Structural dynamics and photoinduced electron transfer

Lead Research Organisation: Queen Mary, University of London
Department Name: Chemistry

Abstract

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.

Planned Impact

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.

Publications

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Pospíšil P (2021) Solvent-Dependent Excited-State Evolution of Prodan Dyes. in The journal of physical chemistry. B

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Takematsu K (2019) Hole Hopping Across a Protein-Protein Interface. in The journal of physical chemistry. B

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Záliš S (2021) Photoinduced hole hopping through tryptophans in proteins. in Proceedings of the National Academy of Sciences of the United States of America

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Šrut A (2022) Nonadiabatic excited-state dynamics of ReCl(CO)3(bpy) in two different solvents. in Physical chemistry chemical physics : PCCP

 
Description 1. Photoinduced electron transfer in biomolecules.
1a. Theoretical simulations of photoinduced electron transfer in proteins have revealed important design principles for constructing biomimetic photocatalytic systems. They stress the importance of solvent (water) access to light-absorbing and electron-shuttling sites, roles of polar amino-acid side chains, and the necessity of unrestricted fluctuations of the protein/solvent environment of active cofactors. These theoretical results are in agreement with our experiments, as well as with literature data. They can be easily extended to other photoactive biomolecular as well as small-molecule systems. Interesting predictions about protein photocatalysis in nonaqueous media and bioelectronic films have been made. Our multiscale simulation method combining classical and quantum molecular dynamics realistically describes temporal evolution of low-lying electronic states of the chromophore, intermediate oxidized sites, as well as the protein and solvating water. It is broadly applicable and will likely find use in the biophysics community.
1b. We are currently obtaining exciting results on photoinduced electron transfer in molecular donor-acceptor systems. This is a work in progress, which provides unprecedented insights into structural factors determining rates and mechanisms of photochemical electron transfer. We focus especially on coupling between electron-transfer and vibrational dynamics. Some of these newly synthesized systems produce long-lived charge-separated states upon irradiation with visible light - a necessary prerequisite for photocatalysis and light-energy harvesting.

2. Protein and solvation dynamics in relation to electron transfer.
2a. We have unequivocally demonstrated that photoinduced electron transfer in proteins labelled with organometallic rhenium carbonyl-polypyridine photosensitizers occurs on the same timescale as dynamic fluctuations of the solvated protein environment. For these experiments, we have utilized the unique ability of rhenium complexes to act at the same time as electron-transfer photosensitizers and luminophores. We found that their phosphorescence shifts with time to lower energies as the electron transfer proceeds. We now pursue the possibility of electron-transfer facilitation through protein and solvent dynamics.
2b. We have unraveled the nature of the processes underlying functioning of Prodan as a molecular probe of solvation and dynamics of biomolecules. In particular, we have shown that Prodan responds to reorientation of solvent dipoles and hydrogen-bond formation. We are now using this knowledge to determine effects of structural dynamics on photoinduced electron transfer in cytochrome-type proteins.

3. Ultrafast dynamics of new electron-transfer photosensitizers.
3a. Using time-resolved Raman spectroscopy, we have observed femtosecond electronic/vibrational dynamics of rhenium carbonyl-polypyridine sensitizers. These observations initiated theoretical investigations state-of-the-art surface hopping dynamics. Results will help explaining experiments on ultrafast electron transfer in donor-acceptor systems and proteins initiated by photoexcitation of an appended rhenium sensitizer.
3b. We have characterized changing electronic structures of ruthenium complexes with cyano-bipyridine ligands as a function of the oxidation state (i.e., the total number of electrons) varied by up to five units. This study has revealed analogies between molecular responses to electrochemical reduction and optical excitation, and explained the enhancement of infrared absorption upon both processes.
3c. Ultrafast photophysics of dinuclear complexes of Ir(I) and Rh(I) with bridging isocyanide ligands has been investigated by time-resolved infrared spectroscopy and quantum chemical calculations as a function of the energy (wavelength) of irradiating laser pulses. This allowed us to selectively excite different excited states of different energies. Remarkably, we found that individual electronic states decay through their own specific deactivation pathways, bypassing states lying lower in energy. A detailed picture of excitation-dependent photophysics was obtained, which indicates a way how to run photochemical electron and atom transfer selectively from different excited states and thereby better utilize the absorbed light energy.
Exploitation Route Outcomes of this research will be taken forward by the academic community dealing with photocatalysis, light-energy harvesting, and bioenergetics. Our theoretical modelling of electron transfer in azurins and experimental studies of molecular donor-acceptor systems revealed design principles that will help constructing biomimetic protein-based photoactive systems ("photoenzymes") capable of specific photochemical redox transformations and/or conversion of light (solar) energy to the energy of chemical bonds in photochemically produced molecules. Our computational methodology will likely be taken up by biophysicists modelling electron-transfer processes in large biomolecular systems. Results obtained on small-molecule sensitizers will also be developed further by academic researchers for novel photocatalytic processes. For example, our dinuclear sensitizers are capable of both photochemical electron- and atom-transfer reactions. To raise the awareness and facilitate dissemination of our results, we promptly publish in leading scientific journals: 7 papers so far, more in preparation. Later in 2022 we will also disseminate results of this project through talks at international scientific conferences.
Sectors Chemicals

 
Description California Institute of Technology 
Organisation California Institute of Technology
Department Beckman Institute
Country United States 
Sector Academic/University 
PI Contribution Measurements on samples of derivatized protein (azurins): determination of relaxation kinetics. Interpretation of the results, joint paper writing.
Collaborator Contribution Synthesis and structural characterization of protein samples (derivatized azurins). Joint paper writing.
Impact Joint paper in J. Phys. Chem. B
 
Description ELI Beamlines 
Organisation ELI Beamlines
Country Czech Republic 
Sector Private 
PI Contribution We brought the sample, initiated the experiments, interpreted results and wrote the paper.
Collaborator Contribution Provided access and measurements on a world-class time-resolved femtosecond stimulated Raman instrument.
Impact paper, J. Phys. Chem. A
Start Year 2018
 
Description JHI 
Organisation J. Heyrovsky Institute of Physical Chemistry
Country Czech Republic 
Sector Public 
PI Contribution We brought the samples and initiated joint experiments. Interpreted results, wrote the papers.
Collaborator Contribution JHI made it possible to measure relaxation dynamics on their equipment. Collaboration with JHI theorists led to precise spectra interpretation. JHI hosted the PDRAs,
Impact 2 papers, J. Phys. Chem. A and J. Phys. Chem. B