Structural dynamics and photoinduced electron transfer

Our life closely depends on light: vision provides us with information on the world around us while photosynthesis supplies us with food, as well as energy that was deposited over millions of years in fossil fuels. Photosynthesis employs a flow of electrons through proteins driven by sunlight and many researchers are trying to replicate it and produce fuels from abundant clean sources in artificial systems. Electron transfer also underlies many enzymatic reactions as well as respiration. Sequential transfer of electrons through chains of aromatic amino acids (tryptophan, tyrosine) was recently suggested to play a protective role in enzymes that use molecular oxygen to oxidize organic compounds in our bodies.

Chemical reactions, including electron transfer, are too often explained in terms of static molecular or protein structures. However, life and chemistry are highly dynamic; molecules as well as their environment are perpetually in motion. Indeed, Richard Feynman famously wrote "everything that is living can be understood in terms of the jiggling and wiggling of atoms". In our work, we will focus on this aspect and try to understand the relation between structural fluctuations and electron transfer. We will study proteins bearing photoactive groups that are capable of inducing transfer of electrons across the protein upon irradiation with visible or ultraviolet light. We will measure how such photoactive assemblies and surrounding water molecules fluctuate in time and relate these structural dynamics with the rates, yields, and directionality of phototriggered electron transfer. Among several protein systems, we will also study proteins (azurins) with several aromatic amino acid groups that can themselves undergo electron transfer, while their mutual distance and orientation fluctuate in time. These investigations will tell us how to design photocatalytic systems for artificial photosynthesis to generate fuels or specialty chemicals, as green plants do. In particular, engineering aromatic amino acid chains into proteins is a promising way to strongly accelerate electron transfer in the desired direction.

Time resolved vibrational spectroscopy methods are perfectly suited for such dynamics studies. Infrared or Raman spectra, which report on molecular vibrational motions, are measured as a function of time after irradiation with short laser pulses of light that trigger both structural relaxation and electron transfer. Shifts and intensity changes of spectral features, together with the emergence of new ones, will simultaneously reveal the nature and rates of structural changes and electron transfer processes. Sophisticated data analysis and theoretical calculations will enable interpretation of experimental results and building up a unifying mechanistic picture of interrelated electron transfer and structural dynamics. UK operates a world leading facility in the field of time resolved vibrational spectroscopy at the Rutherford Appleton Laboratory in Oxfordshire, providing a unique opportunity to carry out the proposed research at the highest experimental level.

Impact will lie in training postdocs, scientific advances and laying grounds for new light-driven catalytic systems ("photoenzymes") for solar energy conversion and specialty chemical synthesis.

Science. Protein dynamics and photoinduced electron transfer underlie a range of important phenomena and applications ranging from protein folding to natural as well as artificial photosynthesis and bioelectronics. We will understand how these two phenomena are related and how they can be used to control the yields and kinetics of electron transfer in complex (bio)molecular systems. A strong academic impact must be ensured first, so that the emerging concepts of interrelated structural and electron-transfer dynamics will be adopted by the scientific community, inspire further research, and used to develop new photocatalytic systems. Hence, the initial pathways to impact will be focused on the academic community.

People. The two PDRAs, as well as QMUL MSci and project students, will obtain exceptionally broad and comprehensive training in chromophore synthesis and characterization, protein expression, advanced laser spectroscopic techniques, data analysis, photochemistry/photophysics, theory, and interpretation of experiments. Although one PDRA will be focused on experimental work and the other on theory, their work will partly overlap and they will be led to share their experience and knowledge. They will advance their "soft-skills" through international collaboration and participation at conferences.

Short-medium term: Research results will be promptly disseminated by publishing in high-quality scientific journals and presenting at principal scientific conferences in the field, for example International Symposia on Photophysics and Photochemistry of Coordination Compounds, RSC and ACS meetings, Gordon Research Conferences. In the final stages of the project, we will generalize the results and also address a wider audience. These are the most appropriate dissemination pathways for a fundamental science project that will benefit the world-wide scientific community in the fields of photochemistry, photophysics, protein and molecular dynamics, electron transfer, photocatalysis, and artificial photosynthesis.

Medium-long term: Controlled and predictable electron transfer can be used to clean energy generation from the sun by photochemical water splitting coupled with carbon dioxide reduction to generate fuels (hydrogen, methanol, carbon monoxide, hydrocarbons). Analogous nitrogen reduction to ammonia by photodriven electron supply would lead to enormous energy savings. On the device side, controlled electron transfer in protein films will lead to sensors, biomemories, and even biocomputing through protein-protein interfaces behaving as semiconducting junctions or using controlled/switchable electron transport through DNA.