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Experimental evidence for ultrafast intermolecular relaxation processes in hydrated biomolecules


Cell and gene damage caused by ionizing radiation has been studied for many years. It is accepted that DNA lesions (single- and double-strand breaks, for example) are induced by secondary species such as radicals, ions and the abundant low-energy secondary electrons generated by the primary radiation. Particularly harmful are dense ionization clusters of several ionization processes within a volume typical for the biomolecular system. Here we report the observation of a damage mechanism in the form of a non-local autoionizing process called intermolecular Coulombic decay (ICD). It directly involves DNA constituents or other organic molecules in an aqueous environment. The products are two energetic ions and three reactive secondary electrons that can cause further damage in their vicinity. Hydrogen-bonded complexes that consist of one tetrahydrofuran (THF) molecule—a surrogate of deoxyribose in the DNA backbone—and one water molecule are used as a model system. After electron impact ionization of the water molecule in the inner-valence shell the vacancy is filled by an outer-valence electron. The released energy is transferred across the hydrogen bridge and leads to ionization of the neighbouring THF molecule. This energy transfer from water to THF is faster than the otherwise occurring intermolecular proton transfer. The signature of the ICD reaction is identified in triple-coincidence measurements of both ions and one of the final state electrons. These results could improve the understanding of radiation damage in biological tissue.

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Fig. 1: Schematic representation of ICD of an inner-valence vacancy in a hydrogen-bonded THF–water dimer.
Fig. 2: Measured correlation map between two fragment ions.
Fig. 3: Measured kinetic energy distributions of the fragment ions and electrons.
Fig. 4: Projectile energy loss distributions.

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

    Article  ADS  Google Scholar 

  2. Öhrwall, G. et al. Femtosecond interatomic Coulombic decay in free neon clusters: Large lifetime differences between surface and bulk. Phys. Rev. Lett. 93, 173401 (2004).

    Article  ADS  Google Scholar 

  3. Schnorr, K. et al. Time-resolved measurement of interatomic Coulombic decay in Ne2. Phys. Rev. Lett. 111, 093402 (2013).

    Article  ADS  Google Scholar 

  4. Trinter, F. et al. Evolution of interatomic Coulombic decay in the time domain. Phys. Rev. Lett. 111, 093401 (2013).

    Article  ADS  Google Scholar 

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

    Article  ADS  Google Scholar 

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

    Article  ADS  Google Scholar 

  7. O’Keeffe, P. et al. The role of the partner atom and resonant excitation energy in interatomic Coulombic decay in rare gas dimers. J. Phys. Chem. Lett. 4, 1797–1801 (2013).

    Article  Google Scholar 

  8. Trinter, F. et al. Resonant Auger decay driving intermolecular Coulombic decay in molecular dimers. Nature 505, 664–666 (2014).

    Article  ADS  Google Scholar 

  9. Iskandar, W. et al. Interatomic Coulombic decay as a new source of low energy electrons in slow ion-dimer collisions. Phys. Rev. Lett. 114, 033201 (2015).

    Article  ADS  Google Scholar 

  10. Nagaya, al. Interatomic Coulombic decay cascades in multiply excited neon clusters. Nat. Commun. 7, 13477 (2016).

    Article  ADS  Google Scholar 

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

    Article  Google Scholar 

  12. Mucke, M. et al. A hitherto unrecognized source of low-energy electrons in water. Nat. Phys. 6, 143–146 (2010).

    Article  Google Scholar 

  13. 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  ADS  Google Scholar 

  14. Thürmer, S. et al. On the nature and origin of dicationic, charge-separated species formed in liquid water on X-ray irradiation. Nat. Chem. 5, 590–596 (2013).

    Article  Google Scholar 

  15. Boudaïffa, B., Cloutier, P., Hunting, D., Huels, M., & Sanche, L. Resonant formation of DNA strand breaks by low-energy (3 to 20 eV) electrons. Science 287, 1658–1660 2000).

    Article  ADS  Google Scholar 

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

    Article  Google Scholar 

  17. Alizadeh, E., Orlando, T. M. & Sanche, L. Biomolecular damage induced by ionizing radiation: The direct and indirect effects of low-energy electrons on DNA. Ann. Rev. Phys. Chem. 66, 379–398 (2015).

    Article  ADS  Google Scholar 

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

    Article  Google Scholar 

  19. Jahnke., T. Interatomic and intermolecular Coulombic decay: the coming of age story. J. Phys. B 48, 082001 (2015).

    Article  ADS  Google Scholar 

  20. 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  Google Scholar 

  21. Auffinger, P., & Westhof, E. Water and ion binding around RNA and DNA (C,G) oligomers. J. Mol. Biol. 300, 1113–1131 2000).

    Article  Google Scholar 

  22. Pimblott, S. M. & LaVerne, J. A. Production of low-energy electrons by ionizing radiation. Rad. Phys. Chem. 76, 1244–1247 (2007).

    Article  ADS  Google Scholar 

  23. Ren, X. et al. An (e, 2e + ion) study of low-energy electron-impact ionization and fragmentation of tetrahydrofuran with high mass and energy resolutions. J. Chem. Phys. 141, 134314 (2014).

    Article  ADS  Google Scholar 

  24. Ullrich, J. et al. Recoil-ion and electron momentum spectroscopy: reaction-microscopes. Rep. Prog. Phys. 66, 1463 (2003).

    Article  ADS  Google Scholar 

  25. Ren, X., Jabbour Al Maalouf, E., Dorn, A. & Denifl, S. Direct evidence of two interatomic relaxation mechanisms in argon dimers ionized by electron impact. Nat. Commun. 7, 11093 (2016).

    Article  ADS  Google Scholar 

  26. Fuss, M. et al. Electron-scattering cross sections for collisions with tetrahydrofuran from 50 to 5000 eV. Phys. Rev. A. 80, 052709 (2009).

    Article  ADS  Google Scholar 

  27. Collin, J. E. & Conde-Caprace, G. Ionization and dissociation of cyclic ethers by electron impact. Int. J. Mass. Spec. Ion. Phys. 1, 213 (1968).

    Article  ADS  Google Scholar 

  28. Mayer, P. M. et al. Does tetrahydrofuran ring open upon ionization and dissociation? A TPES and TPEPICO investigation. J. Phys. Chem. A 113, 10923 (2009).

    Article  Google Scholar 

  29. Yukikazu, I. & Mason, N. Cross sections for electron collisions with water molecules. J. Phys. Chem. Ref. Dat. 34, 1 (2005).

    Article  ADS  Google Scholar 

  30. Ning, C. G. et al. Experimental and theoretical electron momentum spectroscopic study of the valence electronic structure of tetrahydrofuran under pseudorotation. J. Phys. Chem. A 112, 11078–11087 (2008).

    Article  Google Scholar 

  31. Montenegro, E., Scully, S., Wyer, J. A., Senthil, V. & Shah, M. Evaporation, fission and auto-dissociation of doubly charged water. J. Elec. Spec. Rel. Phen. 155, 81–85 (2007).

    Article  Google Scholar 

  32. Tan, K. H., Brion, C. E., van der Leeuw, Ph. E. & van der Wiel, M. J. Absolute oscillator strengths (10-60 eV) for the photoabsorption, photoionisation and fragmentation of H2O. Chem. Phys. 29, 299–309 (1978).

    Article  Google Scholar 

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We thank A. I. Kuleff and L. S. Cederbaum as well as W. Y. Baek, V. Dangendorf and H. Rabus for stimulating discussions. X.R. is grateful for support from Deutsche Forschungsgemeinschaft (DFG) project no. RE 2966/3-1 and from the Thousand Youth Talents Program in China. E.W. acknowledges a fellowship from the Alexander von Humboldt Foundation. A.D.S and A.B.T. acknowledge the Ministry of Education and Science of the Russian Federation (grant no. 4.1671.2017/4.6). K.G. acknowledges financial support from DFG (FOR 1789).

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X.R. and A.D. conceived, designed and performed the experiments, and analysed the data. E.W., X.R. and A.D. carried out the molecular dynamics simulations. A.D.S, A.B.T. and K.G. conducted the calculations for ionization potentials. X.R., A.D.S. and A.D. wrote the manuscript. All authors discussed the results and commented on the manuscript.

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Correspondence to Xueguang Ren or Alexander Dorn.

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Supplementary Figs. 1–3, Supplementary References

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Ren, X., Wang, E., Skitnevskaya, A.D. et al. Experimental evidence for ultrafast intermolecular relaxation processes in hydrated biomolecules. Nature Phys 14, 1062–1066 (2018).

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