THE REDOX PROPERTIES OF CYTOCHROMES-B IMPOSED BY THE MEMBRANE ELECTROSTATIC ENVIRONMENT

The effect of the dipole potential field of extended membrane spanning alpha-helices on the redox potentials of b cytochromes in energy transducing membranes has been calculated in the context of a three phase model for the membrane. In this model, the membrane contains three dielectric layers; (i) a 40-angstrom hydrophobic membrane bilayer, with dielectric constant epsilon(m) = 3-4, (ii) 10-20-angstrom interfacial layers of intermediate polarity, epsilon(in) = 12-20, that consist of lipid polar head groups and peripheral protein segments, and (iii) an external infinite water medium, epsilon(w) = 80. The unusually positive midpoint potential, E(m) = +0.4 V, of the ''high potential'' cytochrome b-559 of oxygenic photosynthetic membranes, a previously enigmatic property of this cytochrome, can be explained by (i) the position of the heme in the positive dipole potential region near the NH2 termini of the two parallel helices that provide its histidine ligands, and (ii) the loss of solvation energy of the heme ion due to the low dielectric constant of its surroundings, leading to an estimate of +0.31 to +0.37 V for the cytochrome E(m). The known tendency of this cytochrome to undergo a large -DELTAE(m) shift upon exposure of thylakoid membranes to proteases or damaging treatments is explained by disruption of the intermediate polarity (epsilon(in)) surface dielectric layer and the resulting contact of the heme with the external water medium. Application of this model to the two hemes (b(n) and b(p)) of cytochrome b of the cytochrome bc1 complex, with the two hemes placed symmetrically in the low dielectric (epsilon(m)) membrane bilayer, results in E(m) values of hemes b(n) and b(p) that are, respectively, somewhat too negative (approximately -0.1 V), and much too positive (approximately +0.3 V), leading to a potential difference, E(m)(b(p)) - E(m)(b(n)), with the wrong sign and magnitude, + 0.25 V instead of -0.10 to -0.15 V. The heme potentials can only be approximately reconciled with experiment, if it is assumed that the two hemes are in different dielectric environments, with that of heme b(p) being more polar.