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

The oxygen-evolving complex of Photosystem II cycles through five oxidation states (S-0-S-4), and dark incubation leads to 25% S-0 and 75% S-1. This distribution cannot be reached with charge recombination reactions between the higher S states and the electron acceptor Q(B)(-). We measured flash-induced oxygen evolution to understand how S-3 and S-2 are converted to lower S states when the electron required to reduce the manganese cluster does not come from Q(B)(-). Thylakoid samples preconditioned to make the concentration of the S-1 state 100% and to oxidize tyrosine Y-D 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 S-2 and S-3 are converted to lower S states via recombination from S(2)Q(B)(-) and S(3)Q(B)(-) and by a slow change of the state of oxygen-evolving complex from S-3 and S-2 to S, and So in reactions with unspecified electron donors. The slow pathway appears to contain two-electron routes, S(2)Q(B) -> S(0)Q(B), and S(3)Q(B) -> S(1)Q(B). 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, S(3)Q(B) -> S(2)Q(B) -> S(1)Q(B) 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 S(2)Q(B) -> S(0)Q(B) but added H2O2 did not enhance this reaction.