Energetics of Electron-Transfer and Protonation Reactions of the Quinones in the Photosynthetic Reaction Center of Rhodopseudomonas viridis

Abstract

The electron-transfer reactions involving the quinones in the bacterial photosynthetic reaction center (bRC) are coupled to a proton uptake by the bRC. In this study, we calculated the energies of the different states of the bRC occurring during these electron-transfer and protonation reactions by an electrostatic model. We considered the possibility that titratable groups of the bRC can change their protonation during these reactions. The protonation probabilities of titratable groups were obtained by a Monte Carlo calculation. In contrast to earlier studies by other groups, we used atomic partial charges derived from quantum-chemical calculations. Our calculated reaction energies are in agreement with experiments. We found that the proton uptake by the bRC is coupled more strongly to changes of the redox state of the quinones than to changes of their protonation state. Thus, the proton uptake by the bRC occurs predominantly before the protonation of QB. According to our computations, the reduction of QB* - to the doubly negative state QB2- is energetically even more unfavorable in the bRC than in solution. Therefore, we suggest that the second electron transfer from QA to QB occurs after QB has received its first proton. We found that the QA. -QB. - state is more populated at pH 7.5 than the QA. -QB.H state. The low population of the QA. -QB.H state may be the reason why the singly protonated QB could not be detected spectroscopically. Our calculations imply that the first protonation of QB. - is a prerequisite for the second electron transfer between QA and QB. Therefore, a pH dependence of the equilibrium between the states QA. -QB. - and QA. -QB. H can also explain the experimentally observed pH dependence of the rate for the second electron-transfer step. On the basis of our calculated reaction energies, we propose the following sequence for the electron-transfer and protonation reactions: (1) first electron transfer from QA to QB, (2) first protonation of QB (at the distal oxygen close to Ser L223), (3) second electron transfer from QA to QB, and (4) second protonation of QB (at the proximal oxygen close to His L190).

Mechanism of proton-coupled quinone reduction in Photosystem II

“…The preferential occurrence of the first protonation at O QB(distal) over O QB(proximal) is consistent with the Q B protonation mechanism in purple bacterial RCs (15,16,24).…”

Evidence for Delocalized Anticooperative Flash Induced Proton Binding as Revealed by Mutants at the M266His Iron Ligand in Bacterial Reaction Centers

“…Several laboratories have developed extensive PoissonBoltzmann calculations aimed at describing the electrostatic and protonation landscape in the RC (24,65,66,72,73). It appears, however, that these calculations predict lower interaction energies between the members of the acidic cluster than those required in the interpretative model that we propose.…”

Tuning Heme Redox Potentials in the Cytochrome c Subunit of Photosynthetic Reaction Centers

“…An ion exclusion layer of 2 Å and a solvent probe radius of 1.4 Å were used to define the volume of the protein. The membrane embedding of the M and L chain was not taken into account, because the cyt c unit is entirely in the aqueous phase where it should experience little influences form the membrane, as has been shown before (15,28). Because of the large dimensions of the protein, the electrostatic potential was calculated by a three step focusing procedure using a grid spacing of 2.5, 1, and 0.25 Å, respectively.…”

“…The program KARLSBERG was used for this task (28), which is freely available on our web server (agknapp.chemie.fu-berlin.de/karlsberg/). Oxidation probabilities were evaluated at pH 7 by varying the solution redox potential E sol (Equation 4) yielding the respective E1 ⁄2 potential.…”