“Spin-Torch NMR”: Transfer of nuclear hyperpolarization to explore molecular environment

• Applicant: Professor Dr. Jörg Matysik
• Subject Area: Analytical Chemistry
• Term: from 2019 to 2023
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 430238088

• Final Report Year: 2023

Final Report Abstract

Heliobacteria are organisms of the earth's early evolution that still exist today. Their photosynthetic reaction centers (RCs) are simple in structure and have perfect C2 symmetry. The identity of the cofactors and the X-ray structure has only been known for a few years. Our work provides very detailed new experimental and theoretical data on the electronic structure and local dynamics of crucial cofactors of heliobacterial RCs. The experiments are a combination of solid-state NMR spectroscopy with signal amplification by the solid-state photo- CIDNP effect. (i) On this new empirical basis, the functional mechanism of heliobacterial RCs will be reconstructed, and the parameter space of functional natural RCs will be extended this new set of data. Working on artificial RCs, this knowledge might be very helpful. - It would have been desirable if the dataset on electronic structure and local dynamics would also be also included the tuning of cofactors by the protein pocket. We will however need more time for that. (ii) Heliobacterial RCs use both electron transfer pathways to equal extents. In contrast, many of the evolutionarily younger RCs selectively use only one of the two electron transfer pathways. The discussion about the control of directionality has been going on for many decades without a clear result. Comparison with data from unidirectional purple bacterial RCs may provide a clue for the longstanding question of the functional symmetry break in photosynthetic RCs. (iii) The very successful analysis of the solid-state photo-CIDNP effect in flavoproteins, socalled LOV domains, has also benefited from the project, as a new preparation method could be developed that allows protein samples to survive very much longer under exposure. This makes two-dimensional experiments on these samples possible as well. Presently, three publications Yunmi Kim et al. are in preparation: dedicated to the electronic ground-state structure of heliobacterial RCs, the dynamics of the relevant cofactors and the overall protein structure and dynamics (with Peter Hildebrand, Institut für Medizinische Physik und Biophysik, Univ. Leipzig).

Publications

• Photo-CIDNP in Solid State. Applied Magnetic Resonance, 53(3-5), 521-537.
  Matysik, Jörg; Ding, Yonghong; Kim, Yunmi; Kurle, Patrick; Yurkovskaya, Alexandra; Ivanov, Konstantin & Alia, A.
  
• Teaching product operators using the Vega diagram. Solid State Nuclear Magnetic Resonance, 122, 101830.
  Matysik, Jörg; Song, Chen; Bielytskyi, Pavlo & Alia, A.
  
• Spin Dynamics of Flavoproteins. International Journal of Molecular Sciences, 24(9), 8218.
  Matysik, Jörg; Gerhards, Luca; Theiss, Tobias; Timmermann, Lisa; Kurle-Tucholski, Patrick; Musabirova, Guzel; Qin, Ruonan; Ortmann, Frank; Solov’yov, Ilia A. & Gulder, Tanja
  
• Spin Hyperpolarization in Modern Magnetic Resonance. Chemical Reviews, 123(4), 1417-1551.
  Eills, James; Budker, Dmitry; Cavagnero, Silvia; Chekmenev, Eduard Y.; Elliott, Stuart J.; Jannin, Sami; Lesage, Anne; Matysik, Jörg; Meersmann, Thomas; Prisner, Thomas; Reimer, Jeffrey A.; Yang, Hanming & Koptyug, Igor V.
  
• Stabilization of a flavoprotein for solid-state photo-CIDNP MAS NMR at room temperature by embedding in a glassy sugar matrix. Journal of Magnetic Resonance, 353, 107497.
  Kurle-Tucholski, Patrick; Köhler, Lisa; Zhao, Ziyue; Link, Gerhard; Wiebeler, Christian & Matysik, Jörg
  
• Structural Elucidation Based on Photo-CIDNP NMR. Integrated Structural Biology, 301-326. Royal Society of Chemistry.
  Matysik, Jörg; Kim, Yunmi; Kurle-Tucholski, Patrick; Musabirova, Guzel; Qin, Ruonan & Alia, A.