Net charge oscillation and proton release during water oxidation in photosynthesis. An electrochromic band shift study at pH 5.5–7.0

Abstract

In the S-state cycle of water oxidation, a local electric field was measured in states S 2 and S 3. This was indicated by the strongly retarded reduction kinetics of the oxidized primary electron donor of PS II in these states (Brettel, K., Schlodder, E. and Witt, H.T. (1984) Biochim. Biophys. Acta 766, 403–415) as well as by electrochromic band shifts in state S 2 and S 3 (Saygin, Ö. and Witt, H.T., FEBS Lett. 176 (1984) 83–87; 189 (1985) 224–226). The electric field oscillation of 0:0:1:1 in S 0:S 1:S 2:S 3 is strictly coupled with the pattern of manganese redox changes measured at 365 nm and of O 2 evolution under very different conditions (Kretschmann, H. and Witt, H.T. (1993) Biochim. Biophys. Acta 1144, 331–345). In this work with PS II complexes from the cyanobacterium Synechococcus elongatus it is shown that the electric field oscillation as well as the pattern of redox changes of manganese are practically pH-independent between pH 5.5 and pH 7.0; i.e., in the range in which the pattern of O 2 evolution and water oxidation, respectively, is pH-independent. It was suggested that a net charge created as charge difference between electron extraction and proton release from the catalytic center may be the origin of the electric field. With this explanation it follows that, with the S 0→S 1→S 2→S 3S 0 transitions, a independent proton release of 1:0:1:2 from the catalytic center takes place. The proton release into the medium is, however, generally pH-dependent. For PS II complexes from cyanobacteria a mechanism is proposed which may be responsible for the modification of the supposed pH-independent proton release from the catalytic center into the pH-dependent proton release into the medium. It is proposed that in the pH 5–7 range an amino acid residue with a p K value of approx. 6 releases a proton induced by a p K shift through electrostatic interaction with the local electric field set up in state S 2. When, subsequently, the created base traps a proton released from the catalytic center in the S 3→S 0 transition, this results in a pH-dependent non-integer oscillation of the proton release into the medium. The predicted values have been compared with the directly measured ones.