Quantitative Determination of the Distribution between Two Photosystem II-Mediated Oxidation Reactions in Oscillatoria chalybea: A Comparison between Water Oxidation and Hydrogen Peroxide Decomposition

Abstract

Abstract Mass spectromctric analysis reveals that oxygen evolution measured as the consequence of short saturating light flashes in thylakoid preparations of the filamentous cyanobacterium Oscillatoria chalybea consists of two portions, one coming from photosynthetic water splitting and one coming from H2O2 decomposition. This H2O2 decomposition is photosystem II-mediated and it is the S-state system which oxidizes H2O2 to give protons and oxygen. Water is neither intermediate nor seems it to be the origin of the reaction. At the high oxygen partial pressure of normal air H2O2 production and its decomposition exceeds manyfold the H2O splitting reaction. H2O2 production seems to come from photosystem II but is not necessarily produced on the acceptor side of photosystem II in the sense of a Mehler type reaction. From the reaction rate and the observed labeling density, it is inferred that production and decomposition must take place within the same reaction site which might be for both, the production and decomposition, the S-state system. In this sense. H2O2 might be the product of the S-state system and seems somehow associated with S2 or S3. Thus, if oxygen evolution is measured as the consequence of short saturating light flashes in an ambient atmosphere of 21% oxygen, mass spectrometry reveals a flash pattern which bears the oxygen label of the ambient atmosphere and which has not much in common with an usual Kok sequence. Such a pattern might start in the first three flashes more or less as a Kok pattern would, but is then in the pattern portion usually characteristic for steady-state oxygen evolution characterized by a periodicity of two indicating that H2O2 decomposition requires only two light quanta. At high oxygen partial pressure (e.g. in 21% ,16O2) both reaction portions can be quantitatively deter- mined by labeling the assay with H2 18O and measuring the evolved (16O::18O)/18O2 ratio which is representative for water splitting. The measured evolution of 16O2 (mass 32) represents H2O2 decomposition, if the 16O2 portion calculated from the measured mass 34/36 ratio is subtracted. At low oxygen partial pressure the H2O2 forming and decomposing reaction is largely sup- pressed and oxygen evolution from water-splitting prevails. As a hypothesis, H2O2 production and its decomposition might be a defective performance of photosystem II at high ambient oxygen partial pressure in these cyanobacteria, perhaps due to the principal absence of two of the extrinsic peptides from photosystem II.