Structural dynamics in proteins induced by and probed with X-ray free-electron laser pulses

• Published in: Nature communications 2020-04, Vol.11 (1), p.1814-1814, Article 1814
• Main Authors: Nass, Karol, Gorel, Alexander, Abdullah, Malik M., V. Martin, Andrew, Kloos, Marco, Marinelli, Agostino, Aquila, Andrew, Barends, Thomas R. M., Decker, Franz-Josef, Bruce Doak, R., Foucar, Lutz, Hartmann, Elisabeth, Hilpert, Mario, Hunter, Mark S., Jurek, Zoltan, Koglin, Jason E., Kozlov, Alexander, Lutman, Alberto A., Kovacs, Gabriela Nass, Roome, Christopher M., Shoeman, Robert L., Santra, Robin, Quiney, Harry M., Ziaja, Beata, Boutet, Sébastien, Schlichting, Ilme
• Format: Article
• Language: English
• Subjects: 631/45/535; 631/535/1266; 631/535/1266/1265; 639/766/1960; 639/766/36; Backbone; Bacterial Proteins - chemistry; Biological properties; Biological samples; Bridges; Crystal structure; Crystallography; Crystals; Disulfides - chemistry; Dynamics; Electrons; Environmental effects; Femtosecond pulses; Ferredoxin; Free electron lasers; Gating; Humanities and Social Sciences; Ionization; Ions; Lasers; Microcrystals; multidisciplinary; Nanocrystals; Proteins; Radiation; Radiation damage; Radiation measurement; RADIATION, THERMAL, AND OTHER ENVIRON. POLLUTANT EFFECTS ON LIVING ORGS. AND BIOL. MAT; Science; Science (multidisciplinary); Structural damage; Sulfur; Sulfur - chemistry; Synchrotrons; X-Rays
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-020-15610-4

X-ray free-electron lasers (XFELs) enable crystallographic structure determination beyond the limitations imposed upon synchrotron measurements by radiation damage. The need for very short XFEL pulses is relieved through gating of Bragg diffraction by loss of crystalline order as damage progresses, but not if ionization events are spatially non-uniform due to underlying elemental distributions, as in biological samples. Indeed, correlated movements of iron and sulfur ions were observed in XFEL-irradiated ferredoxin microcrystals using unusually long pulses of 80 fs. Here, we report a femtosecond time-resolved X-ray pump/X-ray probe experiment on protein nanocrystals. We observe changes in the protein backbone and aromatic residues as well as disulfide bridges. Simulations show that the latter’s correlated structural dynamics are much slower than expected for the predicted high atomic charge states due to significant impact of ion caging and plasma electron screening. This indicates that dense-environment effects can strongly affect local radiation damage-induced structural dynamics. The local X-ray-induced dynamics that occur in protein crystals during serial femtosecond crystallography (SFX) measurements at XFELs are not well understood. Here the authors performed a time-resolved X-ray pump X-ray probe SFX experiment, and they observe distinct structural changes in the disulfide bridges and peptide backbone of proteins; complementing theoretical approaches allow them to further characterize the details of the X-ray induced ionization and local structural dynamics.