Can we transcend the traditional limits of hard X-ray physics to generate pulses so short they can capture the instantaneous movement of electrons within an atom?

During photosynthetic water oxidation, the Mn4Ca cluster in Photosystem II progresses through five intermediate Si (i = 0-4) states. X-ray crystallography studies have reported the insertion of one new O ligand during the formation of the S3 state, but recent studies question the presence of this additional ligand based on cryo-EM and earlier room-temperature crystallography data. There is also controversy about whether the O-O bond interaction already occurs in the S3 state or in the subsequent S3 to S0 transition. Here we report conventional high-resolution data for the S1, S2, and S3 states to a resolution of ~1.9 Å, and anomalous diffraction data at two energies (9.5 keV and 7 keV), that was used to model the Mn positions, followed by determination of oxygen positions using the high-resolution maps. We show that the new oxygen atom, OX (or O6), in the S3 state is observable as a distinct peak without any restraints, confirming its ligation to Mn1 and Ca. The OX-O5 distance is ~2.1 Å, supporting no strong interaction between them in the S3 state, suggesting that if this is the O-O bond formation site, it is formed during the S3 to S0 transition initiated by the final oxidation of the cluster.

We report the successful resolution of the multiplet structure of Kα 1 x-ray emission in manganese (Mn) complexes through seeded stimulated x-ray emission spectroscopy (seeded S-XES). Using a femtosecond pump pulse above the Mn K edge to generate simultaneous 1s core holes, and a second-color tunable seed pulse to initiate the stimulated emission process, we were able to enhance individual lines within the Kα 1 emission. This approach allows to resolve the fine multiplet features that are obscured by lifetime broadening in conventional (spontaneous) Mn Kα XES. The work builds on our previous observation that S-XES from Mn(II) and Mn(VII) complexes pumped at high intensities can exhibit stimulated emission without sacrificing the chemical sensitivity to oxidation states. This technique opens the door to controlled high-resolution electronic structure spectroscopy in transition-metal complexes beyond the core-hole lifetime, with potential applications in catalysis, inorganic chemistry, and materials science.

By combining hard x-ray attosecond pulses from the European XFEL with total-reflection focusing x-ray optics, we generated nanofocused hard x-ray attosecond pulses with intensities and fluences comparable to the highest values attained in the hard x-ray regime. A peak intensity on the order of 10^20 W/cm^2 is confirmed through the observation of saturation in amplified spontaneous emission from copper atoms. These x-ray pulses enable new scientific opportunities, including the exploration of higher-order nonlinear light–matter interactions, damage-free structure determination, and coherent control of atoms and molecules.

Our work reveals the structure of the active state of Methyl-Coenzyme M Reductase (MCR), the key and rate-limiting enzyme in biological methane formation. We find large differences between the active Ni(I) and inactive Ni(II) proteins and provide insight into how nature makes and breaks the C-H bond of methane. The Ni(II)-F430 center in inactive MCR contains four planar nitrogen ligands, a lower axial glutamine oxo, and an upper axial thiolate. The Ni(I)-enzyme replaces the axial ligands with a single water. The one-electron redox change results in movement of the Ni ion and upward swing of the β-lactam ring in the tetrapyrrole coupled to a domino-like protein quake through second sphere residues, inter-subunit interactions, a substrate tunnel, affecting even the dimensions of the unit cell. These structural changes lead Ni(I)-MCR to release a charge clamp that, in the Ni(II) state, locks down substrate Coenzyme B. Determining the Ni(I)-MCR structure required development of rigorous anaerobic crystallographic techniques. Validation of the MCR redox state was accomplished by in-line and parallel spectroscopic and unit cell analyses. This structure has large implications for developing technologies to limit methane emissions and efficiently produce biofuels. Methodology described here will enhance structural biology for other oxygen-sensitive enzymes. ### Competing Interest Statement The authors have declared no competing interest. Office of Basic Energy SciencesOffice of Basic Energy Sciences, https://ror.org/05mg91w61, DE-FG02-08ER15931, FWP 100593, DE-AC02-05CH11231, DE-SC0014664, DE-AC02-76SF00515, DEAC02-05CH11231 National Institutes of HealthNational Institutes of Health, https://ror.org/01cwqze88, GM149528, GM110501, GM126289, GM117126, GM151988, P30GM133894

Since the invention of the laser, nonlinear effects such as filamentation1, Rabi cycling2,3 and collective emission4 have been explored in the optical regime, leading to a wide range of scientific and industrial applications5-8. X-ray free-electron lasers (XFELs) have extended many optical techniques to X-rays for their advantages of ångström-scale spatial resolution and elemental specificity9. An example is XFEL-driven inner-shell Kα1 (2p3/2 → 1s1/2) X-ray lasing in elements ranging from neon to copper, which has been used for nonlinear spectroscopy and development of new X-ray laser sources10-16. Here we show that strong lasing effects similar to those in the optical regime can occur at 1.5-2.1 Å wavelengths during high-intensity (>1019 W cm-2) XFEL-driven Kα1 lasing of copper and manganese. Depending on the temporal XFEL pump pulse substructure, the resulting X-ray pulses (about 106-108 photons) can exhibit strong spatial inhomogeneities and spectral splitting, inhomogeneities and broadening. Three-dimensional Maxwell-Bloch calculations17 show that the observed spatial inhomogeneities result from X-ray filamentation and that the broad spectral features are driven by sub-femtosecond Rabi cycling. Our simulations indicate that these X-ray pulses can have pulse lengths of less than 100 attoseconds and coherence properties that provide opportunities for quantum X-ray optics applications.

We report the successful resolution of the multiplet structure of the Kα1 x-ray emission in manganese (Mn) complexes through seeded stimulated X-ray emission spectroscopy (seeded S-XES). By employing a femtosecond pump pulse above the Mn K edge to generate simultaneous 1s core-holes, and a second-color tunable seed pulse to initiate the stimulated emission process, we were able to enhance individual lines within the Kα1 emission. This approach allows to resolve the fine multiplet features that are obscured by the life-time broadening in conventional Mn Kα XES. The work builds on our previous observation that S-XES from Mn(II) and Mn(VII) complexes pumped at high intensities can exhibit stimulated emission without sacrificing the chemical sensitivity to oxidation states. This technique opens the door to controlled high-resolution electronic structure spectroscopy in transition metal complexes beyond core hole life time broadening with potential applications in catalysis, inorganic chemistry, and materials science.

Conducting real-time, element-specific studies of photo-excited systems is a long-standing challenge. The development of X-ray free-electron lasers (XFELs) has paved the way for the emergence of a promising technique: femtosecond X-ray absorption spectroscopy (fs-XAS). This powerful technique reveals electronic and geometric characteristics, providing unprecedented insight into their dynamic interactions under nonequilibrium conditions. Herein, the fs-XAS technique is employed at PAL-XFEL to unravel light-driven ultrafast electronic and structural changes in epitaxial lanthanum iron oxide (LaFeO3) thin films. Density functional theory (DFT) and multiplet calculations are utilized to expound on the experimental results. The analyses reveal that photoexcitation initially induces high- and intermediate-spin Fe2+ states through ligand-to-metal charge transfer (LMCT), followed by polaron formation. It is demonstrated that the reduced overlap between the oxygen 2p and iron 3d orbitals accounts for all experimental observations, including 1) the XAS shifts to lower energies, 2) the decrease in the crystal field splitting, and 3) the relatively larger shifts observed in the oxygen 1s XAS.

X-ray absorption spectroscopy (XAS) of 3d transition metals provides important electronic structure information for many fields. However, X-ray-induced radiation damage under physiological temperature has prevented using this method to study dilute aqueous systems, such as metalloenzymes, as the catalytic reaction proceeds. Here we present a new approach to enable operando XAS of dilute biological samples and demonstrate its feasibility with K-edge XAS spectra from the Mn cluster in photosystem II and the Fe-S centers in photosystem I. This approach combines highly efficient sample delivery strategies and a robust signal normalization method with high-transmission Bragg diffraction-based spectrometers at X-ray free-electron lasers (XFELs) in a damage-free, shot-by-shot mode. These photon-out spectrometers have been optimized for discriminating the metal Mn/Fe Kα fluorescence signals from the overwhelming scattering background present on currently available detectors for XFELs that lack suitable energy discrimination. We quantify the enhanced performance metrics of the spectrometer and discuss its potential applications for acquiring time-resolved XAS spectra of biological samples during their reactions at XFELs.

We present the first direct experimental confirmation of attosecond pulse generation in the hard X-ray regime with a free-electron laser. Our experiment is based on measurements of a nonlinear optical phenomenon known as amplified spontaneous emission (ASE) from 3d transition metals. By analyzing the yield of the collective X-ray fluorescence induced by ultrashort pulses at the Linac Coherent Light Source, we identify the generation of attosecond pulses and shot-to-shot fluctuations in their duration, ranging from 100 as to 400 as. The observed product of bandwidth and pulse duration for 100 as pulses is approximately 2 fs·eV, indicating the generation of nearly transform-limited pulses. Our results extend the photon energy reach of attosecond techniques by one order of magnitude, providing the ability to simultaneously probe matter on the time-scales of electronic phenomena and with atomic spatial resolution. Furthermore, attosecond hard X-ray pulses can outrun the fastest radiation damage processes, paving the way to single-shot damage-free X-ray measurements.

We report the observation and analysis of the gain curve of amplified Kα x-ray emission from solutions of Mn(II) and Mn(VII) complexes using an x-ray free electron laser to create the 1s core-hole population inversion. We find spectra at amplification levels extending over 4 orders of magnitude until saturation. We observe bandwidths below the Mn 1s core-hole lifetime broadening in the onset of the stimulated emission. In the exponential amplification regime the resolution corrected spectral width of ∼1.7  eV FWHM is constant over 3 orders of magnitude, pointing to the buildup of transform limited pulses of ∼1  fs duration. Driving the amplification into saturation leads to broadening and a shift of the line. Importantly, the chemical sensitivity of the stimulated x-ray emission to the Mn oxidation state is preserved at power densities of ∼10^{20}  W/cm^{2} for the incoming x-ray pulses. Differences in signal sensitivity and spectral information compared to conventional (spontaneous) x-ray emission spectroscopy are discussed. Our findings build a baseline for nonlinear x-ray spectroscopy for a wide range of transition metal complexes in inorganic chemistry, catalysis, and materials science.

In natural photosynthesis, the light-driven splitting of water into electrons, protons and molecular oxygen forms the first step of the solar-to-chemical energy conversion process. The reaction takes place in photosystem II, where the Mn 4 CaO 5 cluster first stores four oxidizing equivalents, the S 0 to S 4 intermediate states in the Kok cycle, sequentially generated by photochemical charge separations in the reaction center and then catalyzes the O–O bond formation chemistry 1 – 3 . Here, we report room temperature snapshots by serial femtosecond X-ray crystallography to provide structural insights into the final reaction step of Kok’s photosynthetic water oxidation cycle, the S 3 →[S 4 ]→S 0 transition where O 2 is formed and Kok’s water oxidation clock is reset. Our data reveal a complex sequence of events, which occur over micro- to milliseconds, comprising changes at the Mn 4 CaO 5 cluster, its ligands and water pathways as well as controlled proton release through the hydrogen-bonding network of the Cl1 channel. Importantly, the extra O atom O x , which was introduced as a bridging ligand between Ca and Mn1 during the S 2 →S 3 transition 4 – 6 , disappears or relocates in parallel with Y z reduction starting at approximately 700 μs after the third flash. The onset of O 2 evolution, as indicated by the shortening of the Mn1–Mn4 distance, occurs at around 1,200 μs, signifying the presence of a reduced intermediate, possibly a bound peroxide.

In a recent paper we proposed to build an x-ray laser oscillator (XLO) in the 6-10 keV range providing intense, stable, transform-limited, x-ray pulses based on population inversion driven by an x-ray pulse train generated by an x-ray free-electron laser (XFEL) operated at a repetition rate of about 100 Hz. Here we present an analysis of recent experimental results on x-ray lasing with population inversion, damage caused by the pump on the lasing medium, and optical cavities, together with theoretical/numerical simulations. Our findings suggest that it is possible to build and operate a second-generation x-ray laser oscillator, XLO-II, operating at up to 125 kHz repetition rate. XLO-II will be pumped by 6-10 keV x-ray SASE pulses, generated by the new LCLS-II-HE XFEL now under construction at SLAC National Accelerator Laboratory, utilizing a CW superconducting linac and capable of running at 1 MHz repetition rate. XLO-II will generate transform-limited, coherent x-ray pulses with an average power in the tens of mW range. It will open new experimental capabilities, for instance in fields like imaging, interferometry, and quantum x-ray optics. The main characteristics of XLO-II and its main components, including the optical cavity, will be discussed.

The water oxidation reaction in photosystem II (PS II) produces most of the molecular oxygen in the atmosphere, which sustains life on Earth, and in this process releases four electrons and four protons that drive the downstream process of CO2 fixation in the photosynthetic apparatus. The catalytic center of PS II is an oxygen-bridged Mn4Ca complex (Mn4CaO5) which is progressively oxidized upon the absorption of light by the chlorophyll of the PS II reaction center, and the accumulation of four oxidative equivalents in the catalytic center results in the oxidation of two waters to dioxygen in the last step. The recent emergence of X-ray free-electron lasers (XFELs) with intense femtosecond X-ray pulses has opened up opportunities to visualize this reaction in PS II as it proceeds through the catalytic cycle. In this review, we summarize our recent studies of the catalytic reaction in PS II by following the structural changes along the reaction pathway via room-temperature X-ray crystallography using XFELs. The evolution of the electron density changes at the Mn complex reveals notable structural changes, including the insertion of OX from a new water molecule, which disappears on completion of the reaction, implicating it in the O-O bond formation reaction. We were also able to follow the structural dynamics of the protein coordinating with the catalytic complex and of channels within the protein that are important for substrate and product transport, revealing well orchestrated conformational changes in response to the electronic changes at the Mn4Ca cluster.

Views Icon Views Article contents Figures & tables Video Audio Supplementary Data Peer Review Share Icon Share Twitter Facebook Reddit LinkedIn Tools Icon Tools Reprints and Permissions Cite Icon Cite Search Site Citation Peter Vester, Katharina Kubicek, Roberto Alonso-Mori, Tadesse Assefa, Elisa Biasin, Morten Christensen, Asmus O. Dohn, Tim B. van Driel, Andreas Galler, Wojciech Gawelda, Tobias C. B. Harlang, Niels E. Henriksen, Kasper S. Kjær, Thomas S. Kuhlman, Zoltán Németh, Zhangatay Nurekeyev, Mátyás Pápai, Jochen Rittman, György Vankó, Hasan Yavas, Diana B. Zederkof, Uwe Bergmann, Martin M. Nielsen, Klaus B. Møller, Kristoffer Haldrup, Christian Bressler; Publisher's Note: "Tracking structural solvent reorganization and recombination dynamics following e− photoabstraction from aqueous I− with femtosecond x-ray spectroscopy and scattering" [J. Chem. Phys. 157, 224201 (2022)]. J. Chem. Phys. 7 April 2023; 158 (13): 139903. https://doi.org/10.1063/5.0151289 Download citation file: Ris (Zotero) Reference Manager EasyBib Bookends Mendeley Papers EndNote RefWorks BibTex toolbar search Search Dropdown Menu toolbar search search input Search input auto suggest filter your search All ContentAIP Publishing PortfolioThe Journal of Chemical Physics Search Advanced Search |Citation Search

There is great interest in developingfully coherentmultidimensionalX-ray/extreme ultraviolet (XUV) spectroscopic techniques because oftheir capability for achieving atomic spectral selectivity. Currentproposals rest on using sequentially and coherently driven core excitationswith multiple X-ray/XUV excitation pulses and measuring the outputusing time domain Fourier transform methods. In this paper, we proposean alternative method that creates an entanglement of core and opticaltransitions to form a Floquet state that creates directional and coherentoutput beams. Multidimensional spectra are obtained by measuring theintensity of output beams while tuning the optical frequencies acrossresonances. This approach expands on previous optical pump-XUVprobe spectroscopy of MoTe2 by theoretically demonstratingits multidimensional capabilities. Both parametric and non-parametricpathways are proposed to optimize the resolution of inhomogeneousbroadening and k-selective features.