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

Abstract

The photosynthetic reaction center (RC) from Rhodopseudomonas viridis contains four cytochrome c hemes. They establish the initial part of the electron transfer (ET) chain through the RC. Despite their chemical identity, their midpoint potentials cover an interval of 440 mV. The individual heme midpoint potentials determine the ET kinetics and are therefore tuned by specific interactions with the protein environment. Here, we use an electrostatic approach based on the solution of the linearized Poisson-Boltzmann equation to evaluate the determinants of individual heme redox potentials. Our calculated redox potentials agree within 25 meV with the experimentally measured values. The heme redox potentials are mainly governed by solvent accessibility of the hemes and propionic acids, by neutralization of the negative charges at the propionates through either protonation or formation of salt bridges, by interactions with other hemes, and to a lesser extent, with other titratable protein side chains. In contrast to earlier computations on this system, we used quantum chemically derived atomic charges, considered an equilibrium-distributed protonation pattern, and accounted for interdependencies of site-site interactions. We provide values for the working potentials of all hemes as a function of the solution redox potential, which are crucial for calculations of ET rates. We identify residues whose site-directed mutation might significantly influence ET processes in the cytochrome c part of the RC. Redox potentials measured on a previously generated mutant could be reproduced by calculations based on a model structure of the mutant generated from the wild type RC.

Heme Attachment Motif Mobility Tunes CytochromecRedox Potential

“…For example, a possible explanation is the observed changes in E m could arise from electrostatic perturbations caused by the mutations. Specifically, the electrostatic potential at the heme iron can be influenced by the charges of surrounding residues (54,55). Here, for example, in Ht-M13V/ K22M, the charged Lys side-chain is replaced by a neutral side-chain, Met.…”

Tuning electron transfer by ester‐group of chlorophylls in bacterial photosynthetic reaction center

“…As a general and uniform strategy, all the crystal waters are removed in our computations [3,4,17,[19][20][21] because of the lack of experimental information for hydrogen atom positions. Cavities resulting after the removal of crystal water are uniformly filled with solvent dielectric of e = 80.…”

“…The protonation patterns were sampled by a Monte Carlo (MC) method with our own program Karlsberg [16]. The dielectric constant was set to e P = 4 inside the protein and e W = 80 for water as done in previous computations for bRC [3,4,17], PSI [8] and PSII [9]. From the calculated redox probability of the redox-active group, the E m is evaluated using the Nernst equation.…”

Electrostatic Environment of Hemes in Proteins: pKas of Hydroxyl Ligands

“…For example, sixcoordinate bis-His-hemes have E m s ranging from -410 to +360 mV with the redox differences being predominately due to the intraprotein electrostatic environment (1,(20)(21)(22). In these proteins the loss of solvation energy (15,23,24), interactions with the protein backbone and with other residues (15,(20)(21)(22)25), and local conformation changes on ionization changes (20, 26) determine the thermodynamic equilibrium measured by pK a s and E m s.Theoretical studies have analyzed hemes in different systems using a number of techniques. The large span of E m s in cytochromes has been subject to analysis by Protein Dipole Langevin Dipole (PDLD) (27,28), continuum electrostatics (CE) 1 (20,21,29,30), and other techniques (31-37).…”