Bidirectional Energy\nFlow in the Photosystem II Supercomplex

The water-splitting capability of Photosystem II (PSII)\nof plants\nand green algae requires the system to balance efficient light harvesting\nalong with effective photoprotection against excitation in excess\nof the photosynthetic capacity, particularly under the naturally fluctuating\nsunlight intensity. The comparatively flat energy landscape of the\nmulticomponent structure, inferred from the spectra of the individual\npigment–protein complexes and the rather narrow and featureless\nabsorption spectrum, is well known. However, how the combination of\nthe required functions emerges from the interactions among the multiple\ncomponents of the PSII supercomplex (PSII-SC) cannot be inferred from\nthe individual pigment–protein complexes. In this work, we\ninvestigate the energy transfer dynamics of the C<sub>2</sub>S<sub>2</sub>-type PSII-SC with a combined spectroscopic and modeling approach.\nSpecifically, two-dimensional electronic-vibrational (2DEV) spectroscopy\nprovides enhanced spectral resolution and the ability to map energy\nevolution in real space, while the quantum dynamical simulation allows\ncomplete kinetic modeling of the 210 chromophores. We demonstrate\nthat additional pathways emerge within the supercomplex. In particular,\nwe show that excitation energy can leave the vicinity of the charge\nseparation components, the reaction center (RC), faster than it can\ntransfer to it. This enables activatable quenching centers in the\nperiphery of the PSII-SC to be effective in removing excessive energy\nin cases of overexcitation. Overall, we provide a quantitative description\nof how the seemingly contradictory functions of PSII-SC arise from\nthe combination of its individual components. This provides a fundamental\nunderstanding that will allow further improvement of artificial solar\nenergy devices and bioengineering processes for increasing crop yield.