Coupling of electron and proton transport in photosynthetic membranes: molecular mechanism

Using the method of Modified Neglect of Diatomic Overlap (MNDO), the electronic structure of plastoquinol (PQH(2)) and plastoquinone (PQ) in neutral, singly (PQ(-)) and doubly (PQ(2-)) reduced states is studied. The conformational analysis performed on these molecules shows that in the lowest energy conformation, the angle between the first link of the tail backbone and the ring plane of neutral and singly reduced PQ and plastoquinol is nearly the same and differs by 15 degrees from that of doubly reduced PQ. Nevertheless, for all states of plastoquinone and for plastoquinol, the total energy changes by less than 0.2 eV when the studied angle is varied from 0 degrees to 180 degrees. As in Rhodobacter sphaeroides, the oxygen of the PQ ring is reported to form a hydrogen bond with a nitrogen in the ring of Histidine (His) L 190. The energy of the PQ-His complex was calculated for different redox states of PQ and for several values of the distance between the molecules (N-O distance from 0.2 to 0.5 nm). For every considered complexes, the total energy dependence on the proton position on the line connecting the N and O atoms was determined, to see if the hydrogen bond is formed. It is shown that for only singly reduced PQ this dependence has a symmetric two-well form, i.e. the hydrogen bond is formed. For neutral and doubly reduced PQ, the curve is also two-well but asymmetric, so that the proton is bound to His or to PQ, correspondingly.On the basis of these results, we propose the following scheme of electron-proton coupling. Negatively charged oxygens of PQ form H-bonds with proton donor groups of the surrounding protein and fix PQ in its pocket. While the negative charges of oxygens increase after quinone reduction, protons shift to PQ oxygens and form strong hydrogen bonds with them. Upon second PQ reduction, protons are torn away from surrounding amino acids and form covalent bonds with the quinol. Resulting PQH(2) detaches from its binding place and is replaced by a neutral PQ. The lacking protons on amino acids in the Q(B) pocket are replaced by a step-by-step transfer from the stroma bulk through the proton channels.