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15N–1H Transfer of Light-Induced Nuclear Hyperpolarization in Frozen Photosynthetic Reaction Centers

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Abstract

Recently, we have demonstrated the possibility to transfer the light-induced hyperpolarization occurring on select 13C nuclei of photosynthetic cofactors due to the solid-state photochemically induced dynamic nuclear polarization (photo-CIDNP) effect into the proton pool via inverse 13C–1H cross-polarization Bielytskyi et al. (J Magn Reson 293: 82–91, 2018). Such approach allowed us to observe the selective response from the protons belonging to photochemically active cofactors in their native protein environment. In the present study, we demonstrate that also 15N nuclei can be used as a source of polarization in a similar type of experiments. We present the 2D photo-CIDNP 15N–1H heteronuclear correlation (HETCOR) experiment acquired on uniformly 15N-labeled quinone-blocked reaction center (RC) from Rhodobacter sphaeroides R26. Obtained 1H chemical shifts match with previously observed ones on selectively 13C-labeled RC from Rhodobacter sphaeroides WT. We expect that using 15N as a source of polarization in potential heteronuclear spin-torch experiments could be advantageous for systems where the procedure for selective 13C labeling is not yet established.

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References

  1. B.E. Bode, S.S. Tamarath, K.B. Sai Sankar Gupta, G. Jeschke, J. Matysik, in Hyperpolarization Methods in NMR Spectroscopy, ed. by L.T. Kuhn (Springer, Berlin, Heidelberg, 2012), pp. 105–121

    Google Scholar 

  2. M. Najdanova, G.J. Janssen, H.J.M. de Groot, J. Matysik, A. Alia, J. Photochem. Photobiol. B 152, 261 (2015)

    Article  Google Scholar 

  3. M.G. Zysmilich, A. McDermott, J. Am. Chem. Soc. 116, 8362 (1994)

    Article  Google Scholar 

  4. G. Jeschke, J. Matysik, Chem. Phys. 294, 239 (2003)

    Article  Google Scholar 

  5. G. Jeschke, J. Am. Chem. Soc. 120, 4425 (1998)

    Article  Google Scholar 

  6. T. Polenova, A.E. McDermot, J. Phys. Chem. B 103, 553 (1999)

    Article  Google Scholar 

  7. A. McDermott, M.G. Zysmilich, T. Polenova, Solid State Nucl. Magn. Reson. 11, 21 (1998)

    Article  Google Scholar 

  8. D. Sosnovsky, G. Jeschke, J. Matysik, H.-M. Vieth, K.L. Ivanov, J. Phys. Chem. 144, 144202 (2016)

    Article  Google Scholar 

  9. J. Matysik, E. Schulten, A. Alia, P. Gast, J. Raap, J. Lugtenburg, A.J. Hoff, H.J.M. de Groot, Biol. Chem. 382, 1271 (2001)

    Article  Google Scholar 

  10. E.A.M. Schulten, J. Matysik, A. Alia, S. Kiihne, J. Raap, J. Lugtenburg, P. Gast, A.J. Hoff, H.J.M. de Groot, Biochemistry 41, 8708 (2002)

    Article  Google Scholar 

  11. S. Paul, B.E. Bode, J. Matysik, A. Alia, J. Phys. Chem. B 119, 13897–13903 (2015)

    Article  Google Scholar 

  12. P. Bielytskyi, D. Gräsing, K.R. Mote, K.B. Sai Sankar Gupta, S. Vega, P.K. Madhu, A. Alia, J. Matysik, J. Magn. Reson. 293, 82 (2018)

    Article  ADS  Google Scholar 

  13. M.G. Zysmilich, A. McDermott, J. Am. Chem. Soc. 118, 5867 (1996)

    Article  Google Scholar 

  14. E. Daviso, K.B. Sai Sankar Gupta, S. Prakash, P. Gast, A. Alia, G. Jeschke, J. Matysik, in Photosynthesis. Energy from the Sun, ed. by J.F. Allen, E. Gantt, J.H. Golbeck, B. Osmond (Springer, Dordrecht, 2008), pp. 25–28

    Chapter  Google Scholar 

  15. S.S. Tamarath, A. Alia, E. Daviso, D. Mance, J.H. Golbeck, J. Matysik, Biochemistry 51, 5763 (2012)

    Article  Google Scholar 

  16. G.J. Janssen, E. Roy, J. Matysik, A. Alia, Appl. Magn. Reson. 42, 57 (2012)

    Article  Google Scholar 

  17. J.C. Zill, Z. He, M. Tank, B.H. Ferlez, D.P. Canniffe, Y. Lahav, P. Bellstedt, A. Alia, I. Schapiro, J.H. Gobeck, D.A. Bryant, J. Matysik, Photosynth. Res. 137, 295 (2018)

    Article  Google Scholar 

  18. J.C. Zill, M. Kansy, R. Goss, A. Alia, C. Wilhelm, J. Matysik, Photosynth. Res. (2018). https://doi.org/10.1007/s11120-018-0578-9

    Google Scholar 

  19. G. Fehler, M.Y. Okamura, in The Photosynthetic Bacteria, ed. by R.K. Clayton, W. Sistrom (Plenum Press, New York, 1978), pp. 349–378

    Google Scholar 

  20. M.R. Fischer, H.J.M. de Groot, J. Raap, C. Winkel, A.J. Hoff, J. Lugtenburg, Biochemistry 31, 11038 (1992)

    Article  Google Scholar 

  21. J. Matysik, A. Alia, J.G. Hollander, T. Egorova-Zachernyuk, P. Gast, H.J.M. de Groot, Indian J. Biochem. Biophys. 37, 418 (2000)

    Google Scholar 

  22. E. Daviso, G. Jeschke, J. Matysik, in Biophysical Techniques in Photosynthesis, vol. II, ed. by T. Aartsma, J. Matysik (Springer Netherlands, Dordrecht, 2008), pp. 385–399

    Chapter  Google Scholar 

  23. R.S. Thakur, N.D. Kurur, P.K. Madhu, Chem. Phys. Lett. 426, 459 (2006)

    Article  ADS  Google Scholar 

  24. M. Lee, W.I. Goldburg, Phys. Rev. A 140, 1261 (1965)

    Article  ADS  Google Scholar 

  25. O.B. Peersen, X. Wu, S.O. Smith, J. Magn. Reson., Ser. A 106, 127 (1994)

    Article  ADS  Google Scholar 

  26. S. Paul, R.S. Thakur, M. Goswami, A.C. Sauerwein, S. Mamone, M. Concistrè, H. Förster, M.H. Levitt, P.K. Madhu, J. Magn. Reson. 197, 14 (2009)

    Article  ADS  Google Scholar 

  27. M. Leskes, P.K. Madhu, S. Vega, Chem. Phys. Lett. 447, 370 (2007)

    Article  ADS  Google Scholar 

  28. K.R. Mote, V. Agarwal, P.K. Madhu, Prog. Nucl. Magn. Reson. Spectrosc. 97, 1 (2016)

    Article  Google Scholar 

  29. C. Coelho, J. Rocha, P.K. Madhu, L. Marfa, J. Magn. Reson. 194, 264 (2008)

    Article  ADS  Google Scholar 

  30. E. Vinogradov, P.K. Madhu, S. Vega, J. Chem. Phys. 115, 8983 (2001)

    Article  ADS  Google Scholar 

  31. E. Vinogradov, P.K. Madhu, S. Vega, Chem. Phys. Lett. 354, 193 (2002)

    Article  ADS  Google Scholar 

  32. M. Leskes, P.K. Madhu, S. Vega, J. Chem. Phys. 125, 124506 (2006)

    Article  ADS  Google Scholar 

  33. D. Marion, M. Ikura, R. Tschudin, A. Bax, J. Magn. Reson. 85, 393 (1989)

    ADS  Google Scholar 

  34. B.-J. van Rossum, C.P. de Groot, V. Ladizhansky, S. Vega, H.J.M. de Groot, J. Am. Chem. Soc. 122, 3465 (2000)

    Article  Google Scholar 

  35. H. Fuess, D. Hohlwein, S.A. Mason, Acta Cryst. B 33, 654 (1977)

    Article  Google Scholar 

  36. E. Daviso, S. Prakash, A. Alia, P. Gast, G. Jeschke, J. Matysik, Appl. Magn. Reson. 37, 49 (2010)

    Article  Google Scholar 

  37. S. Prakash, A. Alia, P. Gast, H.J.M. de Groot, G. Jeschke, J. Matysik, J. Am. Chem. Soc. 127, 14290 (2005)

    Article  Google Scholar 

  38. S.S. Thamarath, B.E. Bode, S. Prakash, K.B. Sai Sankar Gupta, A. Alia, G. Jeschke, J. Matysik, J. Am. Chem. Soc. 134, 5921 (2012)

    Article  Google Scholar 

  39. F. Lendzian, M. Huber, R.A. Isaacson, B. Endeward, M. Plato, B. Bonigk, K. Möbius, W. Lubitz, G. Feher, Biochim. Biophys. Acta 1183, 139 (1993)

    Article  Google Scholar 

  40. K.B. Sai Sankar Gupta, A. Alia, H.J.M. de Groot, J. Matysik, J. Am. Chem. Soc. 135, 10382 (2013)

    Article  Google Scholar 

  41. M.H. Stowell, T.M. McPhillips, D.C. Rees, S.M. Soltis, E. Abresch, G. Feher, Science 276, 812 (1997)

    Article  Google Scholar 

  42. A. Diller, S. Prakash, A. Alia, P. Gast, J. Matysik, G. Jeschke, J. Phys. Chem. B 111, 10606 (2007)

    Article  Google Scholar 

  43. E. Daviso, S. Prakash, A. Alia, P. Gast, J. Neugebauer, G. Jeschke, J. Matysik, Proc. Natl. Acad. Sci. USA 106, 22281 (2009)

    Article  ADS  Google Scholar 

  44. T. Egorova-Zachernyuk, B.J. van Rossum, C. Erkelens, H.J.M. de Groot, Magn. Reson. Chem. 46, 1074 (2008)

    Article  Google Scholar 

  45. A. Alia, P.K. Wawrzyniak, G.J. Janssen, F. Buda, J. Matysik, H.J.M. de Groot, J. Am. Chem. Soc. 131, 9626 (2009)

    Article  Google Scholar 

  46. C. Giessner-Prettre, B. Pullman, J. Theor. Biol. 31, 287 (1971)

    Article  Google Scholar 

  47. M. Ernst, B.H. Meier, in Encyclopedia of NMR, vol. 1, ed. by R.K. Harris, R.E. Wasylishen (Wiley, Chichester, West Sussex, 2012), pp. 44–55

    Google Scholar 

  48. P. Palmas, S. Ilas, E. Girard, Magn. Reson. Chem. 49, 788 (2011)

    Google Scholar 

  49. D. Gräsing, P. Bielytskyi, I.F. Céspedes-Camacho, A. Alia, T. Marquardsen, F. Engelke, J. Matysik, Sci. Rep. 7, 12111 (2017)

    Article  ADS  Google Scholar 

  50. S. Prakash, P. Gast, H.J.M. de Groot, J. Matysik, G. Jeschke, J. Am. Chem. Soc. 128, 12794 (2006)

    Article  Google Scholar 

Download references

Acknowledgements

Generous support by the Deutsche Forschungsgemeinschaft is acknowledged (MA-4972/2-1 and MA 4972/11-1). PB would like to thank Prof. P.K. Madhu (TIFR Hyderabad) for exciting discussions.

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Authors and Affiliations

  1. Institut für Analytische Chemie, Universität Leipzig, Linnéstraße 3, 04103, Leipzig, Germany

    Pavlo Bielytskyi, Daniel Gräsing & Jörg Matysik

  2. Leibniz Institute of Surface Engineering (IOM), Permoserstraße 15, 04318, Leipzig, Germany

    Stefan Zahn

  3. Leiden Institute of Chemistry, Leiden University, Einsteinweg 55, 2301 RA, Leiden, The Netherlands

    A. Alia

  4. Institut für Medizinische Physik und Biophysik, Universität Leipzig, Härtelstr. 16-18, 04107, Leipzig, Germany

    A. Alia

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  1. Pavlo Bielytskyi
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Bielytskyi, P., Gräsing, D., Zahn, S. et al. 15N–1H Transfer of Light-Induced Nuclear Hyperpolarization in Frozen Photosynthetic Reaction Centers. Appl Magn Reson 50, 695–708 (2019). https://doi.org/10.1007/s00723-019-1110-x

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  • DOI: https://doi.org/10.1007/s00723-019-1110-x

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