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Title: Flow-aligned, single-shot fiber diffraction using a femtosecond X-ray free-electron laser

Abstract

A major goal for X-ray free-electron laser (XFEL) based science is to elucidate structures of biological molecules without the need for crystals. Filament systems may provide some of the first single macromolecular structures elucidated by XFEL radiation, since they contain one-dimensional translational symmetry and thereby occupy the diffraction intensity region between the extremes of crystals and single molecules. Here, we demonstrate flow alignment of as few as 100 filaments ( Escherichia coli pili, F-actin, and amyloid fibrils), which when intersected by femtosecond X-ray pulses result in diffraction patterns similar to those obtained from classical fiber diffraction studies. We also determine that F-actin can be flow-aligned to a disorientation of approximately 5 degrees. Using this XFEL-based technique, we determine that gelsolin amyloids are comprised of stacked β-strands running perpendicular to the filament axis, and that a range of order from fibrillar to crystalline is discernable for individual α-synuclein amyloids.

Authors:
 [1];  [2];  [3];  [1];  [2];  [4];  [1];  [5];  [6];  [6];  [6];  [7];  [8];  [8];  [8];  [9];  [6];  [10];  [1];  [6] more »;  [6];  [8];  [11];  [9];  [12];  [12];  [12];  [13];  [6];  [6];  [6];  [9];  [5];  [5];  [5];  [14];  [10];  [15];  [5];  [6];  [6];  [7];  [16];  [6];  [8];  [17] « less
  1. A*STAR (Agency for Science, Technology and Research) (Singapore)
  2. National Univ. of Singapore (Singapore)
  3. A*STAR (Agency for Science, Technology and Research) (Singapore); National Univ. of Singapore (Singapore)
  4. Univ. of Michigan, Ann Arbor, MI (United States)
  5. SLAC National Accelerator Lab., Menlo Park, CA (United States)
  6. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany)
  7. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany); Univ. of Hamburg, Hamburg (Germany)
  8. Univ. of Gothenburg (Sweden)
  9. Univ. of California, Los Angeles, CA (United States)
  10. Univ. of Canterbury, Christchurch (New Zealand)
  11. Institut Laue - Langevin, Grenoble (France); Keele Univ., Staffordshire (United Kingdom)
  12. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  13. Uppsala Univ., Uppsala (Sweden)
  14. Northeastern Univ., Boston, MA (United States)
  15. Institut Laue-Langevin, Grenoble (France); Keele Univ., Staffordshire (United Kingdom)
  16. National Univ. of Singapore (Singapore); A*STAR (Agency for Science, Technology and Research) (Singapore)
  17. A*STAR (Agency for Science, Technology and Research) (Singapore); National Univ. of Singapore (Singapore); Okayama Univ., Okayama (Japan)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1420139
Alternate Identifier(s):
OSTI ID: 1393240
Grant/Contract Number:
AC02-05CH11231; AC02-76SF00515
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Cytoskeleton
Additional Journal Information:
Journal Volume: 74; Journal Issue: 12; Journal ID: ISSN 1949-3584
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; XFEL; fiber diffraction; filament systems

Citation Formats

Popp, David, Loh, N. Duane, Zorgati, Habiba, Ghoshdastider, Umesh, Liow, Lu Ting, Ivanova, Magdalena I., Larsson, Mårten, DePonte, Daniel P., Bean, Richard, Beyerlein, Kenneth R., Gati, Cornelius, Oberthuer, Dominik, Arnlund, David, Branden, Gisela, Berntsen, Peter, Cascio, Duilio, Chavas, Leonard M. G., Chen, Joe P. J., Ding, Ke, Fleckenstein, Holger, Gumprecht, Lars, Harimoorthy, Rajiv, Mossou, Estelle, Sawaya, Michael R., Brewster, Aaron S., Hattne, Johan, Sauter, Nicholas K., Seibert, Marvin, Seuring, Carolin, Stellato, Francesco, Tilp, Thomas, Eisenberg, David S., Messerschmidt, Marc, Williams, Garth J., Koglin, Jason E., Makowski, Lee, Millane, Rick P., Forsyth, Trevor, Boutet, Sebastien, White, Thomas A., Barty, Anton, Chapman, Henry, Chen, Swaine L., Liang, Mengning, Neutze, Richard, and Robinson, Robert C.. Flow-aligned, single-shot fiber diffraction using a femtosecond X-ray free-electron laser. United States: N. p., 2017. Web. doi:10.1002/cm.21378.
Popp, David, Loh, N. Duane, Zorgati, Habiba, Ghoshdastider, Umesh, Liow, Lu Ting, Ivanova, Magdalena I., Larsson, Mårten, DePonte, Daniel P., Bean, Richard, Beyerlein, Kenneth R., Gati, Cornelius, Oberthuer, Dominik, Arnlund, David, Branden, Gisela, Berntsen, Peter, Cascio, Duilio, Chavas, Leonard M. G., Chen, Joe P. J., Ding, Ke, Fleckenstein, Holger, Gumprecht, Lars, Harimoorthy, Rajiv, Mossou, Estelle, Sawaya, Michael R., Brewster, Aaron S., Hattne, Johan, Sauter, Nicholas K., Seibert, Marvin, Seuring, Carolin, Stellato, Francesco, Tilp, Thomas, Eisenberg, David S., Messerschmidt, Marc, Williams, Garth J., Koglin, Jason E., Makowski, Lee, Millane, Rick P., Forsyth, Trevor, Boutet, Sebastien, White, Thomas A., Barty, Anton, Chapman, Henry, Chen, Swaine L., Liang, Mengning, Neutze, Richard, & Robinson, Robert C.. Flow-aligned, single-shot fiber diffraction using a femtosecond X-ray free-electron laser. United States. doi:10.1002/cm.21378.
Popp, David, Loh, N. Duane, Zorgati, Habiba, Ghoshdastider, Umesh, Liow, Lu Ting, Ivanova, Magdalena I., Larsson, Mårten, DePonte, Daniel P., Bean, Richard, Beyerlein, Kenneth R., Gati, Cornelius, Oberthuer, Dominik, Arnlund, David, Branden, Gisela, Berntsen, Peter, Cascio, Duilio, Chavas, Leonard M. G., Chen, Joe P. J., Ding, Ke, Fleckenstein, Holger, Gumprecht, Lars, Harimoorthy, Rajiv, Mossou, Estelle, Sawaya, Michael R., Brewster, Aaron S., Hattne, Johan, Sauter, Nicholas K., Seibert, Marvin, Seuring, Carolin, Stellato, Francesco, Tilp, Thomas, Eisenberg, David S., Messerschmidt, Marc, Williams, Garth J., Koglin, Jason E., Makowski, Lee, Millane, Rick P., Forsyth, Trevor, Boutet, Sebastien, White, Thomas A., Barty, Anton, Chapman, Henry, Chen, Swaine L., Liang, Mengning, Neutze, Richard, and Robinson, Robert C.. Fri . "Flow-aligned, single-shot fiber diffraction using a femtosecond X-ray free-electron laser". United States. doi:10.1002/cm.21378. https://www.osti.gov/servlets/purl/1420139.
@article{osti_1420139,
title = {Flow-aligned, single-shot fiber diffraction using a femtosecond X-ray free-electron laser},
author = {Popp, David and Loh, N. Duane and Zorgati, Habiba and Ghoshdastider, Umesh and Liow, Lu Ting and Ivanova, Magdalena I. and Larsson, Mårten and DePonte, Daniel P. and Bean, Richard and Beyerlein, Kenneth R. and Gati, Cornelius and Oberthuer, Dominik and Arnlund, David and Branden, Gisela and Berntsen, Peter and Cascio, Duilio and Chavas, Leonard M. G. and Chen, Joe P. J. and Ding, Ke and Fleckenstein, Holger and Gumprecht, Lars and Harimoorthy, Rajiv and Mossou, Estelle and Sawaya, Michael R. and Brewster, Aaron S. and Hattne, Johan and Sauter, Nicholas K. and Seibert, Marvin and Seuring, Carolin and Stellato, Francesco and Tilp, Thomas and Eisenberg, David S. and Messerschmidt, Marc and Williams, Garth J. and Koglin, Jason E. and Makowski, Lee and Millane, Rick P. and Forsyth, Trevor and Boutet, Sebastien and White, Thomas A. and Barty, Anton and Chapman, Henry and Chen, Swaine L. and Liang, Mengning and Neutze, Richard and Robinson, Robert C.},
abstractNote = {A major goal for X-ray free-electron laser (XFEL) based science is to elucidate structures of biological molecules without the need for crystals. Filament systems may provide some of the first single macromolecular structures elucidated by XFEL radiation, since they contain one-dimensional translational symmetry and thereby occupy the diffraction intensity region between the extremes of crystals and single molecules. Here, we demonstrate flow alignment of as few as 100 filaments (Escherichia coli pili, F-actin, and amyloid fibrils), which when intersected by femtosecond X-ray pulses result in diffraction patterns similar to those obtained from classical fiber diffraction studies. We also determine that F-actin can be flow-aligned to a disorientation of approximately 5 degrees. Using this XFEL-based technique, we determine that gelsolin amyloids are comprised of stacked β-strands running perpendicular to the filament axis, and that a range of order from fibrillar to crystalline is discernable for individual α-synuclein amyloids.},
doi = {10.1002/cm.21378},
journal = {Cytoskeleton},
number = 12,
volume = 74,
place = {United States},
year = {Fri Jun 02 00:00:00 EDT 2017},
month = {Fri Jun 02 00:00:00 EDT 2017}
}

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  • A major goal for X-ray free-electron laser (XFEL) based science is to elucidate structures of biological molecules without the need for crystals. Filament systems may provide some of the first single macromolecular structures elucidated by XFEL radiation, since they contain one-dimensional translational symmetry and thereby occupy the diffraction intensity region between the extremes of crystals and single molecules. Here, we demonstrate flow alignment of as few as 100 filaments ( Escherichia coli pili, F-actin, and amyloid fibrils), which when intersected by femtosecond X-ray pulses result in diffraction patterns similar to those obtained from classical fiber diffraction studies. We also determinemore » that F-actin can be flow-aligned to a disorientation of approximately 5 degrees. Using this XFEL-based technique, we determine that gelsolin amyloids are comprised of stacked β-strands running perpendicular to the filament axis, and that a range of order from fibrillar to crystalline is discernable for individual α-synuclein amyloids.« less
  • The ultrabright femtosecond X-ray pulses provided by X-ray free-electron lasers open capabilities for studying the structure and dynamics of a wide variety of systems beyond what is possible with synchrotron sources. Recently, this “probe-before-destroy” approach has been demonstrated for atomic structure determination by serial X-ray diffraction of microcrystals. There has been the question whether a similar approach can be extended to probe the local electronic structure by X-ray spectroscopy. To address this, we have carried out femtosecond X-ray emission spectroscopy (XES) at the Linac Coherent Light Source using redox-active Mn complexes. XES probes the charge and spin states as wellmore » as the ligand environment, critical for understanding the functional role of redox-active metal sites. Kβ 1,3 XES spectra of Mn II and Mn 2 III,IV complexes at room temperature were collected using a wavelength dispersive spectrometer and femtosecond X-ray pulses with an individual dose of up to >100 MGy. The spectra were found in agreement with undamaged spectra collected at low dose using synchrotron radiation. Our results demonstrate that the intact electronic structure of redox active transition metal compounds in different oxidation states can be characterized with this shot-by-shot method. This opens the door for studying the chemical dynamics of metal catalytic sites by following reactions under functional conditions. Furthermore, the technique can be combined with X-ray diffraction to simultaneously obtain the geometric structure of the overall protein and the local chemistry of active metal sites and is expected to prove valuable for understanding the mechanism of important metalloproteins, such as photosystem II.« less
  • Structural information about biological macromolecules near the atomic scale provides important insight into the functions of these molecules. To date, X-ray crystallography has been the predominant method used for macromolecular structure determination. However, challenges exist when solving structures with X-rays, including the phase problem and radiation damage. X-ray-free electron lasers (X-ray FELs) have enabled collection of diffraction information before the onset of radiation damage, yet the majority of structures solved at X-ray FELs have been phased using external information via molecular replacement. De novo phasing at X-ray FELs has proven challenging due in part to per-pulse variations in intensity andmore » wavelength. Here we report the solution of a selenobiotinyl-streptavidin structure using phases obtained by the anomalous diffraction of selenium measured at a single wavelength (Se-SAD) at the Linac Coherent Light Source. Finally, our results demonstrate Se-SAD, routinely employed at synchrotrons for novel structure determination, is now possible at X-ray FELs.« less