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Title: Soft x-ray absorption spectroscopy of metalloproteins and high-valent metal-complexes at room temperature using free-electron lasers

Abstract

X-ray absorption spectroscopy at the L-edge of 3d transition metals provides unique information on the local metal charge and spin states by directly probing 3d-derived molecular orbitals through 2p-3d transitions. But, this soft x-ray technique has been rarely used at synchrotron facilities for mechanistic studies of metalloenzymes due to the difficulties of x-ray-induced sample damage and strong background signals from light elements that can dominate the low metal signal. Here, we combine femtosecond soft x-ray pulses from a free-electron laser with a novel x-ray fluorescence-yield spectrometer to overcome these difficulties. We present L-edge absorption spectra of inorganic high-valent Mn complexes (Mn ~ 6-15 mmol/l) with no visible effects of radiation damage. We then present the first L-edge absorption spectra of the oxygen evolving complex (Mn 4 CaO 5 ) in Photosystem II (Mn < 1 mmol/l) at room temperature, measured under similar conditions. Our approach opens new ways to study metalloenzymes under functional conditions.

Authors:
 [1];  [2];  [3];  [4];  [3];  [5];  [3];  [6];  [1];  [1];  [5];  [5];  [7];  [8];  [6];  [4];  [9];  [6];  [6];  [6] more »;  [6];  [6];  [6];  [10];  [11];  [12];  [12];  [12];  [12];  [13];  [13];  [13];  [12];  [14];  [5];  [15];  [7];  [1];  [3];  [3];  [1] « less
  1. Helmholtz-Zentrum Berlin for Materials and Energy, Berlin (Germany). Inst. for Methods and Instrumentation for Synchrotron Radiation Research
  2. SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource
  5. Helmholtz-Zentrum Berlin for Materials and Energy, Berlin (Germany). Inst. for Nanometre Optics and Technology
  6. SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source
  7. SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford PULSE Inst.
  8. SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source, Stanford PULSE Inst.
  9. Synchrotron SOLEIL, St. Aubin (France)
  10. SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford PULSE Inst.; Umea Univ. (Sweden). Inst. for Chemistry, Chemical Biological Center
  11. Umea Univ. (Sweden). Inst. for Chemistry, Chemical Biological Center
  12. California Inst. of Technology (CalTech), Pasadena, CA (United States). Division of Chemistry and Chemical Engineering
  13. Univ. of California, Irvine, CA (United States). Dept. of Chemistry
  14. Umea Univ. (Sweden). Inst. of Chemistry, Centre for Biological Chemistry; Uppsala Univ. (Sweden). Dept. of Chemistry, Molecular Biomimetics
  15. Helmholtz-Zentrum Berlin for Materials and Energy, Berlin (Germany). Inst. for Methods and Instrumentation for Synchrotron Radiation Research; Univ. of Potsdam (Germany). Inst. for Physics and Astronomy
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1416916
Grant/Contract Number:
AC02-05CH11231
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Structural Dynamics
Additional Journal Information:
Journal Volume: 4; Journal Issue: 5; Journal ID: ISSN 2329-7778
Publisher:
American Crystallographic Association/AIP
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Kubin, Markus, Kern, Jan, Gul, Sheraz, Kroll, Thomas, Chatterjee, Ruchira, Löchel, Heike, Fuller, Franklin D., Sierra, Raymond G., Quevedo, Wilson, Weniger, Christian, Rehanek, Jens, Firsov, Anatoly, Laksmono, Hartawan, Weninger, Clemens, Alonso-Mori, Roberto, Nordlund, Dennis L., Lassalle-Kaiser, Benedikt, Glownia, James M., Krzywinski, Jacek, Moeller, Stefan, Turner, Joshua J., Minitti, Michael P., Dakovski, Georgi L., Koroidov, Sergey, Kawde, Anurag, Kanady, Jacob S., Tsui, Emily Y., Suseno, Sandy, Han, Zhiji, Hill, Ethan, Taguchi, Taketo, Borovik, Andrew S., Agapie, Theodor, Messinger, Johannes, Erko, Alexei, Föhlisch, Alexander, Bergmann, Uwe, Mitzner, Rolf, Yachandra, Vittal K., Yano, Junko, and Wernet, Philippe. Soft x-ray absorption spectroscopy of metalloproteins and high-valent metal-complexes at room temperature using free-electron lasers. United States: N. p., 2017. Web. doi:10.1063/1.4986627.
Kubin, Markus, Kern, Jan, Gul, Sheraz, Kroll, Thomas, Chatterjee, Ruchira, Löchel, Heike, Fuller, Franklin D., Sierra, Raymond G., Quevedo, Wilson, Weniger, Christian, Rehanek, Jens, Firsov, Anatoly, Laksmono, Hartawan, Weninger, Clemens, Alonso-Mori, Roberto, Nordlund, Dennis L., Lassalle-Kaiser, Benedikt, Glownia, James M., Krzywinski, Jacek, Moeller, Stefan, Turner, Joshua J., Minitti, Michael P., Dakovski, Georgi L., Koroidov, Sergey, Kawde, Anurag, Kanady, Jacob S., Tsui, Emily Y., Suseno, Sandy, Han, Zhiji, Hill, Ethan, Taguchi, Taketo, Borovik, Andrew S., Agapie, Theodor, Messinger, Johannes, Erko, Alexei, Föhlisch, Alexander, Bergmann, Uwe, Mitzner, Rolf, Yachandra, Vittal K., Yano, Junko, & Wernet, Philippe. Soft x-ray absorption spectroscopy of metalloproteins and high-valent metal-complexes at room temperature using free-electron lasers. United States. doi:10.1063/1.4986627.
Kubin, Markus, Kern, Jan, Gul, Sheraz, Kroll, Thomas, Chatterjee, Ruchira, Löchel, Heike, Fuller, Franklin D., Sierra, Raymond G., Quevedo, Wilson, Weniger, Christian, Rehanek, Jens, Firsov, Anatoly, Laksmono, Hartawan, Weninger, Clemens, Alonso-Mori, Roberto, Nordlund, Dennis L., Lassalle-Kaiser, Benedikt, Glownia, James M., Krzywinski, Jacek, Moeller, Stefan, Turner, Joshua J., Minitti, Michael P., Dakovski, Georgi L., Koroidov, Sergey, Kawde, Anurag, Kanady, Jacob S., Tsui, Emily Y., Suseno, Sandy, Han, Zhiji, Hill, Ethan, Taguchi, Taketo, Borovik, Andrew S., Agapie, Theodor, Messinger, Johannes, Erko, Alexei, Föhlisch, Alexander, Bergmann, Uwe, Mitzner, Rolf, Yachandra, Vittal K., Yano, Junko, and Wernet, Philippe. 2017. "Soft x-ray absorption spectroscopy of metalloproteins and high-valent metal-complexes at room temperature using free-electron lasers". United States. doi:10.1063/1.4986627. https://www.osti.gov/servlets/purl/1416916.
@article{osti_1416916,
title = {Soft x-ray absorption spectroscopy of metalloproteins and high-valent metal-complexes at room temperature using free-electron lasers},
author = {Kubin, Markus and Kern, Jan and Gul, Sheraz and Kroll, Thomas and Chatterjee, Ruchira and Löchel, Heike and Fuller, Franklin D. and Sierra, Raymond G. and Quevedo, Wilson and Weniger, Christian and Rehanek, Jens and Firsov, Anatoly and Laksmono, Hartawan and Weninger, Clemens and Alonso-Mori, Roberto and Nordlund, Dennis L. and Lassalle-Kaiser, Benedikt and Glownia, James M. and Krzywinski, Jacek and Moeller, Stefan and Turner, Joshua J. and Minitti, Michael P. and Dakovski, Georgi L. and Koroidov, Sergey and Kawde, Anurag and Kanady, Jacob S. and Tsui, Emily Y. and Suseno, Sandy and Han, Zhiji and Hill, Ethan and Taguchi, Taketo and Borovik, Andrew S. and Agapie, Theodor and Messinger, Johannes and Erko, Alexei and Föhlisch, Alexander and Bergmann, Uwe and Mitzner, Rolf and Yachandra, Vittal K. and Yano, Junko and Wernet, Philippe},
abstractNote = {X-ray absorption spectroscopy at the L-edge of 3d transition metals provides unique information on the local metal charge and spin states by directly probing 3d-derived molecular orbitals through 2p-3d transitions. But, this soft x-ray technique has been rarely used at synchrotron facilities for mechanistic studies of metalloenzymes due to the difficulties of x-ray-induced sample damage and strong background signals from light elements that can dominate the low metal signal. Here, we combine femtosecond soft x-ray pulses from a free-electron laser with a novel x-ray fluorescence-yield spectrometer to overcome these difficulties. We present L-edge absorption spectra of inorganic high-valent Mn complexes (Mn ~ 6-15 mmol/l) with no visible effects of radiation damage. We then present the first L-edge absorption spectra of the oxygen evolving complex (Mn 4 CaO 5 ) in Photosystem II (Mn < 1 mmol/l) at room temperature, measured under similar conditions. Our approach opens new ways to study metalloenzymes under functional conditions.},
doi = {10.1063/1.4986627},
journal = {Structural Dynamics},
number = 5,
volume = 4,
place = {United States},
year = 2017,
month = 9
}

Journal Article:
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  • X-ray free electron lasers (XFELs) enable unprecedented new ways to study the electronic structure and dynamics of transition metal systems. L-edge absorption spectroscopy is a powerful technique for such studies and the feasibility of this method at XFELs for solutions and solids has been demonstrated. But, the required x-ray bandwidth is an order of magnitude narrower than that of self-amplified spontaneous emission (SASE), and additional monochromatization is needed. We compare L-edge x-ray absorption spectroscopy (XAS) of a prototypical transition metal system based on monochromatizing the SASE radiation of the linac coherent light source (LCLS) with a new technique based onmore » self-seeding of LCLS. We demonstrate how L-edge XAS can be performed using the self-seeding scheme without the need of an additional beam line monochromator. Lastly, we show how the spectral shape and pulse energy depend on the undulator setup and how this affects the x-ray spectroscopy measurements.« less
  • © 2016 Optical Society of America. X-ray free electron lasers (XFELs) enable unprecedented new ways to study the electronic structure and dynamics of transition metal systems. L-edge absorption spectroscopy is a powerful technique for such studies and the feasibility of this method at XFELs for solutions and solids has been demonstrated. However, the required x-ray bandwidth is an order of magnitude narrower than that of self-amplified spontaneous emission (SASE), and additional monochromatization is needed. Here we compare L-edge x-ray absorption spectroscopy (XAS) of a prototypical transition metal system based on monochromatizing the SASE radiation of the linac coherent light sourcemore » (LCLS) with a new technique based on self-seeding of LCLS. We demonstrate how L-edge XAS can be performed using the self-seeding scheme without the need of an additional beam line monochromator. We show how the spectral shape and pulse energy depend on the undulator setup and how this affects the x-ray spectroscopy measurements.« less
  • This report will describe our recent studies of transition metal complex structural dynamics on the fs and ps time scales using an X-ray free electron laser source, Linac Coherent Light Source (LCLS). Ultrafast XANES spectra at the Ni K-edge of nickel(II) tetramesitylporphyrin (NiTMP) were successfully measured for optically excited state at a timescale from 100 fs to 50 ps, providing insight into its sub-ps electronic and structural relaxation processes. Importantly, a transient reduced state Ni(I) (π, 3dx2-y2) electronic state is captured through the interpretation of a short-lived excited state absorption on the low-energy shoulder of the edge, which is aidedmore » by the computation of X-ray transitions for postulated excited electronic states. The observed and computed inner shell to valence orbital transition energies demonstrate and quantify the influence of electronic configuration on specific metal orbital energies. A strong influence of the valence orbital occupation on the inner shell orbital energies indicates that one should not use the transition energy from 1s to other orbitals to draw conclusions about the d-orbital energies. For photocatalysis, a transient electronic configuration could influence d-orbital energies up to a few eV and any attempt to steer the reaction pathway should account for this to ensure that external energies can be used optimally in driving desirable processes. NiTMP structural evolution and the influence of the porphyrin macrocycle conformation on relaxation kinetics can be likewise inferred from this study.« less