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. The authors study intermolecular Coulomb decay that occurs in a sample of THF and water in a reaction microscope employing triple-coincidence measurements of two ions and one electron. They find that ICD is a previously unconsidered effect between water and other organic molecules that are hydrogen-bonded, with ICD outpacing proton transfer.