An international research team has used the SQS instrument at the European XFEL to gain new insights into how radiation damage occurs in biological tissue. The study reveals in detail how water molecules are broken apart by high-energy radiation, creating potentially hazardous electrically charged ions, which can go on to trigger harmful reactions in the organism. The team led by Maria Novella Piancastelli and Renaud Guillemin from the Sorbonne in Paris, Ludger Inhester from DESY and Till Jahnke from European XFEL presents its observations and analyses in the scientific journal Physical Review X.

Since water is present in every known organism, the so-called photolysis of water is often the starting point for radiation damage. “However, the chain of reactions that can be triggered in the body by high-energy radiation is still not fully understood,” explains Inhester. “For example, even just observing the formation of individual ions and radicals in water when high-energy radiation is absorbed is already very difficult.”

To study this sequence of events, the researchers bombarded single water molecules with pulses from the X-ray laser. These pulses are so intense, that in many cases not only one, but two or more X-ray photons were absorbed. The absorption of the second photon gave the research team a glimpse into what happens inside the molecule after the absorption of X-ray light.

“The movement of the atoms of the molecule occurring between the two absorption events leaves a clear fingerprint in the fragmentation pattern of the molecule, in other words, the fragments of the molecule fly apart in a very specific, characteristic way,” says Piancastelli. “By carefully analysing this fingerprint, as well as using detailed simulations, we were able to draw conclusions about the ultra-fast dynamics of the water molecule after it had absorbed the first X-ray photon.” This allowed the scientists to record the disintegration of the water molecule, which lasted only a few femtoseconds (quadrillionths of a second), in the form of a film.

The study shows that the disintegration of the water molecule can be much more complicated than initially expected. The water molecule (H2O) starts to stretch and expand before eventually breaking apart. After only ten femtoseconds, the two hydrogen atoms (H), which are normally attached to the oxygen atom (O) at an angle of 104 degrees, can build up so much momentum as to face each other at an angle of around 180 degrees. As a result, the oxygen atom is not in fact flung away hard when the molecule breaks up, because the momenta of the two hydrogen nuclei largely balance each other out as they fly off, leaving the oxygen virtually at rest in the middle. In an aqueous environment, this can then easily lead to further potentially harmful chemical reactions.

“In our research, we succeeded for the first time in taking a closer look at the dynamics of a water molecule after it absorbs high-energy radiation,” says Inhester, who works at the Centre for Free-Electron Laser Science (CFEL), a collaboration between DESY, the University of Hamburg and the Max Planck Society. “In particular, we were able to characterise the formation of the oxygen and hydrogen ions and radicals more precisely, as well as the way this process unfolds over time. This disintegration of the water molecule is an important first step in the further chain of reactions that ultimately lead to radiation damage.”