Cooperative binding of oxygen to the water-splitting enzyme in the filamentous cyanobacterium Oscillatoria chalybea

In the filamentous cyanobacterium Oscillatoria ia chalybea ben photolysis o f water does not take place in the complete absence of oxygen. A catalytic oxygen partial pressure of 15x10(-6) Torr has to be present for effective w ater splitting to occur. By means of mass spectrometry we measured the phot osynthetic oxygen evolution in the presence of (H2O)-O-18 in dependence on the oxygen partial pressure of the atmosphere and analysed the liberations of O-16(2), (OO)-O-16-O-18 and O-18(2) simultaneously The observed dependen ces of the light-induced oxygen evolution on bound oxygen yield sigmoidal c urves, Hill coefficient values of 3.0, 3.1 and 3.2, respectively, suggest t hat the binding is cooperative and that four molecules of oxygen have to be : bound per chain to the oxygen evolving complex. Oxygen seems to prime the water-splitting reaction by redox steering of the S-state system, putting it in the dark into the condition from which water splitting can start. It appears that in O. chalybea an interaction of oxygen with S-0 and S-1 leads to S-2 and S-3, thus yielding the typical oxygen evolution pattern in whic h even after extensive dark adaptation substantial amounts of Y-1 and Y-2 a re found. The interacting oxygen is apparently reduced to hydrogen peroxide . Mass spectrometry permits to distinguish this highly specific oxygen requ irement from the interaction of bulk atmospheric oxygen with the oxygen evo lving complex of the cyanobacterium. This interaction leads to the formatio n H2O2 which is decomposed under O-2 evolution in the light. The dependence on oxygen-partial pressure and temperature is analysed. Structural peculia rities of the cyanobacterial reaction centre of photosystem II referring to the extrinsic peptides might play a role. (C) 2000 Elsevier Science B.V. A ll rights reserved.