Experimental evidence for ultrafast intermolecular relaxation processes in hydrated biomolecules

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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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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).

Author information

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.

Correspondence to Xueguang Ren or Alexander Dorn.

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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) doi:10.1038/s41567-018-0214-9

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