Cross-species computational analysis of the PMF and its key characteristics

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Photosynthetic proton motive force (PMF) across the thylakoid membrane plays a pivotal role in the regulation of organisms’ energy metabolism. The number of interdependent processes and possible cross-talks between reactions that generate, modulate and depend on PMF are astonishing and their combined effect on the cell’s bioenergetics leads to a nonlinear complexity. Hence, a rigorous framework that allows for a systematic disentangling of its complexity is necessary to develop concepts on how the PMF is achieved and regulated across photosynthetic species. Computational, mechanistic models of the photosynthetic electron transport chain offer a quantitative framework that enables comparative studies. Numerous models of photosynthesis describe PMF, but many of them focus solely on its pH-dependent component (ΔpH), mainly due to its link to the important photoprotective mechanism named non-photochemical quenching. Energy-dependent quenching releases excess light energy as heat, to protect photosystem II against damage. Yet, the importance of the membrane potential (ΔΨ) in the generation of PMF, and photoprotection, should not be ignored, as the photosynthetic electron transport is highly sensitive to the concentration of ions (e.g., H+, K+, Mg2+ and Cl−). Ion transport proteins in the thylakoid membrane, such as KEA3, allow for an out-flux of H+ with a counter-in-flux of cations into the membrane, affecting the contribution of proton-based or potential-driven components of PMF. By dynamic fine-tuning of the two PMF components, photosynthetic organisms can dynamically adapt to environmental changes and balance their energy production to meet their energy demand. In this project, we aim to construct a unifying theoretical framework describing the dynamics of PMF for numerous classes of photosynthetic organisms studied by the GoPMF partners, ranging from cyanobacteria to green microalgae to higher plants. Building on the previously constructed mathematical models of the photosynthetic electron transport chain, we will fully explore the modular design of our models to create a blueprint for PMF regulation. Within this framework, we will be able to systematically investigate the effect of PMF partitioning on the photosynthetic dynamics and perform cross-species comparisons to generate novel hypotheses regarding PMF regulation. Combined with the collected experimental work, our model will guide the experiment in the light-driven production of hydrogen in cyanobacteria. Our ambition is to construct a platform where Aims 1,2,4, and 5 of the GoPMF can be further explored.