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On the nature and origin of dicationic, charge-separated species formed in liquid water on X-ray irradiation

Nature Chemistry volume 5, pages 590–596 (2013)Cite this article

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Abstract

To understand the yield and patterns of damage in aqueous condensed matter, including biological systems, it is essential to identify the initial products subsequent to the interaction of high-energy radiation with liquid water. Until now, the observation of several fast reactions induced by energetic particles in water was not possible on their characteristic timescales. Therefore, some of the reaction intermediates involved, particularly those that require nuclear motion, were not considered when describing radiation chemistry. Here, through a combined experimental and theoretical study, we elucidate the ultrafast proton dynamics in the first few femtoseconds after X-ray core-level ionization of liquid water. We show through isotope analysis of the Auger spectra that proton-transfer dynamics occur on the same timescale as electron autoionization. Proton transfer leads to the formation of a Zundel-type intermediate [HO*···H···H2O]+, which further ionizes to form a so-far unnoticed type of dicationic charge-separated species with high internal energy. We call the process proton-transfer mediated charge separation.

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Figure 1: Schematic of the three autoionization mechanisms of core-ionized liquid water considered here.
Figure 2: Auger-electron spectra from normal (blue) and heavy (red) liquid water, together with the absolute intensity difference between the two spectra (black).
Figure 3: Potential energy curves of ionized water dimers.
Figure 4: The main findings of this work summarized in a graphical form.

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References

  1. Seiwert, T. Y., Salama, J. K. & Vokes, E. E. The concurrent chemoradiation paradigm – general principles. Nature Clin. Pract. Oncol. 4, 86–100 (2007).

    Article  CAS  Google Scholar 

  2. Howell, R. W. Auger processes in the 21st century. Int. J. Radiat. Biol. 84, 959–975 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Eschenbrenner, A. et al. Strand breaks induced in plasmid DNA by ultrasoft X-rays: influence of hydration and packing. Int. J. Radiat. Biol. 83, 687–697 (2007).

    Article  CAS  PubMed  Google Scholar 

  4. Wang, C. R., Nguyen, J. & Lu, Q. B. Bond breaks of nucleotides by dissociative electron transfer of nonequilibrium prehydrated electrons: a new molecular mechanism for reductive DNA damage. J. Am. Chem. Soc. 131, 11320–11322 (2009).

    Article  CAS  PubMed  Google Scholar 

  5. Alizadeh, E. & Sanche, L. Precursors of solvated electrons in radiobiological physics and chemistry. Chem. Rev. 112, 5578–5602 (2012).

    Article  CAS  PubMed  Google Scholar 

  6. Weik, M. et al. Specific chemical and structural damage to proteins produced by synchrotron radiation. Proc. Natl Acad. Sci. USA 97, 623–628 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Hatano, Y., Katsumura, Y. & Mozumder, A. Charged Particle and Photon Interactions with Matter: Recent Advances, Applications, and Interfaces (CRC Press, 2010).

    Book  Google Scholar 

  8. Garrett, B. C. et al. Role of water in electron-initiated processes and radical chemistry: issues and scientific advances. Chem. Rev. 105, 355–389 (2005).

    Article  CAS  PubMed  Google Scholar 

  9. Meesungnoen, J. et al. Multiple ionization effects on the yields of HO2/O2− and H2O2 produced in the radiolysis of liquid water with high-LET 12C6+ ions: a Monte-Carlo simulation study. Chem. Phys. Lett. 377, 419–425 (2003).

    Article  CAS  Google Scholar 

  10. Tavernelli, I. et al. Time-dependent density functional theory molecular dynamics simulations of liquid water radiolysis. Chem. Phys. Chem. 9, 2099–2103 (2008).

    Article  CAS  PubMed  Google Scholar 

  11. Gaigeot, M. P. et al. A multi-scale ab initio theoretical study of the production of free radicals in swift ion tracks in liquid water. J. Phys. B 40, 1–12 (2007).

    Article  CAS  Google Scholar 

  12. Cederbaum, L. S., Zobeley, J. & Tarantelli, F. Giant intermolecular decay and fragmentation of clusters. Phys. Rev. Lett. 79, 4778–4781 (1997).

    Article  CAS  Google Scholar 

  13. Müller, I. B. & Cederbaum, L. S. Electronic decay following ionization of aqueous Li+ microsolvation clusters. J. Chem. Phys. 122, 194305 (2005).

    Article  CAS  Google Scholar 

  14. Hergenhahn, U. Interatomic and intermolecular Coulombic decay: the early years. J. Electron Spectrosc. Relat. Phenom. 184, 78–90 (2011).

    Article  CAS  Google Scholar 

  15. Marburger, S., Kugeler, O., Hergenhahn, U. & Möller, T. Experimental evidence for interatomic Coulombic decay in Ne clusters. Phys. Rev. Lett. 90, 203401 (2003).

    Article  CAS  PubMed  Google Scholar 

  16. Jahnke, T. et al. Experimental observation of interatomic Coulombic decay in neon dimers. Phys. Rev. Lett. 93, 163401 (2004).

    Article  CAS  PubMed  Google Scholar 

  17. Hergenhahn, U. Production of low kinetic energy electrons and energetic ion pairs by intermolecular Coulombic decay. Int. J. Radiat. Biol. 88, 871–883 (2012).

    Article  CAS  PubMed  Google Scholar 

  18. Mucke, M. et al. A hitherto unrecognized source of low-energy electrons in water. Nature Phys. 6, 78–81 (2010).

    Article  CAS  Google Scholar 

  19. Schwartz, C. P., Fatehi, S., Saykally, R. J. & Prendergast, D. Importance of electronic relaxation for inter-Coulombic decay in aqueous systems. Phys. Rev. Lett. 105, 198102 (2010).

    Article  CAS  PubMed  Google Scholar 

  20. Lindblad, A. et al. Charge delocalization dynamics of ammonia in different hydrogen bonding environments: free clusters and in liquid water solution. Phys. Chem. Chem. Phys. 11, 1758–1764 (2009).

    Article  CAS  PubMed  Google Scholar 

  21. Stoychev, S. D., Kuleff, A. I. & Cederbaum, L. S. Intermolecular Coulombic decay in small biochemically relevant hydrogen-bonded systems. J. Am. Chem. Soc. 133, 6817–6824 (2011).

    Article  CAS  PubMed  Google Scholar 

  22. Aziz, E. F., Ottosson, N., Faubel, M., Hertel, I. V. & Winter, B. Interaction between liquid water and hydroxide revealed by core-hole de-excitation. Nature 455, 89–91 (2008).

    Article  CAS  PubMed  Google Scholar 

  23. Pokapanich, W. et al. Auger electron spectroscopy as a probe of the solution of aqueous ions. J. Am. Chem. Soc. 131, 7264–7271 (2009).

    Article  CAS  PubMed  Google Scholar 

  24. Pokapanich, W. et al. Ionic-charge dependence of tie intermolecular Coulombic decay time scale for aqueous ions probed by the core-hole clock. J. Am. Chem. Soc. 133, 13430–13436 (2011).

    Article  CAS  PubMed  Google Scholar 

  25. Pokapanich, W. et al. Bond breaking, electron pushing, and proton pulling: active and passive roles in the interaction between aqueous ions and water as manifested in the O1s Auger decay. J. Phys. Chem. B 116, 3–8 (2012).

    Article  CAS  PubMed  Google Scholar 

  26. Ottosson, N., Öhrwall, G. & Björneholm, O. Ultrafast charge delocalization dynamics in aqueous electrolytes: new insights from Auger electron spectroscopy. Chem. Phys. Lett. 543, 1–11 (2012).

    Article  CAS  Google Scholar 

  27. Öhrwall, G. et al. The electronic structure of free water clusters probed by Auger electron spectroscopy. J. Chem. Phys. 123, 054310 (2005).

    Article  CAS  PubMed  Google Scholar 

  28. Stoychev, S. D., Kuleff, A. I. & Cederbaum, L. S. On the intermolecular Coulombic decay of singly and doubly ionized states of water dimer. J. Chem. Phys. 133, 154307 (2010).

    Article  CAS  PubMed  Google Scholar 

  29. Kryzhevoi, N. V. & Cederbaum, L. S. Non local effects in the core ionization and Auger spectra of small ammonia clusters. J. Phys. Chem. B 115, 5441–5447 (2011).

    Article  CAS  PubMed  Google Scholar 

  30. Hjelte, I. et al. Evidence for ultra-fast dissociation of molecular water from resonant Auger spectroscopy. Chem. Phys. Lett. 334, 151–158 (2001).

    Article  CAS  Google Scholar 

  31. Björneholm, O., Nilsson, A., Sandell, A., Hernnas, B. & Martensson, N. Determination of time scales for charge-transfer screening in physisorbed molecules. Phys. Rev. Lett. 68, 1892–1895 (1992).

    Article  PubMed  Google Scholar 

  32. Schnadt, J. et al. Experimental evidence for sub-3-fs charge transfer from an aromatic adsorbate to a semiconductor. Nature 418, 620–623 (2002).

    Article  CAS  PubMed  Google Scholar 

  33. Föhlisch, A. et al. Direct observation of electron dynamics in the attosecond domain. Nature 436, 373–376 (2005).

    Article  CAS  PubMed  Google Scholar 

  34. Odelius, M. et al. Ultrafast core-hole-induced dynamics in water probed by X-ray emission spectroscopy. Phys. Rev. Lett. 94, 227401 (2005).

    Article  CAS  PubMed  Google Scholar 

  35. Fuchs, O. et al. Isotope and temperature effects in liquid water probed by X-ray absorption and resonant X-ray emission spectroscopy. Phys. Rev. Lett. 100, 027801 (2008).

    Article  CAS  PubMed  Google Scholar 

  36. Tokushima, T. et al. High resolution X-ray emission spectroscopy of liquid water: the observation of two structural motifs. Chem. Phys. Lett. 460, 387–400 (2008).

    Article  CAS  Google Scholar 

  37. Odelius, M. Molecular dynamics simulations of fine structure in oxygen K-edge X-ray emission spectra of liquid water and ice. Phys. Rev. B 79, 144204 (2009).

    Article  CAS  Google Scholar 

  38. Ljungberg, M. P., Nilsson, A. & Pettersson, L. G. M. Semiclassical description of nuclear dynamics in X-ray emission of water. Phys. Rev. B 82, 245115 (2010).

    Article  CAS  Google Scholar 

  39. Ljungberg, M. P., Pettersson, L. G. M. & Nilsson, A. Vibrational interference effects in X-ray emission of a model water dimer: implications for the interpretation of the liquid spectrum. J. Chem. Phys. 134, 044513 (2011).

    Article  CAS  PubMed  Google Scholar 

  40. Winter, B., Aziz, E. F., Hergenhahn, U., Faubel, M. & Hertel, I. V. Hydrogen bonds in liquid water studied by photoelectron spectroscopy. J. Chem. Phys. 126, 124504 (2007).

    Article  CAS  PubMed  Google Scholar 

  41. Winter, B., Hergenhahn, U., Faubel, M., Björneholm, O. & Hertel, I. V. Hydrogen bonding in liquid water probed by resonant Auger-electron spectroscopy. J. Chem. Phys. 127, 094501 (2007).

    Article  CAS  PubMed  Google Scholar 

  42. Nordlund, D. et al. Probing the electron delocalization in liquid water and ice at attosecond time scales. Phys. Rev. Lett. 99, 217406 (2007).

    Article  CAS  PubMed  Google Scholar 

  43. Soper, A. K. & Benmore, C. J. Quantum differences between heavy and light water. Phys. Rev. Lett. 101, 065502 (2008).

    Article  CAS  PubMed  Google Scholar 

  44. Winter, B. et al. Full valence band photoemission from liquid water using EUV synchrotron radiation. J. Phys. Chem. A 108, 2625–2632 (2004).

    Article  CAS  Google Scholar 

  45. Nishizawa, K. et al. High-resolution soft X-ray photoelectron spectroscopy of liquid water. Phys. Chem. Chem. Phys. 13, 413–417 (2011).

    Article  CAS  PubMed  Google Scholar 

  46. Barth, S. et al. Valence ionization of water clusters: from isolated molecules to bulk. J. Phys. Chem. A 113, 13519–13527 (2009).

    Article  CAS  PubMed  Google Scholar 

  47. Takahashi, O. et al. Auger decay calculations with core-hole excited-state molecular-dynamics simulations of water. J. Chem. Phys. 124, 064307 (2006).

    Article  CAS  Google Scholar 

  48. Felicissimo, V. C., Guimaraes, F. F., Gel'mukhanov, F., Cesar, A. & Ågren, H. The principles of infrared-X-ray pump-probe spectroscopy. Applications on proton transfer in core-ionized water dimers. J. Chem. Phys. 122, 094319 (2005).

    Article  CAS  PubMed  Google Scholar 

  49. Felicissimo, V. C. et al. A theoretical study of the role of the hydrogen bond on core ionization of the water dimer. Chem. Phys. 312, 311–318 (2005).

    Article  CAS  Google Scholar 

  50. Stia, C. R. et al. Theoretical investigation of the ultrafast dissociation of core-ionized water and uracil molecules immersed in liquid water. Eur. Phys. J. D 60, 77–83 (2010).

    Article  CAS  Google Scholar 

  51. Vendrell, O., Stoychev, S. D. & Cederbaum, L. S. Generation of highly damaging H2O+ radicals by inner valence shell ionization of water. Chem. Phys. Chem. 11, 1006–1009 (2010).

    Article  CAS  PubMed  Google Scholar 

  52. Marsalek, O. et al. Chasing charge localization and chemical reactivity following photoionization in liquid water. J. Chem. Phys. 135, 224510 (2011).

    Article  CAS  PubMed  Google Scholar 

  53. Anicich, V. G. Evaluated biomolecular ion-molecule gas-phase kinetics of positive ion for use in modeling planetary atmosphere, cometary comae, and interstellar clouds. J. Phys. Chem. Ref. Data 22, 1469–1569 (1993).

    Article  CAS  Google Scholar 

  54. Pimblott, S. M. & LaVerne, J. A. Stochastic simulation of the electron radiolysis of water and aqueous solutions. J. Phys. Chem. A 101, 5828–5838 (1997).

    Article  CAS  Google Scholar 

  55. Garrett, B. C. Ions at the air/water interface. Science 303, 1146–1147 (2004).

    Article  CAS  PubMed  Google Scholar 

  56. Jahnke, T. et al. Ultrafast energy transfer between water molecules. Nature Phys. 6, 139–142 (2010).

    Article  CAS  Google Scholar 

  57. Winter, B. & Faubel, M. Photoemission from liquid aqueous solutions. Chem. Rev. 106, 1176–1211 (2006).

    Article  CAS  PubMed  Google Scholar 

  58. Winter, B. Liquid microjet for photoelectron spectroscopy. Nucl. Instrum. Meth. A 601, 139–150 (2009).

    Article  CAS  Google Scholar 

  59. Seidel, R., Thürmer, S. & Winter, B. Photoelectron spectroscopy meets aqueous solution: studies from a vacuum liquid microjet. J. Phys. Chem. Lett. 2, 633–641 (2011).

    Article  CAS  Google Scholar 

  60. MOLPRO, version 2010.1. A package of ab initio programs (University College, Cardiff, 2010).

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Acknowledgements

We thank N. Kryzhevoi and L. S. Cederbaum for stimulating discussions. We acknowledge the support of the Grant agency of the Czech Republic via grants no. P208/10/1724 and P208/11/0161 to P.S., the US National Science Foundation (CHE-0957869) to S.E.B., the Deutsche Forschungsgemeinschaft (DFG) via projects WI 1327/3-1, UH 3060/5-1, and the DFG Research Unit FOR 1789.

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Authors and Affiliations

  1. Helmholtz-Zentrum Berlin für Materialien und Energie, and Berlin Electron Storage Ring Society for Synchrotron Radiation (BESSY), Berlin, 12489, Germany

    Stephan Thürmer & Bernd Winter

  2. Department of Physical Chemistry, Institute of Chemical Technology, Technická 5, Prague, 16628, Czech Republic

    Milan Ončák & Petr Slavíček

  3. FOM Institute AMOLF, Science Park 102, Amsterdam, 1098 XG, The Netherlands

    Niklas Ottosson

  4. Department of Chemistry, University of Southern California, Los Angeles, 90089, California, USA

    Robert Seidel & Stephen E. Bradforth

  5. Max Planck Institute for Plasma Physics, EURATOM Association, Wendelsteinstrasse 1, Greifswald, 17491, Germany

    Uwe Hergenhahn

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Contributions

S.T. and B.W. conceived, designed and performed the experiments, and analysed the data. P.S. and M.O. conducted the calculations and contributed to data interpretation. N.O. and R.S. contributed materials and/or analysis tools. B.W., P.S., S.T., U.H. and S.E.B. co-wrote the paper. All authors discussed the results and commented on the manuscript.

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Correspondence to Petr Slavíček or Bernd Winter.

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Thürmer, S., Ončák, M., Ottosson, N. et al. On the nature and origin of dicationic, charge-separated species formed in liquid water on X-ray irradiation. Nature Chem 5, 590–596 (2013). https://doi.org/10.1038/nchem.1680

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