X-ray Absorption Spectroscopy of Dilute Metalloenzymes at X-ray Free-Electron Lasers in a Shot-by-Shot Mode

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 <i>operando</i> 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.

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Publication Details

Journal
The Journal of Physical Chemistry Letters
Published
2025-04-07
DOI
https://doi.org/10.1021/acs.jpclett.5c00399
Citations
3
Primary Topic
Photosynthetic Processes and Mechanisms
Type
article
Field-Weighted Citation Impact
2.42

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article

X-ray Absorption Spectroscopy of Dilute Metalloenzymes at X-ray Free-Electron Lasers in a Shot-by-Shot Mode

Moritz Kretzschmar, Leland Bruce Gee, Aaron S. Brewster, Hiroki Makita et al.
3 citations
The Journal of Physical Chemistry Letters
Photosynthetic Processes and Mechanisms
2.42
article

X-ray Absorption Spectroscopy of Dilute Metalloenzymes at X-ray Free-Electron Lasers in a Shot-by-Shot Mode

Moritz Kretzschmar, Leland Bruce Gee, Aaron S. Brewster, Hiroki Makita, Jan F Kern, Erzsi Szilagyi, Takahiro Sato, Petko Chernev, Medhanjali Dasgupta, Thomas Fransson, Margaret Doyle, Thomas Kröll, Isabel Bogacz, Vittal K. Yachandra, A. Oggenfuss, Johannes Messinger, Isabela I. Nangca, Danylо Babich, Kensuke Tono, H. Lemke, Shigeki Owada, Kuntal Chatterjee, Mathias Sander, Dimosthenis Sokaras, Uwe Bergmann, Nicholas K. Sauter, Roberto Alonso‐Mori, Roman Mankowsky, Philipp S. Simon, Junko Yano, Asmit Bhowmick, Mun Hon Cheah, Miao Zhang, Serhane Zerdane, Nicholas Croy
article en
3 citations

Abstract

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 <i>operando</i> 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.

The Journal of Physical Chemistry LettersVol. 16(15)
Uppsala University (SE), University of Wisconsin–Madison (US), Lawrence Berkeley National Laboratory (US), SLAC National Accelerator Laboratory (US), Paul Scherrer Institute (CH), Humboldt-Universität zu Berlin (DE), SPring-8 (JP), Japan Synchrotron Radiation Research Institute (JP), Umeå Plant Science Centre (SE), BioMimetic Systems (United States) (US), Linac Coherent Light Source (US), KTH Royal Institute of Technology (SE), Umeå University (SE)
U.S. Department of Energy, American Physical Society, Stiftelsen för Strategisk Forskning, Paul Scherrer Institut, Vetenskapsrådet, Stiftelsen för Strategisk Forskning, National Institutes of Health, Office of Science, European Research Council, National Institute of General Medical Sciences, Basic Energy Sciences, SLAC National Accelerator Laboratory
Affordable and clean energy
Openalex Percentile: Top 12%
Photosynthetic Processes and Mechanisms
2.42
DOIOpen Access PDFOpenAlex
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