Zournas Apostolos, Mani Kyle, Dismukes G Charles
Waksman Institute of Microbiology, Rutgers University, Piscataway, NJ, 08854, USA.
Department of Chemical and Biological Engineering, Rutgers University, Piscataway, NJ, 08854, USA.
Photosynth Res. 2023 Apr;156(1):129-145. doi: 10.1007/s11120-023-00997-0. Epub 2023 Feb 8.
To date, cyclic electron flow around PSI (PSI-CEF) has been considered the primary (if not the only) mechanism accepted to adjust the ratio of linear vs cyclic electron flow that is essential to adjust the ratio of ATP/NADPH production needed for CO carboxylation. Here we provide a kinetic model showing that cyclic electron flow within PSII (PSII-CEF) is essential to account for the accelerating rate of decay in flash-induced oscillations of O yield as the PQ pool progressively reduces to PQH. Previously, PSII-CEF was modeled by backward transitions using empirical Markov models like Joliot-Kok (J-K) type. Here, we adapted an ordinary differential equation methodology denoted RODE1 to identify which microstates within PSII are responsible for branching between PSII-CEF and Linear Electron Flow (LEF). We applied it to simulate the oscillations of O yield from both Chlorella ohadii, an alga that shows strong PSII-CEF attributed to high backward transitions, and Synechococcus elongatus sp. 7002, a widely studied model cyanobacterium. RODE2 simulations reveal that backward transitions occur in microstates that possess a Q semiquinone prior to the flash. Following a flash that forms microstates populating (QQ), PSII-CEF redirects these two electrons to the donor side of PSII only when in the oxidized S and S states. We show that this backward transition pathway is the origin of the observed period-2 oscillations of flash O yield and contributes to the accelerated decay of period-4 oscillations. This newly added pathway improved RODE1 fits for cells of both S. elongatus and C. ohadii. RODE2 simulations show that cellular adaptation to high light intensity growth is due to a decrease in Q availability (empty or blocked by Q), or equivalently due to a decrease in the difference in reduction potential relative to Q/Q. PSII-CEF provides an alternative mechanism for rebalancing the NADPH:ATP ratio that occurs rapidly by adjusting the redox level of the PQ:PQH pool and is a necessary process for energy metabolism in aquatic phototrophs.
迄今为止，围绕光系统I的循环电子流（PSI-CEF）被认为是调整线性与循环电子流比例的主要（如果不是唯一的）机制，而调整该比例对于调节CO羧化所需的ATP/NADPH产生比例至关重要。在此，我们提供了一个动力学模型，表明光系统II内的循环电子流（PSII-CEF）对于解释随着质体醌（PQ）库逐渐还原为PQH₂时，闪光诱导的O₂产量振荡衰减加速率是必不可少的。此前，PSII-CEF是使用如乔利奥-科克（J-K）类型的经验马尔可夫模型通过反向跃迁进行建模的。在此，我们采用了一种名为RODE1的常微分方程方法，以确定光系统II内哪些微状态负责PSII-CEF与线性电子流（LEF）之间的分支。我们将其应用于模拟奥氏小球藻（一种由于高反向跃迁而表现出强烈PSII-CEF的藻类）和聚球藻7002（一种广泛研究的模式蓝细菌）的O₂产量振荡。RODE2模拟显示，反向跃迁发生在闪光前具有半醌型PQ的微状态中。在形成填充（QQ）微状态的闪光之后，只有当处于氧化的S₂和S₁状态时，PSII-CEF才会将这两个电子重新导向PSII的供体侧。我们表明，这种反向跃迁途径是观察到的闪光O₂产量2周期振荡的起源，并导致4周期振荡的加速衰减。这条新添加的途径改善了RODE1对聚球藻和奥氏小球藻细胞的拟合。RODE2模拟表明，细胞对高光强度生长的适应是由于PQ可用性的降低（空的或被PQH₂阻断），或者等效地是由于相对于PQ/PQH₂还原电位差异的降低。PSII-CEF提供了一种通过调整PQ/PQH₂池的氧化还原水平来快速重新平衡NADPH:ATP比例的替代机制，并且是水生光合生物能量代谢的必要过程。
