Gates Colin, Ananyev Gennady, Roy-Chowdhury Shatabdi, Fromme Petra, Dismukes G Charles
Dept of Chemistry & Chemical Biology, Rutgers University, Piscataway, USA.
Waksman Institute of Microbiology, Rutgers University, Piscataway, USA.
Photosynth Res. 2023 Apr;156(1):113-128. doi: 10.1007/s11120-022-00985-w. Epub 2022 Nov 27.
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 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 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 flash yields, and Joliot-Kok modeling. The LEF/CEF switch rebalances the ratio of reductant energy (PQH) to proton gradient energy (H/H) created by PSII photochemistry. Central to this model is the requirement for a regulatory site (Q) with two redox states in equilibrium with the dissociable secondary electron carrier site Q. Both sites are controlled by electrons and protons. Our evidence fits historical LEF models wherein light-driven water oxidation delivers electrons (from Q) and stromal protons through Q to generate plastoquinol, the terminal product of PSII-LEF in vivo. The new insight is the essential regulatory role of Q. This site senses both the proton gradient (H/H) and the PQ pool redox poise via e/H equilibration with Q. This information directs switching to CEF upon population of the protonated semiquinone in the Qc site (QH), while the WOC is in the reducible S2 or S3 states. Subsequent photochemical primary charge separation (PQ) forms no (QH), but instead undergoes two-electron backward transition in which the Q 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.
超纯化的光系统II复合物结晶为前所未有的均匀微晶（PSIIX），这使得能够观察到以前无法实现的细节，包括在超过200次闪光中闪光诱导的O产量的最长持续振荡以及新的4.7周期水氧化循环。我们为基于分子的光系统II循环电子流机制提供了新证据，该机制解释了随着下游PQ/PQH池响应代谢需求和环境输入而减少时，光系统II内从线性电子流切换到循环电子流的过程。该模型得到了PSIIX闪光血氧测定法（当发生线性电子流/循环电子流切换时）、O闪光产量的傅里叶分析以及乔利奥 - 科克模型的支持。线性电子流/循环电子流切换重新平衡了由光系统II光化学产生的还原剂能量（PQH）与质子梯度能量（H⁺/H⁺）的比例。该模型的核心是需要一个具有两种氧化还原状态且与可解离的二级电子载体位点Q处于平衡的调节位点（Q₀）。这两个位点都受电子和质子控制。我们的证据符合历史上的线性电子流模型，其中光驱动的水氧化通过Q₀传递电子（来自Q）和基质质子以生成质体醌，质体醌是体内光系统II线性电子流的终产物。新的见解是Q₀的关键调节作用。该位点通过与Q₀的e⁻/H⁺平衡感知质子梯度（H⁺/H⁺）和PQ池的氧化还原平衡。当Qc位点（QH）中的质子化半醌积累，而水氧化复合物处于可还原的S₂或S₃状态时，此信息引导切换到循环电子流。随后的光化学初级电荷分离（PQ）不形成（QH），而是经历双电子向后转变过程，其中Q₀质子被泵入内腔，而电子返回水氧化复合物形成（S₁/S₂）。光系统II循环电子流能够产生为细胞过程提供能量所需的额外ATP，包括末端羧化反应，在某些情况下还包括依赖光系统I的循环电子流。
