TY - JOUR
T1 - Cyclic electron flow around photosystem II in silico
T2 - How it works and functions in vivo
AU - Zournas, Apostolos
AU - Mani, Kyle
AU - Dismukes, G. Charles
N1 - Funding Information:
This research was funded by National Natural Science Foundation of China (Grant: 81873615, 82070744, 81770723, 81400732), Academic promotion programme of Shandong First Medical University (NO: 2019QL022) and Taishan Scholars Program (NO: ts201712090, tsqn201812138). Acknowledgments
Publisher Copyright:
© 2023, The Author(s), under exclusive licence to Springer Nature B.V.
PY - 2023
Y1 - 2023
N2 - 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 QB− semiquinone prior to the flash. Following a flash that forms microstates populating (QAQB)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 QB availability (empty or blocked by Q2−B), or equivalently due to a decrease in the difference in reduction potential relative to QA/QA−. 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.
AB - 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 QB− semiquinone prior to the flash. Following a flash that forms microstates populating (QAQB)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 QB availability (empty or blocked by Q2−B), or equivalently due to a decrease in the difference in reduction potential relative to QA/QA−. 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.
KW - Cyclic electron transfer
KW - Light-to-chemical energy conversion
KW - Oxygen evolution
KW - Photosynthetic electron transport
KW - Photosystem II
KW - Water oxidation
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U2 - 10.1007/s11120-023-00997-0
DO - 10.1007/s11120-023-00997-0
M3 - Article
C2 - 36753032
AN - SCOPUS:85147650678
SN - 0166-8595
JO - Photosynthesis research
JF - Photosynthesis research
ER -