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

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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 (QC) with two redox states in equilibrium with the dissociable secondary electron carrier site QB. Both sites are controlled by electrons and protons. Our evidence fits historical LEF models wherein light-driven water oxidation delivers electrons (from QA−) and stromal protons through QB to generate plastoquinol, the terminal product of PSII-LEF in vivo. The new insight is the essential regulatory role of QC. This site senses both the proton gradient (H+o/H+i) and the PQ pool redox poise via e−/H+ equilibration with QB. 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+QA−) forms no (QH2)B, but instead undergoes two-electron backward transition in which the QC 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.

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Acknowledgements

This work was funded by the Department of Energy, Basic Energy Sciences, Grant DE-FG02-10ER16195 (to G.C.D. and G.A.) and the NSF Science and Technology BioXFEL center award 1231306 (to P.F.).

Funding

Basic Energy Sciences, DE-FG02-10ER16195,G. Charles Dismukes,BioXFEL Science and Technology Center, 1231306, Petra Fromme

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Authors and Affiliations

  1. Dept of Chemistry & Chemical Biology, Rutgers University, Piscataway, USA

    Colin Gates, Gennady Ananyev & G. Charles Dismukes

  2. Waksman Institute of Microbiology, Rutgers University, Piscataway, USA

    Colin Gates, Gennady Ananyev & G. Charles Dismukes

  3. Dept of Computational Biology & Molecular Biophysics, Rutgers University, Piscataway, NJ, USA

    Colin Gates

  4. Dept of Chemistry and Biochemistry, Loyola University Chicago, Chicago, IL, USA

    Colin Gates

  5. Center for Applied Structural Discovery, Biodesign Institute, Arizona State University, Tempe, AZ, USA

    Shatabdi Roy-Chowdhury & Petra Fromme

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  1. Colin Gates
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Correspondence to G. Charles Dismukes.

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This article is dedicated to the memory of Professor Kenneth Sauer who made important contributions to understanding of the photosystems and the Z-scheme.

Also, we had a dedication to another friend and mentor to the authors, Prof. Ron Pace, who also passed away during the production of this paper and who served as an inspiration to the work. The dedication read. This work is dedicated to the memory of Professor Ronald Pace whose dogged questioning and insightful ideas inspired us to ask why, to delve deeper, and to always treat historical interpretations as conditional models.

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Gates, C., Ananyev, G., Roy-Chowdhury, S. et al. Regulation of light energy conversion between linear and cyclic electron flow within photosystem II controlled by the plastoquinone/quinol redox poise. Photosynth Res 156, 113–128 (2023). https://doi.org/10.1007/s11120-022-00985-w

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