Regulation of light energy conversion between linear and cyclic electron flow within photosystem II controlled by the plastoquinone/quinol redox poise

Ultrapurified Photosystem II complexes crystalize as uniform microcrystals (PSIIX) of unprecedented homogeneity that allow observation of details previously unachievable, including the longest sustained oscillations of flash-induced O 2 yield over > 200 flashes and a novel period-4.7 water oxidation cycle. We provide new evidence for a molecular-based mechanism for PSII-cyclic electron flow that accounts for switching from linear to cyclic electron flow within PSII as the downstream PQ/PQH 2 pool reduces in response to metabolic needs and environmental input. The model is supported by flash oximetry of PSIIX as the LEF/CEF switch occurs, Fourier analysis of O 2 flash yields, and Joliot-Kok modeling. The LEF/CEF switch rebalances the ratio of reductant energy (PQH 2 ) to proton gradient energy (H + o /H + i ) created by PSII photochemistry. Central to this model is the requirement for a regulatory site (Q C ) with two redox states in equilibrium with the dissociable secondary electron carrier site Q B . Both sites are controlled by electrons and protons. Our evidence fits historical LEF models wherein light-driven water oxidation delivers electrons (from Q A − ) and stromal protons through Q B to generate plastoquinol, the terminal product of PSII-LEF in vivo. The new insight is the essential regulatory role of Q C . This site senses both the proton gradient (H + o /H + i ) and the PQ pool redox poise via e − /H + equilibration with Q B . This information directs switching to CEF upon population of the protonated semiquinone in the Qc site (Q − H + ) C , while the WOC is in the reducible S2 or S3 states. Subsequent photochemical primary charge separation (P + Q A − ) forms no (QH 2 ) B , but instead undergoes two-electron backward transition in which the Q C protons are pumped into the lumen, while the electrons return to the WOC forming (S1/S2). PSII-CEF enables production of additional ATP needed to power cellular processes including the terminal carboxylation reaction and in some cases PSI-dependent CEF.