Understanding charge separation in photosynthetic reaction centers II by a novel spectroscopy of gas phase chlorophyll constructions – ELECTROPHYLLE

The Electrophylle project seeks to characterize a fundamental process involved in the initial transformation of light energy in the reaction center of Photosystem II that initiates photosynthesis in plants and algae. Electrophylle will create a synergy around a new gas phase experimental method applied to chlorophyll systems, a condensed phase approach and their theoretical modeling.
Photosystem II (PSII) plays a central role during photosynthesis: indeed, solar energy collected by the antennae is transferred to PSII where the initial charge separation takes place, leading after subsequent steps to a negative charge production and water splitting into dioxygen+ protons. This charge separation is the initial and limiting step to the production of energy and dioxygen, the sources of life. Its quantum efficiency is close to unity and remains unexplained unless one accepts an hypothesis involving a resonant effect and is produced by natural evolutive adaptation.
Indeed, the core of the PSII reaction center consists of a set of 12 chlorophyll-related molecules undergoing excitonic coupling, which can be reduced to a working ensemble of only 4 molecules. 2D time-domain spectroscopy measurements indicate the crucial influence in the efficiency of the charge separation mechanism, of resonances between chlorophyll vibration frequencies and the energy gaps separating neutral from ionic pairs. The resulting model reproduces the initial charge separation dynamics in this reaction center based however on fragmentary spectroscopic data. The electronic and vibrational structure of the elements in the core of the PSII reaction center, the chlorophylls, their excitonic pairs are insufficiently known to validate the essential hypothesis of a vibration energy gap resonance that will establish a new model. This can only be achieved by measurements in the gas phase or cryogenic solutions or as in the Electrophylle project, by a combination of both with quantum chemistry calculations.
We propose to determine by resonant electron photodetachment spectroscopy, the vibrational and electronic structure of neutral chlorophyll and chlorophyll dimers cooled at 10K and electron tagged. Gas phase spectroscopy of biomolecules has the unique advantage of allowing access to the structure of biomolecules in the absence of medium interactions and being directly comparable to the results of quantum computations. On the other hand, we will achieve microsolvation of chlorophylls by single molecular bonds to bring them into dimers akin to those of the reaction center. This step is essential since it allows tuning their electronic levels into resonance with chlorophyll vibrations that drive charge separation with maximum efficiency. These gas phase measurements will be combined with fluorescence line narrowing (FLN) spectroscopy that addresses the interacting dimers in the protein environment. This will give access to a complete picture of the interaction landscape in chlorophyll dimers in several conditions, from free to assembled into special pairs. Specific quantum calculations will characterize the electronic and vibrational structure of these systems. This will yield energy level positions for chlorophylls and pairs in ground and first electronically excited states, together with a landscape of the interactions within chlorophyll pairs between neutral and ionic states.
This project is designed to characterize a fundamental process related to energy transformation –photosynthesis- by a synergy between a new experimental method as applied to a complex system, the reaction center of Photosytem II, theoretical modelling and condensed phase spectroscopy. The precise modeling and understanding of such a fundamental process could help boosting the efficiency of artificial molecular photocatalysts, the electronic properties of which could be tuned to improve their ability of performing ultrafast (10-12 s) charge separation with high quantum yield.