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One Electron Multiple Proton Transfer in Model Organic Donor–Acceptor Systems: Implications for High-Frequency EPR

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Abstract

EPR spectroscopy is an important spectroscopic method for identification and characterization of radical species involved in many biological reactions. The tyrosyl radical is one of the most studied amino acid radical intermediates in biology. Often in conjunction with histidine residues, it is involved in many fundamental biological electron and proton transfer processes, such as in the water oxidation in photosystem II. As biological processes are typically extremely complicated and hard to control, molecular bio-mimetic model complexes are often used to clarify the mechanisms of the biological reactions. Here, we present theoretical calculations to investigate the sensitivity of magnetic resonance parameters to proton-coupled electron transfer events, as well as conformational substates of the molecular constructs which mimic the tyrosine–histidine (Tyr–His) pairs found in a large variety of proteins. Upon oxidation of the phenol, the Tyr analog, these complexes can perform not only one-electron one-proton transfer (EPT), but also one-electron two-proton transfers (E2PT). It is shown that in aprotic environment the gX-components of the electronic g-tensor are extremely sensitive to the first proton transfer from the phenoxyl oxygen to the imidazole nitrogen (EPT product), leading to a significant increase of the gX-value of up to 0.003, but are not sensitive to the second proton transfer (E2PT). In the latter case, the change of the gX-value is much smaller (ca. 0.0001), which is too small to be distinguished even by high-frequency EPR. The 14N hyperfine values are also too similar to allow differentiation between the different protonation states in EPT and E2PT. The magnetic resonance parameters were also calculated as a function of the rotation angles around single bonds. It was demonstrated that rotation of the phenoxyl group results in large positive changes (> 0.001) in the gX-values. Analysis of the data reveals that the main source of these changes is related to the strength of the H-bond between phenoxyl oxygen and the proton(s) on N1 and N2 positions of the imidazole.

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References

  1. K.-P. Dinse, G. Jeschke, Methods in Physical Chemistry (Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, 2012), pp. 159–189

    Google Scholar 

  2. D. Goldfarb, S. Stoll (eds.), EPR Spectroscopy: Fundamentals and Methods (Wiley, New York, 2018)

    Google Scholar 

  3. S.K. Misra (ed.), Multifrequency Electron Paramagnetic Resonance: Theory and Applications (Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, 2011)

    Google Scholar 

  4. K. Möbius, A. Savitsky, High-Field EPR Spectroscopy on Proteins and Their Model Systems: Characterization of Transient Paramagnetic States (The Royal Society of Chemistry, Cambridge, 2009)

    Google Scholar 

  5. A. Lund, M. Shiotani, S. Shimada, Principles and Applications of ESR Spectroscopy (Springer, Dordrecht, 2011)

    Google Scholar 

  6. A. Schweiger, G. Jeschke, Principles of Pulse Electron Paramagnetic Resonance (Oxford University Press, New York, 2001)

    Google Scholar 

  7. J.A. Weil, J.R. Bolton, J.A. Weil, J.R. Bolton, J.E. Wertz, Electron Paramagnetic Resonance: Elementary Theory and Practical Applications (Wiley, New York, 2007)

    Google Scholar 

  8. M. Drescher, G. Jeschke (eds.), EPR Spectroscopy: Applications in Chemistry and Biology (Springer, Berlin, 2012)

    Google Scholar 

  9. G.R. Eaton, S.S. Eaton, K.M. Salikhov (eds.), Foundations of Modern EPR (World Scientific Publishing, Singapore, 1998)

  10. J. Niklas, O.G. Poluektov, Adv. Energy Mater. 7, 1602226 (2017)

    Google Scholar 

  11. K. Möbius, W. Lubitz, N. Cox, A. Savitsky, Magnetochemistry 4, 85 (2018)

    Google Scholar 

  12. F. Gerson, W. Huber, Electron Spin Resonance Spectroscopy of Organic Radicals (Wiley-VCH, Weinheim, 2003)

    Google Scholar 

  13. H. Kurreck, B. Kirste, W. Lubitz, Angew. Chem. Int. Edit. 23, 173–194 (1984)

    Google Scholar 

  14. H. Kurreck, B. Kirste, W. Lubitz, Electron Nuclear Double Resonance Spectroscopy of Radicals in Solution—Applications to Organic and Biological Chemistry (VCH Publishers Inc., Deerfield Beach, 1988)

    Google Scholar 

  15. K. Möbius, W. Fröhling, F. Lendzian, W. Lubitz, M. Plato, C.J. Winscom, J. Phys. Chem. 86, 4491–4507 (1982)

    Google Scholar 

  16. G. Jeschke, ChemPhysChem 3, 927–932 (2002)

    Google Scholar 

  17. C. Gemperle, A. Schweiger, Chem. Rev. 91, 1481–1505 (1991)

    Google Scholar 

  18. A. Savitsky, K. Möbius, Photosynth. Res. 102, 311–333 (2009)

    Google Scholar 

  19. O. Grinberg, L.J. Berliner (eds.), Very High Frequency (VHF) ESR/EPR, vol. 22 (Springer, New York, 2004)

    Google Scholar 

  20. L. Kulik, W. Lubitz, Photosynth. Res. 102, 391–401 (2009)

    Google Scholar 

  21. Y.S. Lebedev, Appl. Magn. Reson. 7, 339–362 (1994)

    Google Scholar 

  22. O.Y. Grinberg, A.A. Dubinskii, in Very High Frequency (VHF) ESR/EPR, vol. 22, ed. by O. Grinberg, L.J. Berliner (Springer, New York, 2004), pp. 1–18

    Google Scholar 

  23. A.A. Galkin, O.Y. Grinberg, A.A. Dubinskii, N.N. Kabdin, V.N. Krymov, V.I. Kurochkin, Y.S. Lebedev, L.F. Oranskii, V.F. Shuvalov, Instrum. Exp. Tech. 20, 1229–1229 (1977)

    Google Scholar 

  24. A.Y. Bresgunov, A.A. Dubinskii, V.N. Krimov, Y.G. Petrov, O.G. Poluektov, Y.S. Lebedev, Appl. Magn. Reson. 2, 715–728 (1991)

    Google Scholar 

  25. O.Y. Grinberg, A.A. Dubinskii, Y.S. Lebedev, Usp. Khim. 52, 1490–1513 (1983)

    Google Scholar 

  26. C. Rudowicz, S.K. Misra, Appl. Spectrosc. Rev. 36, 11–63 (2001)

    ADS  Google Scholar 

  27. F. Neese, Multifrequency Electron Paramagnetic Resonance (Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, 2011), pp. 295–326

    Google Scholar 

  28. M. Kaupp, M. Bühl, V.G. Malkin (eds.), Calculation of NMR and EPR Parameters: Theory and Applications (Wiley-VCH, Weinheim, 2004)

    Google Scholar 

  29. F. Neese, in High Resolution EPR: Applications to Metalloenzymes and Metals in Medicine, ed. by L. Berliner, G. Hanson (Springer New York, New York, 2009), pp. 175–229

    Google Scholar 

  30. F. Neese, Coord. Chem. Rev. 253, 526–563 (2009)

    Google Scholar 

  31. M.L. Munzarova, P. Kubacek, M. Kaupp, J. Am. Chem. Soc. 122, 11900–11913 (2000)

    Google Scholar 

  32. M. Munzarova, M. Kaupp, J. Phys. Chem. A 103, 9966–9983 (1999)

    Google Scholar 

  33. M. Retegan, N. Cox, W. Lubitz, F. Neese, D.A. Pantazis, Phys. Chem. Chem. Phys. 16, 11901–11910 (2014)

    Google Scholar 

  34. G.T. Babcock, M. Espe, C. Hoganson, N. LydakisSimantiris, J. McCracken, W.J. Shi, S. Styring, C. Tommos, K. Warncke, Acta Chem. Scand. 51, 533–540 (1997)

    Google Scholar 

  35. D.L. Jenson, B.A. Barry, J. Am. Chem. Soc. 131, 10567–10573 (2009)

    Google Scholar 

  36. B.A. Barry, Biochim. Biophys. Acta Bioenerg. 1847, 46–54 (2015)

    Google Scholar 

  37. S. Un, P. Dorlet, A.W. Rutherford, Appl. Magn. Reson. 21, 341–361 (2001)

    Google Scholar 

  38. P. Faller, C. Goussias, A.W. Rutherford, S. Un, Proc. Natl. Acad. Sci. USA 100, 8732–8735 (2003)

    ADS  Google Scholar 

  39. R.E. Blankenship, Molecular Mechanisms of Photosynthesis (Blackwell Science Limited, Oxford, 2002)

    Google Scholar 

  40. T.J. Wydrzynski, K. Satoh (eds.), Photosystem II—The Light-Driven Water: Plastoquinone Oxidoreductase, vol. 22 (Springer, Dordrecht, 2005)

    Google Scholar 

  41. Y. Umena, K. Kawakami, J.R. Shen, N. Kamiya, Nature 473, 55–60 (2011)

    ADS  Google Scholar 

  42. P. Faller, R.J. Debus, K. Brettel, M. Sugiura, A.W. Rutherford, A. Boussac, Proc. Natl. Acad. Sci. USA 98, 14368–14373 (2001)

    ADS  Google Scholar 

  43. R. Chatterjee, C.S. Coates, S. Milikisiyants, C.I. Lee, A. Wagner, O.G. Poluektov, K.V. Lakshmi, Biochemistry 52, 4781–4790 (2013)

    Google Scholar 

  44. S.J. Mora, E. Odella, G.F. Moore, D. Gust, T.A. Moore, A.L. Moore, Acc. Chem. Res. 51, 445–453 (2018)

    Google Scholar 

  45. J.D. Megiatto, D.D. Mendez-Hernandez, M.E. Tejeda-Ferrari, A.L. Teillout, M.J. Llansola-Portoles, G. Kodis, O.G. Poluektov, T. Rajh, V. Mujica, T.L. Groy, D. Gust, T.A. Moore, A.L. Moore, Nat. Chem. 6, 423–428 (2014)

    Google Scholar 

  46. D.A. Svistunenko, Biochim. Biophys. Acta Bioenerg. 1707, 127–155 (2005)

    Google Scholar 

  47. A. Migliore, N.F. Polizzi, M.J. Therien, D.N. Beratan, Chem. Rev. 114, 3381–3465 (2014)

    Google Scholar 

  48. J. Stubbe, W.A. van der Donk, Chem. Rev. 98, 705–762 (1998)

    Google Scholar 

  49. L. Hammarström, S. Styring, Energy Environ. Sci. 4, 2379–2388 (2011)

    Google Scholar 

  50. H.B. Gray, J.R. Winkler, Acc. Chem. Res. 51, 1850–1857 (2018)

    Google Scholar 

  51. S.Y. Reece, D.G. Nocera, Annu. Rev. Biochem. 78, 673–699 (2009)

    Google Scholar 

  52. E. Odella, S.J. Mora, B.L. Wadsworth, J.J. Goings, M.A. Gervaldo, L.E. Sereno, T.L. Groy, D. Gust, T.A. Moore, G.F. Moore, S. Hammes-Schiffer, A.L. Moore, Chem. Sci. 11, 3820–3828 (2020)

    Google Scholar 

  53. E. Odella, B.L. Wadsworth, S.J. Mora, J.J. Goings, M.T. Huynh, D. Gust, T.A. Moore, G.F. Moore, S. Hammes-Schiffer, A.L. Moore, J. Am. Chem. Soc. 141, 14057–14061 (2019)

    Google Scholar 

  54. E. Odella, S.J. Mora, B.L. Wadsworth, M.T. Huynh, J.J. Goings, P.A. Liddell, T.L. Groy, M. Gervaldo, L.E. Sereno, D. Gust, T.A. Moore, G.F. Moore, S. Hammes-Schiffer, A.L. Moore, J. Am. Chem. Soc. 140, 15450–15460 (2018)

    Google Scholar 

  55. M.T. Huynh, S.J. Mora, M. Villalba, M.E. Tejeda-Ferrari, P.A. Liddell, B.R. Cherry, A.L. Teillout, C.W. Machan, C.P. Kubiak, D. Gust, T.A. Moore, S. Hammes-Schiffer, A.L. Moore, ACS Cent. Sci. 3, 372–380 (2017)

    Google Scholar 

  56. P.J. Stephens, F.J. Devlin, C.F. Chabalowski, M.J. Frisch, J. Phys. Chem. 98, 11623–11627 (1994)

    Google Scholar 

  57. A.D. Becke, J. Chem. Phys. 98, 5648–5652 (1993)

    ADS  Google Scholar 

  58. J. Baker, T. Janowski, K. Wolinski, P. Pulay, Wiley Interdiscip. Rev. Comput. Mol. Sci. 2, 63–72 (2012)

    Google Scholar 

  59. S.G. Balasubramani, G.P. Chen, S. Coriani, M. Diedenhofen, M.S. Frank, Y.J. Franzke, F. Furche, R. Grotjahn, M.E. Harding, C. Hattig, A. Hellweg, B. Helmich-Paris, C. Holzer, U. Huniar, M. Kaupp, A.M. Khah, S.K. Khani, T. Müller, F. Mack, B.D. Nguyen, S.M. Parker, E. Perlt, D. Rappoport, K. Reiter, S. Roy, M. Rückert, G. Schmitz, M. Sierka, E. Tapavicza, D.P. Tew, C. Wüllen, V.K. Voora, F. Weigend, A. Wodyński, J.M. Yu, J. Chem. Phys. 152, 36 (2020)

    Google Scholar 

  60. F. Weigend, R. Ahlrichs, Phys. Chem. Chem. Phys. 7, 3297–3305 (2005)

    Google Scholar 

  61. F. Furche, R. Ahlrichs, C. Hattig, W. Klopper, M. Sierka, F. Weigend, Wiley Interdiscip. Rev. Comput. Mol. Sci. 4, 91–100 (2014)

    Google Scholar 

  62. S. Grimme, S. Ehrlich, L. Goerigk, J. Comput. Chem. 32, 1456–1465 (2011)

    Google Scholar 

  63. S. Grimme, J. Antony, S. Ehrlich, H. Krieg, J. Chem. Phys. 132, 154104 (2010)

    ADS  Google Scholar 

  64. F. Neese, Wiley Interdiscip. Rev. Comput. Mol. Sci. 8, 6 (2018)

    Google Scholar 

  65. F. Neese, Wiley Interdiscip. Rev. Comput. Mol. Sci. 2, 73–78 (2012)

    Google Scholar 

  66. V. Barone, M. Cossi, J. Phys. Chem. A 102, 1995–2001 (1998)

    Google Scholar 

  67. M. Steinmetz, A. Hansen, S. Ehrlich, T. Risthaus, S. Grimme, in Density Functionals: Thermochemistry, ed. by E.R. Johnson (Springer International Publishing, Cham, 2015), pp. 1–23

    Google Scholar 

  68. D. Svistunenko, M. Adelusi, M. Dawson, P. Robinson, C. Bernini, A. Sinicropi, R. Basosi, Stud. Univ. Babes Bolyai Chem. 56, 135–146 (2011)

    Google Scholar 

  69. D.A. Svistunenko, C.E. Cooper, Biophys. J. 87, 582–595 (2004)

    ADS  Google Scholar 

  70. S. Sinnecker, E. Reijerse, F. Neese, W. Lubitz, J. Am. Chem. Soc. 126, 3280–3290 (2004)

    Google Scholar 

  71. G.J. Gerfen, B.F. Bellew, S. Un, J.M. Bollinger, J. Stubbe, R.G. Griffin, D.J. Singel, J. Am. Chem. Soc. 115, 6420–6421 (1993)

    Google Scholar 

  72. J.R. Asher, M. Kaupp, Theor. Chem. Acc. 119, 477–487 (2008)

    Google Scholar 

  73. J.R. Asher, N.L. Doltsinis, M. Kaupp, Magn. Reson. Chem. 43, S237–S247 (2005)

    Google Scholar 

  74. J.R. Asher, N.L. Doltsinis, M. Kaupp, J. Am. Chem. Soc. 126, 9854–9861 (2004)

    Google Scholar 

  75. S. Un, M. Atta, M. Fontecave, A.W. Rutherford, J. Am. Chem. Soc. 117, 10713–10719 (1995)

    Google Scholar 

  76. L. Benisvy, R. Bittl, E. Bothe, C.D. Garner, J. McMaster, S. Ross, C. Teutloff, F. Neese, Angew. Chem. Int. Edit. 44, 5314–5317 (2005)

    Google Scholar 

  77. T.I. Smirnova, A.I. Smirnov, S.V. Paschenko, O.G. Poluektov, J. Am. Chem. Soc. 129, 3476–3477 (2007)

    Google Scholar 

  78. T.I. Smirnova, T.G. Chadwick, M.A. Voinov, O. Poluektov, J. van Tol, A. Ozarowski, G. Schaaf, M.M. Ryan, V.A. Bankaitis, Biophys. J. 92, 3686–3695 (2007)

    ADS  Google Scholar 

  79. K. Möbius, A. Savitsky, C. Wegener, M. Plato, M. Fuchs, A. Schnegg, A.A. Dubinskii, Y.A. Grishin, I.A. Grigor'ev, M. Kuhn, D. Duché, H. Zimmermann, H.J. Steinhoff, Magn. Reson. Chem. 43, S4–S19 (2005)

    Google Scholar 

  80. M. Plato, H.J. Steinhoff, C. Wegener, J.T. Torring, A. Savitsky, K. Möbius, Mol. Phys. 100, 3711–3721 (2002)

    ADS  Google Scholar 

  81. S. Sinnecker, A. Rajendran, A. Klamt, M. Diedenhofen, F. Neese, J. Phys. Chem. A 110, 2235–2245 (2006)

    Google Scholar 

  82. M. Witwicki, J. Jezierska, A. Ozarowski, Chem. Phys. Lett. 473, 160–166 (2009)

    ADS  Google Scholar 

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Acknowledgements

This study is based upon work supported by U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences, Division of Chemical Sciences, Geosciences, and Biosciences, under contract number DE-AC02-06CH11357 at Argonne National Laboratory (JN and OGP) and DE-FG02-03ER15393 (ALM and TAM). The work was supported by the Illinois Space Grant Consortium and National Institutes of Health (SC3 GM122614) (HO and KLM). We gratefully acknowledge the computing resources provided on Blues and Bebop, high-performance computing clusters operated by the Laboratory Computing Resource Center at Argonne National Laboratory.

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Authors and Affiliations

  1. Chemical Sciences and Engineering Division, Argonne National Laboratory, Lemont, IL, 60439, USA

    Jens Niklas & Oleg G. Poluektov

  2. Department of Chemistry, Physics, and Engineering Studies, Chicago State University, Chicago, IL, 60628, USA

    Kristy L. Mardis & Harriet Omodayo

  3. School of Molecular Sciences, Arizona State University, Tempe, AZ, 85287, USA

    Emmanuel Odella, Thomas A. Moore & Ana L. Moore

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  1. Kristy L. Mardis
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Mardis, K.L., Niklas, J., Omodayo, H. et al. One Electron Multiple Proton Transfer in Model Organic Donor–Acceptor Systems: Implications for High-Frequency EPR. Appl Magn Reson 51, 977–991 (2020). https://doi.org/10.1007/s00723-020-01252-8

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