• Energy Research

The integration of the water-oxidation enzyme photosystem II (PSII) into electrodes allows the electrons extracted from water oxidation to be harnessed for enzyme characterization and to drive novel endergonic reactions. However, PSII continues to underperform in integrated photoelectrochemical systems despite extensive optimization efforts. Here we carried out protein-film photoelectrochemistry using spinach and Thermosynechococcus elongatus PSII, and we identified a competing charge transfer pathway at the enzyme-electrode interface that short-circuits the known water-oxidation pathway. This undesirable pathway occurs as a result of photo-induced O2 reduction occurring at the chlorophyll pigments and is promoted by the embedment of PSII in an electron-conducting fullerene matrix, a common strategy for enzyme immobilization. Anaerobicity helps to recover the PSII photoresponse and unmasks the onset potentials relating to the QA/QB charge transfer process. These findings impart a fuller understanding of the charge transfer pathways within PSII and at photosystem-electrode interfaces, which will lead to more rational design of pigment-containing photoelectrodes in general.

In this chapter we introduce the physical models at the basis of photosynthetic light harvesting and energy conversion (charge separation). We discuss experiments that demonstrate the processes of light harvesting in the major plant light-harvesting complex (LHCII) and charge separation in the photosystem II reaction center (PSII RC) and how these processes can be modeled at a quantitative level. This is only possible by taking into account the exciton structure of the chromophores in the pigment-protein complexes, static (conformational) disorder, and coupling of electronic excitations and charge-transfer (CT) states to fast nuclear motions. We give examples of simultaneous fitting of linear and nonlinear (timedependent) spectral responses based on modified Redfield theory that resulted in a consistent physical picture of the energy- and electron-transfer reactions. This picture, which includes the time scales and pathways of energy and charge transfer, allows for a visualization of the excitation dynamics, thus leading to a deeper understanding of how photosynthetic pigment-proteins perform their function in the harvesting and efficient conversion of solar energy. We show that LHCII has the intrinsic capacity to switch between different light-harvesting and energydissipating (quenched) states. We introduce the conformational "switching" model for the LHCII protein to explain its role both in light harvesting and in photoprotection. This model explains how the local environment of the protein controls its intrinsic conformational disorder to serve a functional role. Finally, we demonstrate that the PSII RC performs charge separation via two competing pathways of which the selection depends on the conformational disorder induced by slow protein motions. Therefore, we show that the pigment-protein interactions play a decisive role in controlling the functionality of the pigment-protein complexes at work in photosynthesis.

New insights on Lhca4 from two-dimensional electronic spectroscopy and modelling: population of the charge-transfer state and newly identified low-energy trap.

Two-dimensional photon echo in the photosystem II reaction center reveals the exciton-vibrational coherences that promote directed energy/electron transfers.

AbstractIn photosynthesis, pigment–protein complexes achieve outstanding photoinduced charge separation efficiencies through a set of strategies in which excited states delocalization over multiple pigments (“excitons”) and charge‐transfer states play key roles. These concepts, and their implementation in bioinspired artificial systems, are attracting increasing attention due to the vast potential that could be tapped by realizing efficient photochemical reactions. In particular, de novo designed proteins provide a diverse structural toolbox that can be used to manipulate the geometric and electronic properties of bound chromophore molecules. However, achieving excitonic and charge‐transfer states requires closely spaced chromophores, a non‐trivial aspect since a strong binding with the protein matrix needs to be maintained. Here, we show how a general‐purpose artificial protein can be optimized via molecular dynamics simulations to improve its binding capacity of a chlorophyll derivative, achieving complexes in which chromophores form two closely spaced and strongly interacting dimers. Based on spectroscopy results and computational modeling, we demonstrate each dimer is excitonically coupled, and propose they display signatures of charge‐transfer state mixing. This work could open new avenues for the rational design of chromophore–protein complexes with advanced functionalities.

Recently, exciton-photon strong coupling has been proposed as a means to control and enhance energy transfer in ensembles of organic molecules. Here, we demonstrate that the exciton dynamics in an archetypal purple bacterial photosynthetic unit, composed of six LH2 antennas surrounding a single LH1 complex, is greatly modified by its interaction with an optical cavity. We develop a Bloch-Redfield master equation approach that accounts for the interplay between the B800 and B850 bacteriochlorophyll molecules within each LH2 antenna, as well as their interactions with the central LH1 complex. Using a realistic parametrization of both photosynthetic unit and optical cavity, we investigate the formation of polaritons in the system, revealing that these can be tuned to accelerate its exciton dynamics by three orders of magnitude. This yields a significant occupation of the LH1 complex, the stage immediately prior to the reaction center, with only a few-femtosecond delay after the initial excitation of the LH2 B800 pigments. Our theoretical findings unveil polaritonic phenomena as a promising route for the characterization, tailoring, and optimization of light-harvesting mechanisms in natural and artificial photosynthetic processes. 21 pages, 4 figures

Photosynthesis is the natural process that converts solar photons into energy-rich products that are needed to drive the biochemistry of life. Two ultrafast processes form the basis of photosynthesis: excitation energy transfer and charge separation. Under optimal conditions, every photon that is absorbed is used by the photosynthetic organism. Fundamental quantum mechanics phenomena, including delocalization, underlie the speed, efficiency and directionality of the charge-separation process. At least four design principles are active in natural photosynthesis, and these can be applied practically to stimulate the development of bio-inspired, human-made energy conversion systems.