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Ultrafast Spectroscopy of Hydrogenase Enzyme Models

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Coherent Multidimensional Spectroscopy

Part of the book series: Springer Series in Optical Sciences ((SSOS,volume 226))

Abstract

Hydrogenase enzymes are nature’s solution to using molecular hydrogen as an energy source. While the air-sensitivity of these biological catalysts make them impractical for industrial hydrogen generation, synthetic mimics show promise in acting as effective substitutes. Hydrogenase model compounds also enable detailed investigation of the ultrafast dynamics and chemical reaction mechanisms using ultrafast infrared spectroscopy. This chapter reviews the progress in applying ultrafast transient infrared absorption and multidimensional spectroscopy to a range of small molecule hydrogenase model compounds, as well as several macromolecular and larger constructs. The rich vibrational structure and straightforward chemical modularity of these diiron compounds represent an exciting class of molecules that are, at the same time, excellent model systems for fundamental chemical dynamics, and practical molecular catalytic components with direct application to next-generation hydrogen-based energy strategies.

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References

  1. J.W. Peters, G.J. Schut, E.S. Boyd, D.W. Mulder, E.M. Shepard, J.B. Broderick, P.W. King, M.W.W. Adams, FeFe- and NiFe-hydrogenase diversity, mechanism, and maturation. Biochim. Biophys. Acta 2015, 1350–1369 (1853)

    Google Scholar 

  2. T.D. Veras, T.S. Mozer, D. dos Santos, A.D. Cesar, Hydrogen: trends, production and characterization of the main process worldwide. Int. J. Hydrog. Energy 42, 2018–2033 (2017)

    Article  Google Scholar 

  3. G.J. Kubas, Fundamentals of H2 binding and reactivity on transition metals underlying hydrogenase function and H2 production and storage. Chem. Rev. 107, 4152–4205 (2007)

    Article  Google Scholar 

  4. D. Schilter, J.M. Camara, M.T. Huynh, S. Hammes-Schiffer, T.B. Rauchfuss, Hydrogenase enzymes and their synthetic models: the role of metal hydrides. Chem. Rev. 116, 8693–8749 (2016)

    Article  Google Scholar 

  5. J.M. Camara, T.B. Rauchfuss, Combining acid-base, redox and substrate binding functionalities to give a complete model for the FeFe-hydrogenase. Nat. Chem. 4, 26–30 (2012)

    Article  Google Scholar 

  6. I.P. Georgakaki, L.M. Thomson, E.J. Lyon, M.B. Hall, M.Y. Darensbourg, Fundamental properties of small molecule models of Fe-only hydrogenase: computations relative to the definition of an entatic state in the active site. Coord. Chem. Rev. 238, 255–266 (2003)

    Article  Google Scholar 

  7. J.W. Peters, W.N. Lanzilotta, B.J. Lemon, L.C. Seefeldt, X-ray crystal structure of the Fe-only hydrogenase (Cpl) from Clostridium pasteurianum to 1.8 angstrom resolution. Science 282, 1853–1858 (1998)

    Google Scholar 

  8. D.L.M. Suess, R.D. Britt, Biosynthesis of the FeFe hydrogenase active site. FASEB J. 30 (2016)

    Google Scholar 

  9. A. Kohen, Role of dynamics in enzyme catalysis: substantial versus semantic controversies. Acc. Chem. Res. 48, 466–473 (2015)

    Article  Google Scholar 

  10. D. Beece, L. Eisenstein, H. Frauenfelder, D. Good, M.C. Marden, L. Reinisch, A.H. Reynolds, L.B. Sorensen, K.T. Yue, Solvent Viscosity and protein dynamics. Biochemistry 19, 5147–5157 (1980)

    Article  Google Scholar 

  11. E.Z. Eisenmesser, O. Millet, W. Labeikovsky, D.M. Korzhnev, M. Wolf-Watz, D.A. Bosco, J.J. Skalicky, L.E. Kay, D. Kern, Intrinsic dynamics of an enzyme underlies catalysis. Nature 438, 117–121 (2005)

    Article  ADS  Google Scholar 

  12. S. Hecht, J.M.J. Frechet, Dendritic encapsulation of function: applying nature’s site isolation principle from biomimetics to materials science. Angew. Chem.-Int. Ed. 40, 74–91 (2001)

    Article  Google Scholar 

  13. T.J. Yu, Y. Zeng, J.P. Chen, Y.Y. Li, G.Q. Yang, Y. Li, Exceptional dendrimer-based mimics of diiron hydrogenase for the photochemical production of hydrogen. Angew. Chem.-Int. Ed. 52, 5631–5635 (2013)

    Article  Google Scholar 

  14. M.L. Singleton, J.H. Reibenspies, M.Y. Darensbourg, A cyclodextrin host/guest approach to a hydrogenase active site biomimetic cavity. J. Am. Chem. Soc. 132, 8870–8871 (2010)

    Article  Google Scholar 

  15. P.A. Eckert, K.J. Kubarych, Dynamic flexibility of hydrogenase active site models studied with 2D-IR spectroscopy. J. Phys. Chem. A 121, 608–615 (2017)

    Article  Google Scholar 

  16. M.G.I. Galinato, C.M. Whaley, N. Lehnert, Vibrational analysis of the model complex mu-edt [Fe(CO)3]2 and comparison to iron-only hydrogenase: the activation scale of hydrogenase model systems. Inorg. Chem. 49, 3201–3215 (2010)

    Article  Google Scholar 

  17. A.I. Stewart, I.P. Clark, M. Towrie, S.K. Ibrahim, A.W. Parker, C.J. Pickett, N.T. Hunt, Structure and vibrational dynamics of model compounds of the FeFe-hydrogenase enzyme system via ultrafast two-dimensional infrared spectroscopy. J. Phys. Chem. B 112, 10023–10032 (2008)

    Article  Google Scholar 

  18. S. Kaziannis, J.A. Wright, M. Candelaresi, R. Kania, G.M. Greetham, A.W. Parker, C.J. Pickett, N.T. Hunt, The role of CN and CO ligands in the vibrational relaxation dynamics of model compounds of the [FeFe]-hydrogenase enzyme. Phys. Chem. Chem. Phys. 13, 10295–10305 (2011)

    Article  Google Scholar 

  19. G.M. Bonner, A.R. Ridley, S.K. Ibrahim, C.J. Pickett, N.T. Hunt, Probing the effect of the solution environment on the vibrational dynamics of an enzyme model system with ultrafast 2D-IR spectroscopy. Faraday Discuss. 145, 429–442 (2010)

    Article  ADS  Google Scholar 

  20. A.R. Ridley, A.I. Stewart, K. Adamczyk, H.N. Ghosh, B. Kerkeni, Z.X. Guo, E.T.J. Nibbering, C.J. Pickett, N.T. Hunt, Multiple-timescale photoreactivity of a model compound related to the active site of FeFe-hydrogenase. Inorg. Chem. 47, 7453–7455 (2008)

    Article  Google Scholar 

  21. S. Kaziannis, S. Santabarbara, J.A. Wright, G.M. Greetham, M. Towrie, A.W. Parker, C.J. Pickett, N.T. Hunt, Femtosecond to microsecond photochemistry of a FeFe hydrogenase enzyme model compound. J. Phys. Chem. B 114, 15370–15379 (2010)

    Article  Google Scholar 

  22. A.I. Stewart, J.A. Wright, G.M. Greetham, S. Kaziannis, S. Santabarbara, M. Towrie, A.W. Parker, C.J. Pickett, N.T. Hunt, Determination of the photolysis products of FeFe hydrogenase enzyme model systems using ultrafast multidimensional infrared spectroscopy. Inorg. Chem. 49, 9563–9573 (2010)

    Article  Google Scholar 

  23. P.W.J.M. Frederix, R. Kania, J.A. Wright, D.A. Lamprou, R.V. Ulijn, C.J. Pickett, N.T. Hunt, Encapsulating [FeFe]-hydrogenase model compounds in peptide hydrogels dramatically modifies stability and photochemistry. Dalton Trans. 41, 13112–13119 (2012)

    Article  Google Scholar 

  24. R. Kania, P.W.J.M. Frederix, J.A. Wright, R.V. Ulijn, C.J. Pickett, N.T. Hunt, Solution-phase photochemistry of a [FeFe] hydrogenase model compound: evidence of photoinduced isomerisation. J. Chem. Phys. 136, 044521 (2012)

    Article  ADS  Google Scholar 

  25. P. Frederix, K. Adamczyk, J.A. Wright, T. Tuttle, R.V. Ulijn, C.J. Pickett, N.T. Hunt, Investigation of the ultrafast dynamics occurring during unsensitized photocatalytic H2 evolution by an FeFe-hydrogenase subsite analogue. Organometallics 33, 5888–5896 (2014)

    Article  Google Scholar 

  26. R. Fritzsch, O. Brady, E. Adair, J.A. Wright, C.J. Pickett, N.T. Hunt, Encapsulating subsite analogues of the [FeFe]-hydrogenases in micelles enables direct water interactions. J. Phys. Chem. Lett. 7, 2838–2843 (2016)

    Article  Google Scholar 

  27. N.T. Hunt, J.A. Wright, C. Pickett, Detection of transient intermediates generated from subsite analogues of FeFe hydrogenases. Inorg. Chem. 55, 399–410 (2016)

    Article  Google Scholar 

  28. S. Garrett-Roe, F. Perakis, F. Rao, P. Hamm, Three-dimensional infrared spectroscopy of isotope-substituted liquid water reveals heterogeneous dynamics. J. Phys. Chem. B 115, 6976–6984 (2011)

    Article  Google Scholar 

  29. S. Garrett-Roe, P. Hamm, What can we learn from three-dimensional infrared spectroscopy? Acc. Chem. Res. 42, 1412–1422 (2009)

    Article  Google Scholar 

  30. R.L. Meyer, A.D. Zhandosova, T.M. Biser, E.J. Heilweil, C.J. Stromberg, Photochemical dynamics of a trimethyl-phosphine derivatized FeFe-hydrogenase model compound. Chem. Phys. 512, 135–145 (2018)

    Article  Google Scholar 

  31. B.W. Caplins, J.P. Lomont, S.C. Nguyen, C.B. Harris, Vibrational cooling dynamics of a FeFe-hydrogenase mimic probed by time-resolved infrared spectroscopy. J. Phys. Chem. A 118, 11529–11540 (2014)

    Article  Google Scholar 

  32. J.L. Bingaman, C.L. Kohnhorst, G.A. Van Meter, B.A. McElroy, E.A. Rakowski, B.W. Caplins, T.A. Gutowski, C.J. Stromberg, C.E. Webster, E.J. Heilweil, Time-resolved vibrational spectroscopy of FeFe-hydrogenase model compounds. J. Phys. Chem. A 116, 7261–7271 (2012)

    Article  Google Scholar 

  33. C.J. Stromberg, E.J. Heilweil, Ultrafast photodynamics of cyano-functionalized FeFe hydrogenase model compounds. J. Phys. Chem. A 122, 4023–4030 (2018)

    Article  Google Scholar 

  34. M. Johnson, J. Thuman, R.G. Letterman, C.J. Stromberg, C.E. Webster, E.J. Heilweil, Time-resolved infrared studies of a trimethylphosphine model derivative of FeFe-hydrogenase. J. Phys. Chem. B 117, 15792–15803 (2013)

    Article  Google Scholar 

  35. P. Li, S. Amirjalayer, F. Hartl, M. Lutz, B. de Bruin, R. Becker, S. Woutersen, J.N.H. Reek, Direct probing of photoinduced electron transfer in a self-assembled biomimetic 2Fe2S-hydrogenase complex using ultrafast vibrational spectroscopy. Inorg. Chem. 53, 5373–5383 (2014)

    Article  Google Scholar 

  36. R. Becker, S. Amirjalayer, P. Li, S. Woutersen, J.N.H. Reek, An iron-iron hydrogenase mimic with appended electron reservoir for efficient proton reduction in aqueous media. Sci. Adv. 2, e1501014 (2016)

    Article  ADS  Google Scholar 

  37. E.J. Lyon, I.P. Georgakaki, J.H. Reibenspies, M.Y. Darensbourg, Coordination sphere flexibility of active-site models for Fe-only hydrogenase: studies in intra- and intermolecular diatomic ligand exchange. J. Am. Chem. Soc. 123, 3268–3278 (2001)

    Article  Google Scholar 

  38. A.D. Hill, M.C. Zoerb, S.C. Nguyen, J.P. Lomont, M.A. Bowring, C.B. Harris, Determining equilibrium fluctuations using temperature-dependent 2D-IR. J. Phys. Chem. B 117, 15346–15355 (2013)

    Article  Google Scholar 

  39. I.A. Nilsen, D.G. Osborne, A.M. White, J.M. Anna, K.J. Kubarych, Monitoring equilibrium reaction dynamics of a nearly barrierless molecular rotor using ultrafast vibrational echoes. J. Chem. Phys. 141, 134313 (2014)

    Article  ADS  Google Scholar 

  40. J.M. Anna, J.T. King, K.J. Kubarych, Multiple structures and dynamics of [CpRu(CO)2]2 and [CpFe(CO)2]2 in solution revealed with two-dimensional infrared spectroscopy. Inorg. Chem. 50, 9273–9283 (2011)

    Article  Google Scholar 

  41. J.T. King, J.M. Anna, K.J. Kubarych, Solvent-hindered intramolecular vibrational redistribution. Phys. Chem. Chem. Phys. 13, 5579–5583 (2011)

    Article  Google Scholar 

  42. C.A. Tooley, S. Pazicni, E.B. Berda, Toward a tunable synthetic [FeFe] hydrogenase mimic: single-chain nanoparticles functionalized with a single diiron cluster. Polym. Chem. 6, 7646–7651 (2015)

    Article  Google Scholar 

  43. J.X. Jian, Q. Liu, Z.J. Li, F. Wang, X.B. Li, C.B. Li, B. Liu, Q.Y. Meng, B. Chen, K. Feng, C.H. Tung, L.Z. Wu, Chitosan confinement enhances hydrogen photogeneration from a mimic of the diiron subsite of [FeFe]-hydrogenase. Nat. Commun. 4, 2695 (2013)

    Article  ADS  Google Scholar 

  44. Y. Sano, A. Onoda, T. Hayashi, A hydrogenase model system based on the sequence of cytochrome c: photochemical hydrogen evolution in aqueous media. Chem. Commun. 47, 8229–8231 (2011)

    Article  Google Scholar 

  45. X.Q. Li, M. Wang, D.H. Zheng, K. Han, J.F. Dong, L.C. Sun, Photocatalytic H2 production in aqueous solution with host-guest inclusions formed by insertion of an FeFe-hydrogenase mimic and an organic dye into cyclodextrins. Energy Environ. Sci. 5, 8220–8224 (2012)

    Article  Google Scholar 

  46. M. De Rosa, P. La Manna, C. Talotta, A. Soriente, C. Gaeta, P. Neri, Supramolecular organocatalysis in water mediated by macrocyclic compounds. Fronti. Chem. 6 (2018)

    Google Scholar 

  47. H.B. Gray, J.R. Winkler, Electron transfer in proteins. Annu. Rev. Biochem. 65, 537–561 (1996)

    Article  Google Scholar 

  48. D. Laage, T. Elsaesser, J.T. Hynes, Water dynamics in the hydration shells of biomolecules. Chem. Rev. 117, 10694–10725 (2017)

    Article  Google Scholar 

  49. V.P. Roy, K.J. Kubarych, Interfacial hydration dynamics in cationic micelles using 2D-IR and NMR. J. Phys. Chem. B 121, 9621–9630 (2017)

    Article  Google Scholar 

  50. S. Pullen, H.H. Fei, A. Orthaber, S.M. Cohen, S. Ott, Enhanced photochemical hydrogen production by a molecular diiron catalyst incorporated into a metal-organic framework. J. Am. Chem. Soc. 135, 16997–17003 (2013)

    Article  Google Scholar 

  51. J. Nishida, A. Tamimi, H.H. Fei, S. Pullen, S. Ott, S.M. Cohen, M.D. Fayer, Structural dynamics inside a functionalized metal-organic framework probed by ultrafast 2D IR spectroscopy. Proc. Natl. Acad. Sci. USA 111, 18442–18447 (2014)

    Article  ADS  Google Scholar 

  52. P.A. Eckert, K.J. Kubarych, Solvent quality controls macromolecular structural dynamics of a dendrimeric hydrogenase model. J. Phys. Chem. B 122, 12154–12163 (2018)

    Article  Google Scholar 

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Acknowledgements

Our research on hydrogenase models is supported by the National Science Foundation (CHE–1300239 and CHE-1565795).

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Correspondence to Kevin J. Kubarych .

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Eckert, P.A., Kubarych, K.J. (2019). Ultrafast Spectroscopy of Hydrogenase Enzyme Models. In: Cho, M. (eds) Coherent Multidimensional Spectroscopy. Springer Series in Optical Sciences, vol 226. Springer, Singapore. https://doi.org/10.1007/978-981-13-9753-0_11

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