Two-Electron Reactions S2QB →S0QB and S3QB →S1QB are Involved in Deactivation of Higher S States of the Oxygen-Evolving Complex of Photosystem II

Abstract

The oxygen-evolving complex of Photosystem II cycles through five oxidation states (S0–S4), and dark incubation leads to 25% S0 and 75% S1. This distribution cannot be reached with charge recombination reactions between the higher S states and the electron acceptor QB−. We measured flash-induced oxygen evolution to understand how S3 and S2 are converted to lower S states when the electron required to reduce the manganese cluster does not come from QB−. Thylakoid samples preconditioned to make the concentration of the S1 state 100% and to oxidize tyrosine YD were illuminated by one or two laser preflashes, and flash-induced oxygen evolution sequences were recorded at various time intervals after the preflashes. The distribution of the S states was calculated from the flash-induced oxygen evolution pattern using an extended Kok model. The results suggest that S2 and S3 are converted to lower S states via recombination from S2QB− and S3QB− and by a slow change of the state of oxygen-evolving complex from S3 and S2 to S1 and S0 in reactions with unspecified electron donors. The slow pathway appears to contain two-electron routes, S2QB →S0QB, and S3QB →S1QB. The two-electron reactions dominate in intact thylakoid preparations in the absence of chemical additives. The two-electron reaction was replaced by a one-electron-per-step pathway, S3QB →S2QB →S1QB in PS II-enriched membrane fragments and in thylakoids measured in the presence of artificial electron acceptors. A catalase effect suggested that H2O2 acts as an electron donor for the reaction S2QB →S0QB but added H2O2 did not enhance this reaction.