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Transferring the entatic-state principle to copper photochemistry

Nature Chemistry volume 10, pages 355–362 (2018)Cite this article

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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.

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References

  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).

    CAS  PubMed  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    Google Scholar 

  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).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

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

    Google Scholar 

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

    CAS  Google Scholar 

  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).

    Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  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).

    Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  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).

    CAS  Google Scholar 

  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).

    Google Scholar 

  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).

    CAS  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  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).

    CAS  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  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).

    CAS  PubMed  PubMed Central  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  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).

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  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).

    CAS  Google Scholar 

  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).

    Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  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).

    CAS  Google Scholar 

  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).

    CAS  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

  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).

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  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).

    CAS  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  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).

    CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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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.

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Authors and Affiliations

  1. Institute of Nanostructure and Solid State Physics, University of Hamburg, Hamburg, 22761, Germany

    B. Dicke, B. Grimm-Lebsanft, F. Biebl, D. Rukser, M. Naumova, M. Biednov, G. Neuber, A. Wetzel & M. Rübhausen

  2. Center for Free-Electron Laser Science (CFEL), Luruper Chaussee 149, Hamburg, 22761, Germany

    B. Dicke, B. Grimm-Lebsanft, F. Biebl, D. Rukser, M. Biednov, G. Neuber, A. Wetzel, K. R. Beyerlein, H. N. Chapman & M. Rübhausen

  3. Institute for Inorganic Chemistry, RWTH Aachen University, Aachen, 52074, Germany

    A. Hoffmann, J. Stanek & S. Herres-Pawlis

  4. Institute for BioMolecular Optics and Center for Integrated Protein Science (CIPSM), Ludwig-Maximilians-Universität Munich, Oettingenstraße 67, Munich, 80538, Germany

    M. S. Rampp, B. Maerz, S. M. Hofmann & W. Zinth

  5. Deutsches Elektronensynchrotron (DESY), Notkestraße 85, Hamburg, 22607, Germany

    D. Göries, P. Roedig, A. Meents & H. N. Chapman

  6. Department of Chemistry, University of Paderborn, Paderborn, 33098, Germany

    M. Naumova

  7. Department of Cell and Molecular Biology, Laboratory of Molecular Biophysics, Uppsala University, Husargatan 3 (Box 596), Uppsala, SE-751 24, Sweden

    J. Bielecki & J. Andreasson

  8. European XFEL, Holzkoppel 4, Schenefeld, 22869, Germany

    J. Bielecki & C. Bressler

  9. ELI Beamlines, Institute of Physics, Czech Academy of Science, Na Slovance 2, Prague, 182 21, Czech Republic

    J. Andreasson

  10. Department of Physics, Condensed Matter Physics, Chalmers University of Technology, Göteborg, Sweden

    J. Andreasson

  11. Department of Physics, Technical University of Denmark, Fysikvej 307, Kongens Lyngby, 2800, Denmark

    C. Bressler

  12. The Hamburg Center for Ultrafast Imaging, Universität Hamburg, Luruper Chaussee 149, Hamburg, 22761, Germany

    C. Bressler

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  1. B. Dicke
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Contributions

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.

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Correspondence to W. Zinth, 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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