Solid State NMR and modelling of photoinduced energy and electron transfer

Prof. dr. Huub de Groot

Huub de Groot is professor in Biophysical Organic Chemistry. With his team he works in the field of photosynthesis and artificial photosynthesis. The molecular basis for photosynthesis is formed by protein complexes and organelles that contain chlorophyll molecules. The antenna systems herein capture photons from sunlight. The light energy is then transmitted to the reaction centers, where it is converted into chemical energy. In order to study this process and work towards its application for renewable energy, we use Magic Angle Spinning (MAS) NMR, and contribute to the development of this method. We founded the first ultra high field MAS NMR facility in the world, using major European subsidies. This has triggered a revolution in the solid state MAS NMR scientific community and allows to solve structure that is inaccessible to diffraction or NMR in solution. We have initiated and participate in the development of BioSolar Cells, natural and artificial systems for the direct conversion of light energy into fuel and cellular products.

Over the years our research team has focused on the development of high resolution solid state Magic Angle Spinning MAS NMR spectroscopy and its application for studying the fundamentals of membrane proteins involved in energy conversion in natural photosynthesis and other photobiological processes by resolving mechanisms of function. In recent years we use this knowledge for providing guidance to the chemical design of responsive materials for artificial photosynthesis.

Developing responsive photocatalytic matrices is an important goal of the research into artificial photosynthesis. Crucial elements are the photosynthetic reaction centers that drive the water oxidation and proton or CO2 reduction processes, of which the detailed mechanisms are not yet fully understood in natural photosynthesis. Nature uses four manganese ions bridged by oxygen to split water. It is a bad catalyst that is turned into a good photocatalyst by the action of the protein matrix around it. The whole process of water splitting is very complex. Our recent measurements and modelling of natural photosynthesis have shown that stress on the chlorophylls in the ground state from the surrounding matrix makes that upon excitation electrons are freed in the dye in a coherent proton coupled process where quantum tunnelling and classical coherent motion go hand in hand, performing an intricate molecular dance. The fine art of developing artificial photosynthesis is to mimic this dance and fit all energy requirements into the available budget represented by the difference between the open voltage of an optimal tandem cell (~2.8V) and the net voltage associated with energy storage (1.23V). Nature has a very clever trick to do this efficiently. It combines the three largest losses: preventing reverse reactions internally, the need for water-splitting overpotential, and providing required heat at the end of the process, by integrating them with kinetic control over the reaction by the complex structure – a matrix of proteins – that contains all active components. With this integrated triple-play strategy, the energy efficiency is optimal and the production of heat is delayed to the end of the reaction, where it is needed. Our research leads us to understand the basic principles behind this process.

The biological design of photosynthesis is established by evolution. Nature uses what is around and makes only limited modifications. By taking a biological motif and making minor changes, the solutions that biology has selected can serve as starting points for the reverse engineering of an artificial photosynthesis framework. Chlorobaculum tepidum, a green bacterium, has evolved chlorosomes, highly ordered structures where chlorophyll molecules have found their place in such a way that they capture almost all incoming photons and communicate very efficiently with the reaction centres involved. The chlorosome framework is remarkably robust and accommodates a large chemical variety. Together with colleagues in the Netherlands and abroad, we have resolved the structure of the chlorosomes and how the heterogeneity is established. We now use chlorosomes as a source of inspiration for artificial systems, by putting semi-synthetic chlorins in solid membranes, with synthetic self-assembled dyes that are subject to strongly competing interactions, similar to the biology, and with programmable peptide scaffolds.

The work on photosynthesis and artificial photosynthesis in our group is leading, with NMR following, but never limiting. Thus, we have started already at an early stage to transform MAS NMR into a mature technique to study structure, dynamics, and mechanisms of function. We have established MAS NMR at ultra high field for structure and structure function studies, and have combined MAS NMR with optical excitation for photo-CIDNP enhancement for improved sensitivity and selectivity. With constrained ab initio and multiscale modeling we interpret our experimental data. This allows to understand primary mechanisms in photosynthesis and to apply them for the chemical design of smart matrices for energy conversion from photon to fuel. We collaborate extensively with colleagues using vibrational spectroscopy and electron microscopy, and we have established a research line in magnetic resonance microscopy. We use both extensive and selective isotope enrichment, perform protein expression and have studied morphologies of polymeric materials and provided a class of water oxidation catalysts. Our approaches have disseminated into laboratories over the world and many of our alumni have established independent research groups and developed their own academic careers after they left our group in Leiden. Current challenges are to explore the use of 1H for detailed structure determination in solid state NMR; to understand and apply the fundamental principles of kinetic control for efficient energy conversion in natural and artificial photosynthesis; to contribute to the design of triple play smart matrix photocatalysts that use kinetic control by buying time for efficiency; to exploit the biological-geological history as an independent evolutionary determinant for semi-synthetic chemical design, and to bridge the gap between physiology and “omics” technologies with microimaging and HRMAS metabolomics for directed evolution of high performance phototrophs.

Research areas

Our research output is classified according to the following areas:

1.    Ultra High Field MAS NMR
a.    Resolving reaction coordinates in photosynthetic reaction centers (Huub de Groot, Francesco Buda, Alia)
b.    Chlorosome-inspired photoanode design for water oxidation  (Huub de Groot, Francesco Buda)
c.    Integration of MAS NMR with imaging (EM and diffraction) for resolving structure (Huub de Groot, Francesco Buda)
d.    Fourier operators for 1H MAS NMR at ultra high field (Huub de Groot)

2.    Modelling
a.    Bio-inspired in silico design of molecular modules for solar fuel devices (Francesco Buda, Huub de Groot).
b.    Stochastic quasi-Newton: enhanced sampling of the PES (Agur Sevink)
c.    Minimal models for biomolecular and biomimetic responsive matrices (Agur Sevink)
d.    Kinetics and thermodynamics of multi-electron catalysis (Francesco Buda, Huub de Groot)

3.    Biology/biophysics
a.    MRM and MRS for tracking metabolic profiles in ultra high field from plants to animals (Alia, Huub de Groot)
b.    Directed evolution for gaining photosynthetic energy efficiency: phenotypic engineering, photosystem III and (semi-)artificial symbionts (Wim de Grip, Huub de Groot, Alia)
c.    Historical contingency in the evolutionary design of photosynthetic energy conversion (Jan Wijbrans, Alia, Francesco Buda, Huub de Groot)

4.    Applications
a.    Ultra High Field NMR (MAS, mu-MRI, MRS)
b.    Photo-CIDNP (Karthick Babu sai Sankar Gupta, Alia, Huub de Groot)
c.    DFT at different length scales (Francesco Buda, Agur Sevink)
d.    NMR phenotyping micro-technology at ultra high field (Alia, Huub de Groot)
e.    Imaging cryoprobe (MRM/MRS) (Alia, Huub de Groot)
f.    Membrane proteins: labeling, expression, reconstitution (Alia, Wim de Grip; with Anjali Pandit)

  1. Joya, K.S., H.J.M. de Groot, "Controlled Surface-Assembly of Nanoscale Leaf-Type Cu-Oxide Electrocatalyst for High Activity Water Oxidation", ACS Catalysis, vol. 6, issue 3, pp. 1768 - 1771, 03/2016. DOI: 10.1021/acscatal.5b02950
  2. Augustijn, D., U. Roy, R. van Schadewijk, H.J.M. de Groot, A. Alia, "Metabolic Profiling of Intact Arabidopsis thaliana Leaves during Circadian Cycle Using 1H High Resolution Magic Angle Spinning NMR", PLOS ONE, vol. 11, issue 9, pp. e0163258, 9/2016. DOI: 10.1371/journal.pone.0163258
  3. Monti, A., C.F.A. Negre, V.S. Batista, L.G.C. Rego, H.J.M. de Groot, F. Buda, "Crucial Role of Nuclear Dynamics for Electron Injection in a Dye–Semiconductor Complex", The Journal of Physical Chemistry Letters, vol. 6, issue 12, pp. 2393 - 2398, 06/2015. DOI: 10.1021/acs.jpclett.5b00876
  4. Purchase, R.L., H.J.M. de Groot, "Biosolar cells: global artificial photosynthesis needs responsive matrices with quantum coherent kinetic control for high yield", Interface Focus, vol. 5, issue 372735260311249007345125892102653621225-26619810713733912391628, pp. 20150014 - 20150014, 06/2015. DOI: 10.1098/rsfs.2015.0014
  5. Alia, A., F. Buda, H.J.M. de Groot, J. Matysik, "Solid-State NMR of Nanomachines Involved in Photosynthetic Energy Conversion", Annual Review of Biophysics, Vol 42, vol. 42, pp. 675-699, 2013. DOI: 10.1146/Annurev-Biophys-083012-130415
  6. Eisenmayer, T.J., H.J.M. de Groot, E. van de Wetering, J. Neugebauer, F. Buda, "Mechanism and Reaction Coordinate of Directional Charge Separation in Bacterial Reaction Centers", The Journal of Physical Chemistry Letters, vol. 3, issue 6, pp. 694 - 697, 03/2012. DOI: 10.1021/jz201695p
  7. Ganapathy, S., G.T. Oostergetel, P.K. Wawrzyniak, M. Reus, A.G.M. Chew, F. Buda, E.J. Boekema, D.A. Bryant, et al., "Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes", Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 21, pp. 8525-8530, May, 2009. DOI: 10.1073/pnas.0903534106

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