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 tran sducing membranes has been calculated in the context of a three phase model for the membrane. In this model, the membrane contains three die lectric layers; (i) a 40-angstrom hydrophobic membrane bilayer, with d ielectric constant epsilon(m) = 3-4, (ii) 10-20-angstrom interfacial l ayers of intermediate polarity, epsilon(in) = 12-20, that consist of l ipid polar head groups and peripheral protein segments, and (iii) an e xternal infinite water medium, epsilon(w) = 80. The unusually positive midpoint potential, E(m) = +0.4 V, of the ''high potential'' cytochro me b-559 of oxygenic photosynthetic membranes, a previously enigmatic property of this cytochrome, can be explained by (i) the position of t he heme in the positive dipole potential region near the NH2 termini o f the two parallel helices that provide its histidine ligands, and (ii ) the loss of solvation energy of the heme ion due to the low dielectr ic 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 t o undergo a large -DELTAE(m) shift upon exposure of thylakoid membrane s to proteases or damaging treatments is explained by disruption of th e intermediate polarity (epsilon(in)) surface dielectric layer and the resulting contact of the heme with the external water medium. Applica tion 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 i n the low dielectric (epsilon(m)) membrane bilayer, results in E(m) va lues of hemes b(n) and b(p) that are, respectively, somewhat too negat ive (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 t he 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 envir onments, with that of heme b(p) being more polar.