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

Abstract

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.

Keywords: Electron acceptors; Kok model; Microcrystals; Oxygen evolution; Photosystem II; VZAD; Water-oxidizing complex.