Sang-Kil Son

Multiwavelength anomalous diffraction at high x-ray intensity.

The multiwavelength anomalous diffraction (MAD) method is used to determine phase information in x-ray crystallography by employing anomalous scattering from heavy atoms. X-ray free-electron lasers (FELs) show promise for revealing the structure of single molecules or nanocrystals, but the phase problem remains largely unsolved. Because of the ultrabrightness of x-ray FEL, samples experience severe electronic radiation damage, especially to heavy atoms, which hinders direct implementation of MAD with x-ray FELs. Here, we propose a generalized version of MAD phasing at high x-ray intensity. We demonstrate the existence of a Karle-Hendrickson-type equation in the high-intensity regime and calculate relevant coefficients with detailed electronic damage dynamics of heavy atoms. The present method offers a potential for ab initio structural determination in femtosecond x-ray nanocrystallography.

Deep Inner-Shell Multiphoton Ionization by Intense X-Ray Free-Electron Laser Pulses

We have investigated multiphoton multiple ionization dynamics of xenon atoms using a new x-ray free-electron laser facility, SPring-8 Angstrom Compact free electron LAser (SACLA) in Japan, and identified that Xe(n+) with n up to 26 is produced at a photon energy of 5.5 keV. The observed high charge states (n≥24) are produced via five-photon absorption, evidencing the occurrence of multiphoton absorption involving deep inner shells. A newly developed theoretical model, which shows good agreement with the experiment, elucidates the complex pathways of sequential electronic decay cascades accessible in heavy atoms. The present study of heavy-atom ionization dynamics in high-intensity hard-x-ray pulses makes a step forward towards molecular structure determination with x-ray free-electron lasers.

Nanoplasma Formation by High Intensity Hard X-rays.

Using electron spectroscopy, we have investigated nanoplasma formation from noble gas clusters exposed to high-intensity hard-x-ray pulses at ~5u2009keV. Our experiment was carried out at the SPring-8 Angstrom Compact free electron LAser (SACLA) facility in Japan. Dedicated theoretical simulations were performed with the molecular dynamics tool XMDYN. We found that in this unprecedented wavelength regime nanoplasma formation is a highly indirect process. In the argon clusters investigated, nanoplasma is mainly formed through secondary electron cascading initiated by slow Auger electrons. Energy is distributed within the sample entirely through Auger processes and secondary electron cascading following photoabsorption, as in the hard x-ray regime there is no direct energy transfer from the field to the plasma. This plasma formation mechanism is specific to the hard-x-ray regime and may, thus, also be important for XFEL-based molecular imaging studies. In xenon clusters, photo- and Auger electrons contribute more significantly to the nanoplasma formation. Good agreement between experiment and simulations validates our modelling approach. This has wide-ranging implications for our ability to quantitatively predict the behavior of complex molecular systems irradiated by high-intensity hard x-rays.

Femtosecond response of polyatomic molecules to ultra-intense hard X-rays

X-ray free-electron lasers enable the investigation of the structure and dynamics of diverse systems, including atoms, molecules, nanocrystals and single bioparticles, under extreme conditions. Many imaging applications that target biological systems and complex materials use hard X-ray pulses with extremely high peak intensities (exceeding 1020 watts per square centimetre). However, fundamental investigations have focused mainly on the individual response of atoms and small molecules using soft X-rays with much lower intensities. Studies with intense X-ray pulses have shown that irradiated atoms reach a very high degree of ionization, owing to multiphoton absorption, which in a heteronuclear molecular system occurs predominantly locally on a heavy atom (provided that the absorption cross-section of the heavy atom is considerably larger than those of its neighbours) and is followed by efficient redistribution of the induced charge. In serial femtosecond crystallography of biological objects—an application of X-ray free-electron lasers that greatly enhances our ability to determine protein structure—the ionization of heavy atoms increases the local radiation damage that is seen in the diffraction patterns of these objects and has been suggested as a way of phasing the diffraction data. On the basis of experiments using either soft or less-intense hard X-rays, it is thought that the induced charge and associated radiation damage of atoms in polyatomic molecules can be inferred from the charge that is induced in an isolated atom under otherwise comparable irradiation conditions. Here we show that the femtosecond response of small polyatomic molecules that contain one heavy atom to ultra-intense (with intensities approaching 1020 watts per square centimetre), hard (with photon energies of 8.3u2009kiloelectronvolts) X-ray pulses is qualitatively different: our experimental and modelling results establish that, under these conditions, the ionization of a molecule is considerably enhanced compared to that of an individual heavy atom with the same absorption cross-section. This enhancement is driven by ultrafast charge transfer within the molecule, which refills the core holes that are created in the heavy atom, providing further targets for inner-shell ionization and resulting in the emission of more than 50 electrons during the X-ray pulse. Our results demonstrate that efficient modelling of X-ray-driven processes in complex systems at ultrahigh intensities is feasible.

Towards RIP using free-electron laser SFX data.

Here, it is shown that simulated native serial femtosecond crystallography (SFX) cathepsin B data can be phased by rapid ionization of sulfur atoms. Utilizing standard software adopted for radiation-damage-induced phasing (RIP), the effects on both substructure determination and phasing of the number of collected patterns and fluences are explored for experimental conditions already available at current free-electron laser facilities.

Determination of multiwavelength anomalous diffraction coefficients at high x-ray intensity

The high-intensity version of multiwavelength anomalous diffraction (MAD) has a potential for solving the phase problem in femtosecond crystallography with x-ray free-electron lasers (XFELs). For MAD phasing, it is required to calculate or measure the MAD coefficients involved in the key equation, which depend on XFEL pulse parameters. In this work, we revisit the generalized Karle–Hendrickson equation to clarify the importance of configurational fluctuations of heavy atoms induced by intense x-ray pulses, and investigate the high-intensity cases of transmission and fluorescence measurements of samples containing heavy atoms. Based on transmission/fluorescence and diffraction experiments with crystalline samples of known structures, we propose an experimental procedure to determine all MAD coefficients at high x-ray intensity, which can be used in ab initio phasing for unknown structures.

Incoherent x-ray scattering in single molecule imaging

Imaging of the structure of single proteins or other biomolecules with atomic resolution would be enormously beneficial to structural biology. X-ray free-electron lasers generate highly intense and ultrashort x-ray pulses, providing a route towards imaging of single molecules with atomic resolution. The information on molecular structure is encoded in the coherent x-ray scattering signal. In contrast to crystallography there are no Bragg reflections in single molecule imaging, which means the coherent scattering is not enhanced. Consequently, a background signal from incoherent scattering deteriorates the quality of the coherent scattering signal. This background signal cannot be easily eliminated because the spectrum of incoherently scattered photons cannot be resolved by usual scattering detectors. We present an ab initio study of incoherent x-ray scattering from individual carbon atoms, including the electronic radiation damage caused by a highly intense x-ray pulse. We find that the coherent scattering pattern suffers from a significant incoherent background signal at high resolution. For high x-ray fluence the background signal becomes even dominating. Finally, based on the atomic scattering patterns, we present an estimation for the average photon count in single molecule imaging at high resolution. By varying the photon energy from 3.5 keV to 15 keV, we find that imaging at higher photon energies may improve the coherent scattering signal quality.

Towards phasing using high X-ray intensity

Analysis of serial femtosecond crystallography data collected at the Linac Coherent Light Source using two distinct photon fluxes shows different degrees of ionization of Gd atoms bound to a lysozyme protein, due to electronic damage processes. The charge contrast on the heavy atoms is quantified using difference Fourier maps, and the way in which this could be applied to phasing is discussed.

Electronic damage in S atoms in a native protein crystal induced by an intense X-ray free-electron laser pulse

Current hard X-ray free-electron laser (XFEL) sources can deliver doses to biological macromolecules well exceeding 1 GGy, in timescales of a few tens of femtoseconds. During the pulse, photoionization can reach the point of saturation in which certain atomic species in the sample lose most of their electrons. This electronic radiation damage causes the atomic scattering factors to change, affecting, in particular, the heavy atoms, due to their higher photoabsorption cross sections. Here, it is shown that experimental serial femtosecond crystallography data collected with an extremely bright XFEL source exhibit a reduction of the effective scattering power of the sulfur atoms in a native protein. Quantitative methods are developed to retrieve information on the effective ionization of the damaged atomic species from experimental data, and the implications of utilizing new phasing methods which can take advantage of this localized radiation damage are discussed.

Photoelectron spectroscopy method to reveal ionization potential lowering in nanoplasmas

Here we propose a scheme for probing the outer-shell atomic energy levels within a laser-created nanoplasma, using photoelectron spectroscopy data obtained from the irradiation of the nanoplasma with an ultraintense ‘probing’ pulse from a soft x-ray free-electron laser. The proposed method can then detect shifts of outer-shell energy levels of an atom or an ion within a plasma, due to the effect of charged plasma environment on atomic potentials, known as the ‘plasma screening effect’. Various theoretical models exist that estimate the magnitude of the screening effect. However, the first experimental data that can verify theoretical models have become available only recently (Vinko et al 2012 Nature 482 59). They were obtained with a hard x-ray-based experimental method which uses the information encoded in fluorescence spectra and is, therefore, restricted to deep atomic shells. Below, we show that our photoelectron spectroscopy method of probing a nanoplasma with a destructive, high-intensity soft x-ray pulse that brings the irradiated system to the regime of ‘massively parallel’ ionization (Gnodtke et al 2012 Phys. Rev. Lett. 108 175003) enables access to the information on the energy level (and ultimately energy level shift) of the valence orbital. In particular, the result of such a photoelectron spectroscopy experiment could help to clarify the discrepancy between the ion abundances in nanoplasmas observed during the recent high-harmonic-generation and free-electron-laser experiments with intense soft x-ray pulses. (Some figures may appear in colour only in the online journal)