Real-time nanoscale manipulation of structure and environment to understand light-harvesting regulation in photosynthesis

forthcoming

Sunlight is a source of life for plants but also of photodamage. To harvest solar energy “safely”, plants have developed a nanoscale mechanism controlled by small proteins which bind pigments, called light-harvesting complexes (LHCs). At low light intensities, the LHCs harvest and transport solar energy to the sites of photochemistry. Under intense light, LHCs switch function to dissipate excess energy as heat. Through this photoprotective switch, the LHCs efficiently protect plants from photodamage. Yet, how do plants activate the LHC photoprotective switch? Current models assume that the switch is driven by protein conformational changes of the LHCs, regulated by the environment through pH changes and interactions with protein and cofactors. However, no experimental tool implemented in the field of photosynthesis allows to identify the conformational changes responsible of photoprotection and to determine how the environment controls them – limiting our mechanistic understanding of light-harvesting regulation in plants. I will tackle this challenge by: 1) Pioneering the study of LHC nanomechanics via single-molecule optical tweezers, resolved in force and fluorescence, to track LHC conformational changes at single-residue level and identify those driving the photoprotective switch. 2) Leveraging a novel ultrafast multipulse spectroscopic tool — just developed by my group — to rapidly control environmental changes and determine the intermediate steps in the photoprotective switch of the LHCs. 3) Integrating ad hoc molecular dynamics simulations to map how external physiological factors tune the conformational landscape of the LHCs. By implementing a novel optical and computational toolkit, I will advance our understanding of how plants regulate light harvesting at the nanoscale, while establishing a new framework in photosynthesis and photobiology to determine how structure and environment control the function of photosensory proteins across all life domains.