron Transfer to the M-Side Bacteriopheophytin in Rhodobacter capsulatus Reaction Centers

“…There P + H L -decays with a lifetime of ∼10 ns at 295 K and ∼20 ns at 77 K, although the precise lifetime as well as the fraction of charge recombination that leads to the ground state versus 3 P depends on conditions. 26,71,[113][114][115][116] Overall our results here indicate that the temperature dependence of P + H M -decay is similar to that of P + H L -in showing a small decrease between 295 and 77 K.…”

“…[55][56][57] Additionally, calculations generally place the P + B -state higher in free energy than the P + H -state on both L and M branches by 0.15-0.25 eV, consistent with the difference in redox potentials of bacteriochlorophyll and bacteriopheophytin in vitro. [58][59][60][61] Calculations and experiments have provided estimates or bracketed ranges for the free energies of the charge-separated states in the wild-type RC: P + B L -0.05-0.1 eV below P*; 29,50,51,[62][63][64][65][66][67][68][69][70] P + H L -∼0.25 eV below P* when relaxed; [71][72][73][74][75] P + B M -0.1-0.2 eV above P* and P + H M -below P* by no more than ∼0.15 eV and probably within 0.1 eV. [50][51][52][76][77][78][79] Systematic efforts to manipulate the free energy differences of the L-and M-branch charge-separated states by site-directed mutagenesis of key amino acids, including those near B M and B L , have led to mutant RCs in which electron transfer to the M branch competes effectively with charge separation to the L branch, yielding P + H M -(reviewed in ref 80).…”

Energetics of Bacterial Photosynthesis

“…5,6 The resulting bestfit reorganization energies for primary charge separation have evolved over the years from very low magnitudes ≈0.06-0.1 eV in earlier studies [7][8][9] to 0.19 eV later on, 10 and to a noticeably larger magnitude of 0.35 eV in more recent fits. 11 The situation with the available database of electron-transfer reorganization parameters has improved in the recent decade with the widespread of numerical simulations of biological systems.…”

“…State 3 can recombine to the original ground state P on the nanosecond time scale. 10 An additional recombination channel of state 3 is to a photoexcited triplet of the special pair, 3 P* (state 4). The energy gaps between P and P* and between P and 3 P* are known from experimental spectroscopic measurements, 10 while the free energy gaps between other states shown in Figure 2 are from our calculations described below.…”

Asymmetric Electron Transfer in Reaction Centers of Purple Bacteria Strongly Depends on Different Electron Matrix Elements in the Active and Inactive Branches

“…Recent measurements by Volk et al 46 and the calculation of Sim and Makri 47 suggested that ∆G WT for the first step of ET in the wild type Rb. sphaeroides is -0.05 eV.…”