Bidirectional Energy Flow in the Photosystem II Supercomplex

Abstract

AbstractThe water splitting capability of Photosystem II (PSII) of plants and green algae requires the system to balance efficient light harvesting along with effective photoprotection against excitation in excess of photosynthetic capacity1,2, particularly under the naturally fluctuating sunlight intensity. The comparatively flat energy landscape of the multi-component structure, inferred from spectra of the individual pigment-protein complexes and the rather narrow and featureless absorption spectrum, is well known3–7. However, how the combination of the required functions emerge from the interactions among the multiple components of the PSII supercomplex (PSII-SC) cannot be inferred from the individual pigment-protein complexes. In this work, we investigate the energy transfer dynamics of the C2S2-type PSII-SC with a combined spectroscopic and modeling approach. Specifically, two-dimensional electronic-vibrational (2DEV) spectroscopy8,9provides enhanced spectral resolution and the ability to map energy evolution in real space, while the quantum dynamical simulation allows complete kinetic modeling of the 210 chromophores. We demonstrate that additional pathways emerge within the supercomplex. In particular, we show that excitation energy can leave the vicinity of the charge separation components, the reaction center (RC), faster than transferring to it. This enables activatable quenching centers in the periphery of the PSII-SC to be effective in removing excessive energy in cases of over-excitation2. Overall, we provide a quantitative description of how the seemingly contradictory functions of PSII-SC arise from the combination of its individual components. This provides a fundamental understanding that will allow further improvement of artificial solar energy devices and bioengineering processes for increasing crop yield10.