Regulation of light energy conversion between linear and cyclic electron flow within photosystem II controlled by the...

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 O₂ 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/PQH₂ 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 O₂ flash yields, and Joliot-Kok modeling. The LEF/CEF switch rebalances the ratio of reductant energy (PQH₂) 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 (QH₂)_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.