Cyclic electron flow around photosystem II in silico: How it works and functions in vivo

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 CO₂ 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 O₂ yield as the PQ pool progressively reduces to PQH₂. 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 O₂ 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_B^- semiquinone prior to the flash. Following a flash that forms microstates populating (Q_AQ_B)^2-, PSII-CEF redirects these two electrons to the donor side of PSII only when in the oxidized S₂ and S₃ states. We show that this backward transition pathway is the origin of the observed period-2 oscillations of flash O₂ 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_B availability (empty or blocked by Q^2-_B), or equivalently due to a decrease in the difference in reduction potential relative to Q_A/Q_A^-. PSII-CEF provides an alternative mechanism for rebalancing the NADPH:ATP ratio that occurs rapidly by adjusting the redox level of the PQ:PQH₂ pool and is a necessary process for energy metabolism in aquatic phototrophs.