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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
+ Show Author Affiliations
  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); USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1416916
Alternate Identifier(s):
OSTI ID: 1378120
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
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.
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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. https://doi.org/10.1063/1.4986627
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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. Fri . "Soft x-ray absorption spectroscopy of metalloproteins and high-valent metal-complexes at room temperature using free-electron lasers". United States. https://doi.org/10.1063/1.4986627. https://www.osti.gov/servlets/purl/1416916.
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@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}
}
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