NCO, a Key Fragment Upon Dissociative Electron Attachment and Electron Transfer to Pyrimidine Bases: Site Selectivity for a Slow Decay Process

  • Filipe Ferreira da Silva
  • Carolina Matias
  • Diogo Almeida
  • Gustavo García
  • Oddur Ingólfsson
  • Helga Dögg Flosadóttir
  • Benedikt Ómarsson
  • Sylwia Ptasinska
  • Benjamin Puschnigg
  • Paul Scheier
  • Paulo Limão-Vieira
  • Stephan Denifl
Research Article


We report gas phase studies on NCO fragment formation from the nucleobases thymine and uracil and their N-site methylated derivatives upon dissociative electron attachment (DEA) and through electron transfer in potassium collisions. For comparison, the NCO production in metastable decay of the nucleobases after deprotonation in matrix assisted laser desorption/ionization (MALDI) is also reported. We show that the delayed fragmentation of the dehydrogenated closed-shell anion into NCO upon DEA proceeds few microseconds after the electron attachment process, indicating a rather slow unimolecular decomposition. Utilizing partially methylated thymine, we demonstrate that the remarkable site selectivity of the initial hydrogen loss as a function of the electron energy is preserved in the prompt as well as the metastable NCO formation in DEA. Site selectivity in the NCO yield is also pronounced after deprotonation in MALDI, though distinctly different from that observed in DEA. This is discussed in terms of the different electronic states subjected to metastable decay in these experiments. In potassium collisions with 1- and 3-methylthymine and 1- and 3-methyluracil, the dominant fragment is the NCO ion and the branching ratios as a function of the collision energy show evidence of extraordinary site-selectivity in the reactions yielding its formation.

Graphical abstract

Key words

NCO anion Electron transfer Negative ion formation Metastable decay DEA Collision dynamics Matrix assisted laser desorption/ionization (MALDI) 



The authors acknowledge support for this work from the FWF, Wien (P-22665) and the European Commission, Brussels. F.F.S. and D.A. acknowledge the Portuguese Foundation for Science and Technology (FCT-MEC) for post-doctoral and post-graduate scholarships SFRH/BPD/68979/2010 and SFRH/BD/61645/2009, respectively. D.A. together with P.L.-V. acknowledge the PEst-OE/FIS/UI0068/2011 and PTDC/FIS-ATO/1832/2012 grants. O.I. acknowledges support from the Icelandic Centre for Research (RANNIS) and the Research Fund of the University of Iceland, and H.D.F. acknowledges a Ph.D. grant from the Eimskip University Fund. G.G. acknowledges support from the Spanish Ministerio de Economia y Productividad (Project FIS2009-10245). This work also forms a part of the EU/ESF COST Actions Electron Controlled Chemical Lithography (ECCL) CM0601, The Chemical Cosmos CM0805, and the Nanoscale Insights into Ion Beam Cancer Therapy (Nano-IBCT) MP1002.

Supplementary material

13361_2013_715_MOESM1_ESM.pdf (3.2 mb)
ESM 1 (PDF 3.22 MB)


  1. 1.
    Boudaïffa, B., Cloutier, P., Hunting, D., Huels, M.A., Sanche, L.: Resonant formation of DNA strand breaks by low-energy (3 to 20 eV) electrons. Science 287, 1658–1660 (2000)CrossRefGoogle Scholar
  2. 2.
    Martin, F., Burrow, P.D., Cai, Z., Cloutier, P., Hunting, D., Sanche, L.: DNA strand breaks induced by 0–4 eV electrons: The role of shape resonances. Phys. Rev. Lett. 93, 068101-1–068101-4 (2004)Google Scholar
  3. 3.
    Alizadeh, E., Sanche, L.: Precursors of solvated electrons in radiobiological physics and chemistry. Chem. Rev. 12, 5578–5602 (2012)CrossRefGoogle Scholar
  4. 4.
    Baccarelli, I., Bald, I., Gianturco, F.A., Illenberger, E., Kopyra, J.: Electron-induced damage of DNA and its components: experiments and theoretical models. Phys. Rep. 508, 1–44 (2011)CrossRefGoogle Scholar
  5. 5.
    Bald, I., Langer, J., Tegeder, P., Ingólfsson, O.: From isolated molecules through clusters and condensates to the building blocks of life. A short tribute to Professor Eugen Illenberger's work in the field of negative ion chemistry. Int. J. Mass Spectrom. 277, 4–25 (2008)CrossRefGoogle Scholar
  6. 6.
    Sanche, L.: Role of secondary low energy electrons in radiobiology and chemoradiation therapy of cancer. Chem. Phys. Lett. 474, 1–6 (2009)CrossRefGoogle Scholar
  7. 7.
    Baccarelli, I., Gianturco, F.A., Scifoni, E., Solov’yov, A.V., Surdutovich, E.: Molecular level assessments of radiation biodamage. Eur. Phys. J. D 60, 1–10 (2010)CrossRefGoogle Scholar
  8. 8.
    Simons, J.: How do low-energy (0.1–2 eV) electrons cause DNA-strand breaks? Acc. Chem. Res. 39, 772–779 (2006)CrossRefGoogle Scholar
  9. 9.
    Gu, J., Leszcynski, J., Schaeffer III, H.F.: Interactions of electrons with bare and hydrated biomolecules: from nucleic acid bases to DNA segments. Chem. Rev. 112, 5603–5640 (2012)CrossRefGoogle Scholar
  10. 10.
    Orlando, T.M., Oh, D., Chen, Y., Aleksandrov, A.B.: Low-energy electron diffraction and induced damage in hydrated DNA. J. Chem. Phys. 128, 195102-1–195102-7 (2008)CrossRefGoogle Scholar
  11. 11.
    Abdoul-Carime, H., Gohlke, S., Illenberger, E.: Site-specific dissociation of DNA bases by slow electrons at early stages of irradiation. Phys. Rev. Lett. 92, 168103-1–168103-4 (2004)CrossRefGoogle Scholar
  12. 12.
    Ptasinska, S., Denifl, S., Grill, V., Märk, T.D., Illenberger, E., Scheier, P.: Bond- and site-selective loss of H- from pyrimidine bases. Phys. Rev. Lett. 95, 093201-1–093201-4 (2005)Google Scholar
  13. 13.
    Ptasinska, S., Denifl, S., Grill, V., Märk, T.D., Scheier, P., Gohlke, S., Huels, M., Illenberger, E.: Bond-selective H-ion abstraction from thymine. Angew. Chem. Int. Ed. 44, 1647–1650 (2005)CrossRefGoogle Scholar
  14. 14.
    Prabhudesai, V.S., Kelkar, A.H., Nandi, D., Krishnakumar, E.: Functional group-dependent site-specific fragmentation of molecules by low energy electrons. Phys. Rev. Lett. 95, 143202-1–143202-4 (2005)CrossRefGoogle Scholar
  15. 15.
    Sloan, P.A., Palmer, R.E.: Two-electron dissociation of single molecules by atomic manipulation at room temperature. Nature 434, 367–371 (2005)CrossRefGoogle Scholar
  16. 16.
    Riedel, D., Bocquet, M.-L., Lesnard, H., Lastapis, M., Lorente, N., Sonnet, P., Dujardin, G.: Selective scanning tunnelling microscope electron-induced reactions of single biphenyl molecules on a Si(100) surface. J. Am. Chem. Soc. 131, 7344–7352 (2009)CrossRefGoogle Scholar
  17. 17.
    Ning, Z., Polanyi, J.C.: Charge delocalization induces reaction in molecular chains at a surface. Angew. Chem. Int. Ed. 52, 320–324 (2013)CrossRefGoogle Scholar
  18. 18.
    Ptasinska, S., Denifl, S., Gohlke, S., Scheier, P., Illenberger, E., Märk, T.D.: Decomposition of thymidine by low-energy electrons: Implications for the molecular mechanisms of single-strand breaks in DNA. Angew. Chem. Int. Ed. 45, 1893–1896 (2006)CrossRefGoogle Scholar
  19. 19.
    Baccarelli, I., Gianturco, F.A., Grandi, A., Sanna, V., Lucchese, R.R., Bald, I., Kopyra, J., Illenberger, E.: Selective bond breaking in beta-D-ribose by gas-phase electron attachment around 8 eV. J. Am. Chem. Soc. 129, 6269–6277 (2007)CrossRefGoogle Scholar
  20. 20.
    Bald, I., Kopyra, J., Illenberger, E.: Selective excision of C5 from D-ribose in the gas phase by low-energy electrons (0–1 eV): implications for the mechanism of DNA damage. Angew. Chem., Int. Ed. 45, 4851–4855 (2006)CrossRefGoogle Scholar
  21. 21.
    Denifl, S., Zappa, F., Mähr, I., Lecointre, J., Probst, M., Märk, T.D., Scheier, P.: Mass spectrometric investigation of anions formed upon free electron attachment to nucleobase molecules and clusters embedded in superfluid helium droplets. Phys. Rev. Lett. 97, 04320-1–04320-4 (2006)CrossRefGoogle Scholar
  22. 22.
    Papp, P., Urban, J., Matejcik, S., Stano, M., Ingólfsson, O.: Dissociative electron attachment to gas phase valine: a combined experimental and theoretical study. J. Chem. Phys. 125, 204301-1–204301-8 (2006)CrossRefGoogle Scholar
  23. 23.
    Flosadottir, H.D., Denifl, S., Zappa, F., Wendt, N., Mauracher, A., Bacher, A., Jonsson, H., Märk, T.D., Scheier, P., Ingólfsson, O.: Combined experimental and theoretical study on the nature and the metastable decay pathways of the amino acid ion fragment [M–H]. Angew. Chem. Int. Ed. 46, 8057–8059 (2007)CrossRefGoogle Scholar
  24. 24.
    Vasil'ev, Y.V., Figard, B.J., Voinov, V.G., Barofsky, D.F., Deinzer, M.L.: Resonant electron capture by some amino acids and their methyl esters. J. Am. Chem. Soc. 128, 5506–5515 (2006)CrossRefGoogle Scholar
  25. 25.
    Vizcaino, V., Puschnigg, B., Huber, S.E., Probst, M., Fabrikant, I.I., Gallup, G.A., Illenberger, E., Scheier, P., Denifl, S.: Hydrogen loss in aminobutanoic acid isomers by the sigma* resonance formed in electron capture. New J. Phys. 14, 043017-1–043017-12 (2012)CrossRefGoogle Scholar
  26. 26.
    Gschliesser, D., Vizcaino, V., Probst, M., Scheier, P., Denifl, S.: Formation and decay of the dehydrogenated parent anion upon electron attachment to dialanine. Chem. Eur. J. 18/15, 4613–4619 (2012)CrossRefGoogle Scholar
  27. 27.
    Yandell, M.A., King, S.B., Neumark, D.M.: Time-resolved radiation chemistry: photoelectron imaging of transient negative ions of nucleobases. J. Am. Chem. Soc. 135, 2128–2131 (2013)CrossRefGoogle Scholar
  28. 28.
    Denifl, S., Ptasinska, S., Probst, M., Hrusak, J., Scheier, P., Märk, T.D.: Electron attachment to the gas-phase DNA bases cytosine and thymine. J. Phys. Chem. A. 108, 6562–6569 (2004)CrossRefGoogle Scholar
  29. 29.
    Li, X., Sanche, L., Sevilla, M.D.: Low energy electron interactions with uracil: the energetics predicted by theory. J. Phys. Chem. B. 108, 5472–5476 (2004)CrossRefGoogle Scholar
  30. 30.
    Takayanagi, T., Asakura, T., Motegi, H.: Theoretical study on the mechanism of low-energy dissociative electron attachment for uracil. J. Phys. Chem. A. 113, 4795–4801 (2009)CrossRefGoogle Scholar
  31. 31.
    González-Ramírez, I., Segarra-Martí, J., Serrano-Andrés, L., Merchán, M., Rubio, M., Roca-Sanjuán, D.: On the N-1-H and N-3-H bond dissociation in uracil by low energy electrons: a CASSCF/CASPT2 study. J. Chem. Theory Comput. 8, 2769–2776 (2012)CrossRefGoogle Scholar
  32. 32.
    Burrow, P., Gallup, G., Scheer, A., Denifl, S., Ptasinska, S., Märk, T.D., Scheier, P.: Vibrational Feshbach resonances in uracil and thymine. J. Chem. Phys. 124, 124310-1–124310-7 (2006)CrossRefGoogle Scholar
  33. 33.
    Winstead, C., McKoy, V.: Low-energy electron collisions with gas-phase uracil. J. Chem. Phys. 125, 174304-1–174304-8 (2006)Google Scholar
  34. 34.
    Winstead, C., McKoy, V.: Ring-breaking electron attachment to uracil: following bond dissociations via evolving resonances. J. Chem. Phys. 129, 077101-1–077101-2 (2008); J. Chem. Phys. 128, 174302 (2008)Google Scholar
  35. 35.
    Gianturco, F. A.; Sebastianelli, F.; Lucchese, R. R.; Baccarelli, I.; Sanna, N.: Ring-breaking electron attachment to uracil: Following bond dissociations via evolving resonances. J. Chem. Phys. 128, 174302-1-174302-8 (2008); Erratum: “Ring-breaking electron attachment to uracil: Following bond dissociations via evolving resonances”. J. Chem. Phys. 131, 249901-1-249901-2 (2008)Google Scholar
  36. 36.
    Dora, A., Bryjko, L., van Mourik, T., Tennyson, J.: R-matrix study of elastic and inelastic electron collisions with cytosine and thymine. J. Phys. B. 45, 175203-1–175203-10 (2012)CrossRefGoogle Scholar
  37. 37.
    Dora, A., Tennyson, J., Bryjko, L., van Mourik, T.: R-matrix calculation of low-energy electron collisions with uracil. J. Chem. Phys. 130, 164307-1–164307-8 (2009)CrossRefGoogle Scholar
  38. 38.
    Aflatooni, K., Scheer, A.M., Burrow, P.D.: Total dissociative electron attachment cross sections for molecular constituents of DNA. J. Chem. Phys. 125, 054301-1–054301-5 (2006)CrossRefGoogle Scholar
  39. 39.
    Davis, D., Vysotskiy, V.P., Sajeev, Y., Cederbaum, L.S.: A one-step four-bond-breaking reaction catalyzed by an electron. Angew. Chem. Int. Ed. 51, 8003–8007 (2012)CrossRefGoogle Scholar
  40. 40.
    Asfandiarov, N.L., Pshenichnyuk, S.A., Lukin, V.G., Pshenichnyuk, I.A., Modelli, A., Matejcik, S.: Temporary anion states and dissociative electron attachment to nitrobenzene derivatives. Int. J. Mass Spectrom. 264, 22–37 (2007)CrossRefGoogle Scholar
  41. 41.
    Mauracher, A., Denifl, S., Edtbauer, A., Hager, M., Probst, M., Echt, O., Märk, T.D., Scheier, P., Field, T.A., Graupner, K.: Metastable anions of dinitrobenzene: resonances for electron attachment and kinetic energy release. J. Chem. Phys. 133, 244302-1–244302-9 (2010)CrossRefGoogle Scholar
  42. 42.
    Shchukin, P.V., Muftakhov, M.V., Pogulay, A.V.: Study of fragmentation pathways of metastable negative ions in aliphatic dipeptides using the statistical theory. Rapid Commun. Mass Spectrom. 26, 828–834 (2012)CrossRefGoogle Scholar
  43. 43.
    Zappa, F., Beikircher, M., Mauracher, A., Denifl, S., Probst, M., Injan, N., Limtrakul, J., Bacher, A., Echt, O., Märk, T.D., Scheier, P., Field, T.A., Graupner, K.: Metastable dissociation of anions formed by electron attachment. Chem. Phys. Chem. 9, 607–611 (2008)CrossRefGoogle Scholar
  44. 44.
    Flosadóttir, H.D., Ómarsson, B., Bald, I., Ingolfsson, O.: Metastable decay of DNA components and their compositions—a perspective on the role of reactive electron scattering in radiation damage. Eur. Phys. J. D 66, 13–32 (2012)CrossRefGoogle Scholar
  45. 45.
    Flosadóttir, H.D., Jónsson, H., Sigurdsson, S.T., Ingólfsson, O.: Experimental and theoretical study of the metastable decay of negatively charged nucleosides in the gas phase. Phys. Chem. Chem. Phys. 13, 15283–15290 (2011)CrossRefGoogle Scholar
  46. 46.
    Bald, I., Flosadóttir, H.D., Ómarsson, B., Ingólfsson, O.: Metastable fragmentation of a thymidine-nucleotide and its components. Int. J. Mass Spectrom. 313, 15–20 (2012)CrossRefGoogle Scholar
  47. 47.
    Bald, I., Flosadóttir, H.D., Kopyra, J., Illenberger, E., Ingólfsson, O.: Fragmentation of deprotonated D-ribose and D-fructose in MALDI-Comparison with dissociative electron attachment. Int. J. Mass. Spectrom. 280, 190–197 (2009)CrossRefGoogle Scholar
  48. 48.
    Flosadóttir, H.D., Bald, I., Ingólfsson, O.: Fast and metastable fragmentation of deprotonated D-fructose—a combined experimental and computational study. Int. J. Mass. Spectrom. 305, 50–57 (2011)CrossRefGoogle Scholar
  49. 49.
    Almeida, D., Ferreira da Silva, F., García, G., Limão-Vieira, P.: Selective bond cleavage in potassium collisions with pyrimidine bases of DNA. Phys. Rev. Lett. 110, 023201-1–023201-5 (2013)CrossRefGoogle Scholar
  50. 50.
    Almeida, D., Antunes, R., Martins, G., Eden, S., Ferreira da Silva, F., Nunes, Y., Garcia, G., Limão-Vieira, P.: Electron transfer-induced fragmentation of thymine and uracil in atom-molecule collisions. Phys. Chem. Chem. Phys. 13, 15657–15665 (2011)CrossRefGoogle Scholar
  51. 51.
    Hanel, G., Gstir, B., Denifl, S., Scheier, P., Probst, M., Farizon, B., Farizon, M., Illenberger, I., Märk, T.D.: Electron attachment to uracil: Effective destruction at subexcitation energies. Phys. Rev. Lett. 90, 188104-1–188104-4 (2003)CrossRefGoogle Scholar
  52. 52.
    Scheer, A.M., Silvernail, C., Belot, J.A., Aflatooni, K., Gallup, G.A., Burrow, P.D.: Dissociative electron attachment to uracil deuterated at the N-1 and N-3 positions. Chem. Phys. Lett. 411, 46–50 (2005)CrossRefGoogle Scholar
  53. 53.
    Antunes, R., Almeida, D., Martins, G., Mason, N.J., Garcia, G., Maneira, M.J.P., Nunes, Y., Limão-Vieira, P.: Negative ion formation in potassium-nitromethane collisions. Phys. Chem. Chem. Phys. 12, 12513–12519 (2010)CrossRefGoogle Scholar
  54. 54.
    Stano, M., Flosadottir, H.D., Ingolfsson, O.: Effective quenching of fragment formation in negative ion oligonucleotide matrix-assisted laser desorption/ionization mass spectrometry through sodium adduct formation. Rapid Commun. Mass Spectrom. 20, 3498–3502 (2006)CrossRefGoogle Scholar
  55. 55.
    Breeger, S., von Meltzer, M., Hennecke, U., Carell, T.: Investigation of the pathways of excess electron transfer in DNA with flavin-donor and oxetane-acceptor modified DNA hairpins. Chem. Eur. J. 12, 6469–6477 (2006)CrossRefGoogle Scholar
  56. 56.
    Grimme, S.: Semiempirical hybrid density functional with perturbative second-order correlation. J. Chem. Phys. 124, 034108-1–034108-16 (2006)CrossRefGoogle Scholar
  57. 57.
    Zheng, J., Xu, X., Truhlar, D.G.: Minimally augmented Karlsruhe basis sets. Theor. Chem. Acc. 128, 295–305 (2011)CrossRefGoogle Scholar
  58. 58.
    Becke, A.D.: Density‐functional thermochemistry. III. The role of exact exchange. J. Chem. Phys. 98 (7), 5648–5652 (1993)Google Scholar
  59. 59.
    Krishnan, R., Binkley, J.S., Seeger, R., Pople, J.A.: Self‐consistent molecular orbital methods. XX. A basis set for correlated wave functions. J. Chem. Phys. 72, 650–654 (1980)CrossRefGoogle Scholar
  60. 60.
    Jónsson, H.: Simulation of surface processes. Proc. Natl. Acad. Sci. U. S. A. 108, 944–949 (2011)CrossRefGoogle Scholar
  61. 61.
    Gallup, G.A., Fabrikant, I.I.: Vibrational Feshbach resonances in dissociative electron attachment to uracil. Phys. Rev. A 83, 012706-1–012706-7 (2011)CrossRefGoogle Scholar
  62. 62.
    Greisch, F., Gabelica, V., Remacle, F., De Pauw, E.: Thermometer ions for matrix-enhanced laser desorption/ionization internal energy calibration. Rapid Commun. Mass Spectrom. 17, 1847–1854 (2003)CrossRefGoogle Scholar
  63. 63.
    Luo, G., Marginean, I., Vertes, A.: Internal energy of ions generated by matrix-assisted laser desorption/ionization. Anal. Chem. 74, 6185–6190 (2002)CrossRefGoogle Scholar
  64. 64.
    Almeida, D., Kinzel, D., Ferreira da Silva, F., Puschnigg, B., Gschliesser, D., Scheier, P., Denifl, S., García, G., González, L., Limão-Vieira, P.: N-site demethylation in pyrimidine bases as studied by low energy electrons and ab initio calculations. Phys. Chem. Chem. Phys. 15, 11431–11440 (2013)Google Scholar
  65. 65.
    Denifl, S., Zappa, F., Mauracher, A., Ferreirada Silva, F., Bacher, A., Echt, O., Märk, T.D., Böhme, D.K., Scheier, P.: Dissociative electron attachment to DNA bases near absolute zero temperature: freezing dissociation intermediates. Chem. Phys. Chem. 9, 1387–1389 (2008)CrossRefGoogle Scholar

Copyright information

© American Society for Mass Spectrometry 2013

Authors and Affiliations

  • Filipe Ferreira da Silva
    • 1
  • Carolina Matias
    • 1
    • 2
  • Diogo Almeida
    • 1
  • Gustavo García
    • 3
  • Oddur Ingólfsson
    • 4
  • Helga Dögg Flosadóttir
    • 4
  • Benedikt Ómarsson
    • 4
  • Sylwia Ptasinska
    • 5
  • Benjamin Puschnigg
    • 2
  • Paul Scheier
    • 2
  • Paulo Limão-Vieira
    • 1
  • Stephan Denifl
    • 2
  1. 1.Laboratório de Colisões Atómicas e Moleculares, CEFITEC, Departamento de Física, Faculdade de Ciências e TecnologiaUniversidade Nova de LisboaCaparicaPortugal
  2. 2.Institut für Ionenphysik und Angewandte Physik and Center for Biomolecular Sciences InnsbruckLeopold-Franzens Universität InnsbruckInnsbruckAustria
  3. 3.Instituto de Física Fundamental, Consejo Superior de Investigaciones Científicas (CSIC)MadridSpain
  4. 4.Department of Chemistry and Science InstituteUniversity of IcelandReykjavikIceland
  5. 5.Department of Physics and Radiation LaboratoryUniversity of Notre DameNotre DameUSA

Personalised recommendations