Transferring the entatic-state principle to copper photochemistry

Abstract

The entatic state denotes a distorted coordination geometry of a complex from its typical arrangement that generates an improvement to its function. The entatic-state principle has been observed to apply to copper electron-transfer proteins and it results in a lowering of the reorganization energy of the electron-transfer process. It is thus crucial for a multitude of biochemical processes, but its importance to photoactive complexes is unexplored. Here we study a copper complex—with a specifically designed constraining ligand geometry—that exhibits metal-to-ligand charge-transfer state lifetimes that are very short. The guanidine–quinoline ligand used here acts on the bis(chelated) copper(I) centre, allowing only small structural changes after photoexcitation that result in very fast structural dynamics. The data were collected using a multimethod approach that featured time-resolved ultraviolet–visible, infrared and X-ray absorption and optical emission spectroscopy. Through supporting density functional calculations, we deliver a detailed picture of the structural dynamics in the picosecond-to-nanosecond time range.

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Figure 1: Model complexes for the entatic state and their spectroscopic features.
Figure 2: Time-resolved UV/vis and infrared spectra of compound 1.
Figure 3: Schematic representation of the involved states.
Figure 4: Time-resolved X-ray absorption data.
Figure 5: Visualization of the ‘entatic’ coordinates for the optical excitation of compound 1.

References

  1. 1

    Vallee, B. L. & Williams, R. J. P. Metalloenzymes: the entactic nature of their active sites. Proc. Natl Acad. Sci. USA 59, 498–505 (1968).

  2. 2

    Williams, R. J. P. Energised (entatic) states of groups and of secondary structures in proteins and metalloproteins. Eur. J. Biochem. 234, 363–381 (1995).

  3. 3

    Williams, R. J. P. Catalysis by metallo-enzymes: the entatic state. Inorg. Chim. Acta Rev. 5, 137–155 (1971).

  4. 4

    Gray, H. B. & Malmström, B. G. Long-range electron transfer in multisite metalloproteins. Biochemistry 28, 7499–7505 (1989).

  5. 5

    Malmström, B. G. Rack-induced bonding in blue-copper proteins. Eur. J. Biochem. 223, 711–718 (1994).

  6. 6

    Comba, P. Strains and stresses in coordination compounds. Coord. Chem. Rev. 182, 343–371 (1999).

  7. 7

    Lancaster, K. M., DeBeer George, S., Yokoyama, K., Richards, J. H. & Gray, H. B. Type-zero copper proteins. Nat. Chem. 1, 711–715 (2009).

  8. 8

    Comba, P. et al. A bispidine iron(IV)–oxo complex in the entatic state. Angew. Chem. Int. Ed. 55, 11129–11133 (2016).

  9. 9

    Comba, P. Coordination compounds in the entatic state. Coord. Chem. Rev. 200–202, 217–245 (2000).

  10. 10

    Hoffmann, A. et al. Catching an entatic state—a pair of copper complexes. Angew. Chem. Int. Ed. 53, 299–304 (2014).

  11. 11

    Mara, M. W., Fransted, K. A. & Chen, L. X. Interplays of excited state structures and dynamics in copper(I) diimine complexes: implications and perspectives. Coord. Chem. Rev. 282–283, 2–18 (2015).

  12. 12

    Hua, L., Iwamura, M., Takeuchi, S. & Tahara, T. The substituent effect on the MLCT excited state dynamics of Cu(I) complexes studied by femtosecond time-resolved absorption and observation of coherent nuclear wavepacket motion. Phys. Chem. Chem. Phys. 17, 2067–2077 (2015).

  13. 13

    Iwamura, M., Takeuchi, S. & Tahara, T. Ultrafast excited-state dynamics of copper(I) complexes. Acc. Chem. Res. 48, 782–791 (2015).

  14. 14

    Solomon, E. I. et al. Copper active sites in biology. Chem. Rev. 114, 3659–3853 (2014).

  15. 15

    Solomon, E. I. & Hadt, R. G. Recent advances in understanding blue copper proteins. Coord. Chem. Rev. 255, 774–789 (2011).

  16. 16

    Choi, M. & Davidson, V. L. Cupredoxins—a study of how proteins may evolve to use metals for bioenergetic processes. Metallomics 3, 140–151 (2011).

  17. 17

    Comba, P. & Schiek, W. Fit and misfit between ligands and metal ions. Coord. Chem. Rev. 238–239, 21–29 (2003).

  18. 18

    Rorabacher, D. B. Electron transfer by copper centers. Chem. Rev. 104, 651–697 (2004).

  19. 19

    Gray, H. B., Malmström, B. G. & Williams, R. J. P. Copper coordination in blue proteins. J. Biol. Inorg. Chem. 5, 551–559 (2000).

  20. 20

    Bergmann, L., Hedley, G. J., Baumann, T., Bräse, S. & Samuel, I. D. W. Direct observation of intersystem crossing in a thermally activated delayed fluorescence copper complex in the solid state. Sci. Adv. 2, 1–6 (2016).

  21. 21

    Lockard, J. V. et al. Influence of ligand substitution on excited state structural dynamics in Cu(I) bisphenanthroline complexes. J. Phys. Chem. B 114, 14521–14527 (2010).

  22. 22

    Kohler, L. et al. Synthesis, structure, ultrafast kinetics, and light-induced dynamics of CuHETPHEN chromophores. Dalton Trans. 45, 9871–9883 (2016).

  23. 23

    Hancock, R. D. & Martell, A. E. Ligand design for selective complexation of metal ions in aqueous solution. Chem. Rev. 89, 1875–1914 (1989).

  24. 24

    Knapp, S. et al. Nearly tetrahedral 1:2 complexes of copper(I), copper(II), nickel(II), cobalt(II), and zinc(II) with 2,2′-bis(2-imidazolyl)biphenyl. J. Am. Chem. Soc. 109, 1882–1883 (1987).

  25. 25

    Comba, P., Kerscher, M. & Roodt, A. Slow electron self-exchange in spite of a small inner-sphere reorganisation energy—the electron-transfer properties of a copper complex with a tetradentate bispidine ligand. Eur. J. Inorg. Chem. 23, 4640–4645 (2004).

  26. 26

    Xie, B., Elder, T., Wilson, L. J. & Stanbury, D. M. Internal reorganization energies for copper redox couples: the slow electron-transfer reactions of the [CuII/I(bib)2]2+/+ couple. Inorg. Chem. 38, 12–19 (1999).

  27. 27

    Chaka, G. et al. A definitive example of a geometric ‘entatic state’ effect: electron-transfer kinetics for a copper(II/I) complex involving a quinquedentate macrocyclic trithiaether–bipyridine ligand. J. Am. Chem. Soc. 129, 5217–5227 (2007).

  28. 28

    Garcia, L. et al. Entasis through hook-and-loop fastening in a glycoligand with cumulative weak forces stabilizing CuI. J. Am. Chem. Soc. 137, 1141–1146 (2015).

  29. 29

    Dahl, E. W. & Szymczak, N. K. Hydrogen bonds dictate the coordination geometry of copper: characterization of a square-planar copper(I) complex. Angew. Chem. Int. Ed. 55, 3101–3105 (2016).

  30. 30

    Bucher, D. B., Pilles, B. M., Carell, T. & Zinth, W. Charge separation and charge delocalization identified in long-living states of photoexcited DNA. Proc. Natl Acad. Sci. USA 111, 4369–4374 (2014).

  31. 31

    Vos, M. H. & Liebl, U. Time-resolved infrared spectroscopic studies of ligand dynamics in the active site from cytochrome C oxidase. Biochim. Biophys. Acta 1847, 79–85 (2015).

  32. 32

    Poynton, F. E. et al. Direct observation by time-resolved infrared spectroscopy of the bright and the dark excited states of the [Ru(phen)2(dppz)]2+ light-switch compound in solution and when bound to DNA. Chem. Sci. 7, 3075–3084 (2016).

  33. 33

    Hall, J. P. et al. Monitoring one-electron photo-oxidation of guanine in DNA crystals using ultrafast infrared spectroscopy. Nat. Chem. 7, 961–967 (2015).

  34. 34

    Gawelda, W. et al. Electronic and molecular structure of photoexcited [RuII(bpy)3]2+ probed by picosecond X-ray absorption spectroscopy. J. Am. Chem. Soc. 128, 5001–5009 (2006).

  35. 35

    Bressler, C. et al. Towards structural dynamics in condensed chemical systems exploiting ultrafast time-resolved X-ray absorption spectroscopy. J. Chem. Phys. 116, 2955–2966 (2002).

  36. 36

    Bressler, C. & Chergui, M. Molecular structural dynamics probed by ultrafast X-ray absorption spectroscopy. Annu. Rev. Phys. Chem. 61, 263–282 (2010).

  37. 37

    Mara, M. W. et al. Effects of electronic and nuclear interactions on the excited-state properties and structural dynamics of copper(I) diimine complexes. J. Phys. Chem. B 117, 1921–1931 (2013).

  38. 38

    Chen, L. X. Probing transient molecular structures in photochemical processes using laser-initiated time-resolved X-ray absorption spectroscopy. Annu. Rev. Phys. Chem. 56, 221–254 (2005).

  39. 39

    Chen, L. X. et al. MLCT state structure and dynamics of a copper(I) diimine complex characterized by pump–probe X-ray and laser spectroscopies and DFT calculations. J. Am. Chem. Soc. 125, 7022–7034 (2003).

  40. 40

    Chen, L. X. Taking snapshots of photoexcited molecules in disordered media by using pulsed synchrotron X-rays. Angew. Chem. Int. Ed. 43, 2886–2905 (2004).

  41. 41

    Göries, D. et al. Time-resolved pump and probe X-ray absorption fine structure spectroscopy at beamline P11 at PETRA III. Rev. Sci. Instrum. 87, 53116 (2016).

  42. 42

    Jesser, A., Rohrmüller, M., Schmidt, W. G. & Herres-Pawlis, S. Geometrical and optical benchmarking of copper guanidine–quinoline complexes: insights from TD-DFT and many-body perturbation theory. J. Comput. Chem. 35, 1–17 (2014).

  43. 43

    Chaudhuri, J., Kume, S., Jagur-Grodzinski, J. & Szwarc, M. Chemistry of radical anions of heterocyclic aromatics: I. Electron spin resonance and electronic spectra. J. Am. Chem. Soc. 90, 6421–6425 (1968).

  44. 44

    Hamm, P., Ohline, S. M. & Zinth, W. Vibrational cooling after ultrafast photoisomerization of azobenzene measured by femtosecond infrared spectroscopy. J. Chem. Phys. 106, 519–529 (1997).

  45. 45

    Du, L. & Lan, Z. Ultrafast structural flattening motion in photoinduced excited state dynamics of a bis(diimine) copper(I) complex. Phys. Chem. Chem. Phys. 18, 7641–7650 (2016).

  46. 46

    Westre, T. E. et al. A multiplet analysis of Fe K-edge 1s → 3d pre-edge features of iron complexes. J. Am. Chem. Soc. 119, 6297–6314 (1997).

  47. 47

    Rehr, J. J. & Albers, R. C. Theoretical approaches to X-ray absorption fine structure. Rev. Mod. Phys. 72, 621–654 (2000).

  48. 48

    Stern, E. A. Theory of the extended X-ray-absorption fine structure. Phys. Rev. B 10, 3027–3037 (1974).

  49. 49

    Sayers, D. E., Stern, E. A. & Lytle, F. W. New technique for investigating noncrystalline structures: Fourier analysis of the extended X-ray-absorption fine structure. Phys. Rev. Lett. 27, 1204–1207 (1971).

  50. 50

    Siddique, Z. A., Yamamoto, Y., Ohno, T. & Nozaki, K. Structure-dependent photophysical properties of singlet and triplet metal-to-ligand charge transfer states in copper(I) bis(diimine) compounds. Inorg. Chem. 42, 6366–6378 (2003).

  51. 51

    Cannizzo, A. et al. Femtosecond fluorescence and intersystem crossing in rhenium(I) carbonyl–bipyridine complexes. J. Am. Chem. Soc. 130, 8967–8974 (2008).

  52. 52

    Czerwieniec, R., Leitl, M. J., Homeier, H. H. H. & Yersin, H. Cu(I) complexes—thermally activated delayed fluorescence. Photophysical approach and material design. Coord. Chem. Rev. 325, 2–28 (2016).

  53. 53

    Mara, M. W. et al. Metalloprotein entatic control of ligand–metal bonds quantified by ultrafast X-ray spectroscopy. Science 356, 1276–1280 (2017).

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Acknowledgements

S.H.-P. acknowledges generous funding by the Deutsche Forschungsgemeinschaft (FOR1405 and SFB749, project B10) and M.R. thanks the Bundesministerium für Bildung und Forschung (BMBF VUV-FAST/05K2014 and 05K12GU1) and DFG (FOR1405). Also, W.Z. thanks the SFB749 (project A5) and the Cluster of Excellence ‘Munich-Center for Advanced Photonics’ and ‘Center for Integrated Protein Science (CIPSM)’. This work was supported by the project ELI (Extreme Light Infrastructure) phase 2 (CZ.02.1.01/0.0/0.0/15_008/0000162) from the European Regional Development Fund. J.A. acknowledges funding from the Röntgen Ångström Cluster and the Chalmers Area of Advance Materials Science. C.B. is grateful for funding by the European XFEL, the DFG via SFB925 (TP A4) and the Centre for Ultrafast Imaging. Parts of this research were carried out at beamline P11 at the PETRA III storage ring at DESY, a member of the Helmholtz Association. We thank the DESY beamline scientists B. Reime, A. Burkhardt, S. Panneerselvam and O. Lorbeer for their support. Moreover, we thank the XFEL team members C. Youngman, P. Gessler, A. Beckmann and A. Galler for the efficient integration of the MHz digitizer into our X-ray setup at P11.

Author information

B.D., M.N., M.B., B.G.-L., S.H.-P., A.H., J.S., D.R., A.W. and J.B. performed the transient XAS measurements under the supervision of M.R.; the set-up for the transient XAS measurements was designed and developed by D.G., B.D., P.R. and A.M.; A.M., C.B., B.D., D.G., S.H.-P. and M.R. contributed to the improved data-acquisition technique; B.D. and M.N. analysed the transient XAS data; B.G.-L. performed the time-resolved optical emission experiments under the supervision of M.R.; J.A., F.B., H.N.C., K.R.B. and G.N. participated in the discussions about the data; A.H. and J.S. prepared the samples and A.H. performed the DFT calculations; the interpretation of the theoretical data in relation to the diverse experimental data was done by A.H. and S.H.-P.; M.S.R. and S.M.H. performed the transient infrared measurements under the supervision of W.Z.; B.M. accomplished the transient UV/vis measurements under the supervision of W.Z.; the interpretation of the entire experimental optical and XAS data was delivered by C.B., M.R., S.H.-P. and W.Z.; S.H.-P., W.Z. and M.R. designed the study and wrote the manuscript together with C.B., A.H. and B.D.

Correspondence to W. Zinth or M. Rübhausen or S. Herres-Pawlis.

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Dicke, B., Hoffmann, A., Stanek, J. et al. Transferring the entatic-state principle to copper photochemistry. Nature Chem 10, 355–362 (2018). https://doi.org/10.1038/nchem.2916

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