Observing heme doming in myoglobin with femtosecond X-ray absorption spectroscopy
Abstract
We report time-resolved X-ray absorption measurements after photolysis of carbonmonoxy myoglobin performed at the LCLS X-ray free electron laser with nearly 100 fs (FWHM) time resolution. Data at the Fe K-edge reveal that the photoinduced structural changes at the heme occur in two steps, with a faster (~70 fs) relaxation preceding a slower (~400 fs) one. We tentatively attribute the first relaxation to a structural rearrangement induced by photolysis involving essentially only the heme chromophore and the second relaxation to a residual Fe motion out of the heme plane that is coupled to the displacement of myoglobin F-helix.
- Authors:
-
- Univ. of Palermo, Palermo (Italy)
- SLAC National Accelerator Lab., Menlo Park, CA (United States)
- CNRS - Institut de Biologie Structurale, Grenoble 38044, France
- Univ. of Rennes, Rennes (France)
- Publication Date:
- Research Org.:
- SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1190858
- Resource Type:
- Journal Article: Accepted Manuscript
- Journal Name:
- Structural Dynamics
- Additional Journal Information:
- Journal Volume: 2; Journal Issue: 4; Journal ID: ISSN 2329-7778
- Publisher:
- American Crystallographic Association/AIP
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 63 RADIATION, THERMAL, AND OTHER ENVIRON. POLLUTANT EFFECTS ON LIVING ORGS. AND BIOL. MAT.
Citation Formats
Levantino, M., Lemke, H. T., Schirò, G., Glownia, M., Cupane, A., and Cammarata, M. Observing heme doming in myoglobin with femtosecond X-ray absorption spectroscopy. United States: N. p., 2015.
Web. doi:10.1063/1.4921907.
Levantino, M., Lemke, H. T., Schirò, G., Glownia, M., Cupane, A., & Cammarata, M. Observing heme doming in myoglobin with femtosecond X-ray absorption spectroscopy. United States. https://doi.org/10.1063/1.4921907
Levantino, M., Lemke, H. T., Schirò, G., Glownia, M., Cupane, A., and Cammarata, M. 2015.
"Observing heme doming in myoglobin with femtosecond X-ray absorption spectroscopy". United States. https://doi.org/10.1063/1.4921907. https://www.osti.gov/servlets/purl/1190858.
@article{osti_1190858,
title = {Observing heme doming in myoglobin with femtosecond X-ray absorption spectroscopy},
author = {Levantino, M. and Lemke, H. T. and Schirò, G. and Glownia, M. and Cupane, A. and Cammarata, M.},
abstractNote = {We report time-resolved X-ray absorption measurements after photolysis of carbonmonoxy myoglobin performed at the LCLS X-ray free electron laser with nearly 100 fs (FWHM) time resolution. Data at the Fe K-edge reveal that the photoinduced structural changes at the heme occur in two steps, with a faster (~70 fs) relaxation preceding a slower (~400 fs) one. We tentatively attribute the first relaxation to a structural rearrangement induced by photolysis involving essentially only the heme chromophore and the second relaxation to a residual Fe motion out of the heme plane that is coupled to the displacement of myoglobin F-helix.},
doi = {10.1063/1.4921907},
url = {https://www.osti.gov/biblio/1190858},
journal = {Structural Dynamics},
issn = {2329-7778},
number = 4,
volume = 2,
place = {United States},
year = {Wed Jul 01 00:00:00 EDT 2015},
month = {Wed Jul 01 00:00:00 EDT 2015}
}
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Works referenced in this record:
Femtosecond X-ray Absorption Spectroscopy at a Hard X-ray Free Electron Laser: Application to Spin Crossover Dynamics
journal, January 2013
- Lemke, Henrik T.; Bressler, Christian; Chen, Lin X.
- The Journal of Physical Chemistry A, Vol. 117, Issue 4
Photolysis-induced structural changes in single crystals of carbonmonoxy myoglobin at 40 K
journal, October 1994
- Teng, T. -Y.; Šrajer, V.; Moffat, K.
- Nature Structural & Molecular Biology, Vol. 1, Issue 10
Achieving few-femtosecond time-sorting at hard X-ray free-electron lasers
journal, February 2013
- Harmand, M.; Coffee, R.; Bionta, M. R.
- Nature Photonics, Vol. 7, Issue 3
Picosecond Raman study of energy flow in a photoexcited heme protein
journal, November 1991
- Lingle, Robert; Xu, Xiaobing; Zhu, Huiping
- The Journal of Physical Chemistry, Vol. 95, Issue 23
X-ray absorption spectroscopy of biological photolysis products: kilohertz photolysis and soft X-ray applications
journal, April 2005
- Wang, Hongxin; Peng, Gang; Cramer, Stephen P.
- Journal of Electron Spectroscopy and Related Phenomena, Vol. 143, Issue 1
Femtosecond XANES Study of the Light-Induced Spin Crossover Dynamics in an Iron(II) Complex
journal, January 2009
- Bressler, Ch.; Milne, C.; Pham, V. -T.
- Science, Vol. 323, Issue 5913
Tracking excited-state charge and spin dynamics in iron coordination complexes
journal, May 2014
- Zhang, Wenkai; Alonso-Mori, Roberto; Bergmann, Uwe
- Nature, Vol. 509, Issue 7500
A high-repetition rate scheme for synchrotron-based picosecond laser pump/x-ray probe experiments on chemical and biological systems in solution
journal, June 2011
- Lima, Frederico A.; Milne, Christopher J.; Amarasinghe, Dimali C. V.
- Review of Scientific Instruments, Vol. 82, Issue 6
Ultrafast Structural Relaxation of Myoglobin Following Photodissociation of Carbon Monoxide Probed by Time-Resolved Resonance Raman Spectroscopy
journal, November 2001
- Mizutani, Yasuhisa; Kitagawa, Teizo
- The Journal of Physical Chemistry B, Vol. 105, Issue 44
Investigations of the thermal response of laser-excited biomolecules
journal, February 1994
- Li, P.; Champion, P. M.
- Biophysical Journal, Vol. 66, Issue 2
Ligand binding and protein relaxation in heme proteins: a room temperature analysis of nitric oxide geminate recombination
journal, April 1991
- Petrich, J. W.; Lambry, J. C.; Kuczera, K.
- Biochemistry, Vol. 30, Issue 16
A single-shot transmissive spectrometer for hard x-ray free electron lasers
journal, July 2012
- Zhu, Diling; Cammarata, Marco; Feldkamp, Jan M.
- Applied Physics Letters, Vol. 101, Issue 3
Directed Energy “Funneling" Mechanism for Heme Cooling Following Ligand Photolysis or Direct Excitation in Solvated Carbonmonoxy Myoglobin
journal, July 2001
- Sagnella, Diane E.; Straub, John E.
- The Journal of Physical Chemistry B, Vol. 105, Issue 29
Detailed Transient Heme Structures of Mb-CO in Solution after CO Dissociation: An X-ray Transient Absorption Spectroscopic Study
journal, November 2012
- Stickrath, Andrew B.; Mara, Michael W.; Lockard, Jenny V.
- The Journal of Physical Chemistry B, Vol. 117, Issue 16
Sequential Activation of Molecular Breathing and Bending during Spin-Crossover Photoswitching Revealed by Femtosecond Optical and X-Ray Absorption Spectroscopy
journal, November 2014
- Cammarata, Marco; Bertoni, Roman; Lorenc, Maciej
- Physical Review Letters, Vol. 113, Issue 22
Molecular dynamics simulations of cooling in laser-excited heme proteins.
journal, December 1986
- Henry, E. R.; Eaton, W. A.; Hochstrasser, R. M.
- Proceedings of the National Academy of Sciences, Vol. 83, Issue 23
Evidence for sub-picosecond heme doming in hemoglobin and myoglobin: a time-resolved resonance Raman comparison of carbonmonoxy and deoxy species
journal, January 1995
- Franzen, S.; Bohn, B.; Poyart, C.
- Biochemistry, Vol. 34, Issue 4
X-ray Absorption Studies of the Photo-induced Structural Changes of Myoglobin in Physiological
conference, January 2012
- Lima, Frederico A.; Milne, Christopher J.; Rittmann-Frank, Mercedes Hannelore
- International Conference on Ultrafast Structural Dynamics, Research in Optical Sciences
Time-Resolved X-ray Absorption Spectroscopy of Carbon Monoxide-Myoglobin Recombination After Laser Photolysis
journal, February 1984
- Mills, D. M.; Lewis, A.; Harootunian, A.
- Science, Vol. 223, Issue 4638
Femtosecond photolysis of CO-ligated protoheme and hemoproteins: appearance of deoxy species with a 350-fsec time constant.
journal, January 1983
- Martin, J. L.; Migus, A.; Poyart, C.
- Proceedings of the National Academy of Sciences, Vol. 80, Issue 1
Fluorescence detection of EXAFS: Sensitivity enhancement for dilute species and thin films
journal, December 1993
- Jaklevic, J.; Kirby, J. A.; Klein, M. P.
- Solid State Communications, Vol. 88, Issue 11-12
Functional Aspects of Ultra-rapid Heme Doming in Hemoglobin, Myoglobin, and the Myoglobin Mutant H93G
journal, January 1995
- Franzen, Stefan; Bohn, Brigitte; Poyart, Claude
- Journal of Biological Chemistry, Vol. 270, Issue 4
Resonance Raman investigation of myoglobin and hemoglobin
journal, September 1984
- Bangcharoenpaurpong, O.; Schomacker, K. T.; Champion, P. M.
- Journal of the American Chemical Society, Vol. 106, Issue 19
Calculations of electron inelastic mean free paths. V. Data for 14 organic compounds over the 50-2000 eV range
journal, March 1994
- Tanuma, S.; Powell, C. J.; Penn, D. R.
- Surface and Interface Analysis, Vol. 21, Issue 3
Crystal structure of photolysed carbonmonoxy-myoglobin
journal, October 1994
- Schlichting, Ilme; Berendzen, Joel; Phillips, George N.
- Nature, Vol. 371, Issue 6500
New insight into metalloporphyrin excited state structures and axial ligand binding from X-ray transient absorption spectroscopic studies
journal, October 2014
- Shelby, Megan L.; Mara, Michael W.; Chen, Lin X.
- Coordination Chemistry Reviews, Vol. 277-278
X-ray absorption spectra: K-edges of 3d transition metals, L-edges of 3d and 4d metals, and M-edges of palladium
journal, May 1982
- Müller, J. E.; Jepsen, O.; Wilkins, J. W.
- Solid State Communications, Vol. 42, Issue 5
Light-Induced Relaxation of Photolyzed Carbonmonoxy Myoglobin: A Temperature-Dependent X-Ray Absorption Near-Edge Structure (XANES) Study
journal, April 2005
- Arcovito, A.; Lamb, D. C.; Nienhaus, G. U.
- Biophysical Journal, Vol. 88, Issue 4
Photophysics and reactivity of heme proteins: a femtosecond absorption study of hemoglobin, myoglobin, and protoheme
journal, May 1988
- Petrich, J. W.; Poyart, C.; Martin, J. L.
- Biochemistry, Vol. 27, Issue 11
Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser
journal, August 2014
- Arnlund, David; Johansson, Linda C.; Wickstrand, Cecilia
- Nature Methods, Vol. 11, Issue 9
Picosecond primary structural transition of the heme is retarded after nitric oxide binding to heme proteins
journal, July 2010
- Kruglik, S. G.; Yoo, B. -K.; Franzen, S.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 31
Myoglobin: The hydrogen atom of biology and a paradigm of complexity
journal, July 2003
- Frauenfelder, H.; McMahon, B. H.; Fenimore, P. W.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 15
Ultrafast myoglobin structural dynamics observed with an X-ray free-electron laser
journal, April 2015
- Levantino, Matteo; Schirò, Giorgio; Lemke, Henrik Till
- Nature Communications, Vol. 6, Issue 1
Molecular Dynamics Study on the Solvent Dependent Heme Cooling Following Ligand Photolysis in Carbonmonoxy Myoglobin
journal, March 2007
- Zhang, Yong; Fujisaki, Hiroshi; Straub, John E.
- The Journal of Physical Chemistry B, Vol. 111, Issue 12
Direct Observation of Cooling of Heme Upon Photodissociation of Carbonmonoxy Myoglobin
journal, October 1997
- Mizutani, Y.
- Science, Vol. 278, Issue 5337
Watching a Protein as it Functions with 150-ps Time-Resolved X-ray Crystallography
journal, June 2003
- Schotte, F.
- Science, Vol. 300, Issue 5627
Molecular dynamics simulation of photodissociation of carbon monoxide from hemoglobin.
journal, April 1985
- Henry, E. R.; Levitt, M.; Eaton, W. A.
- Proceedings of the National Academy of Sciences, Vol. 82, Issue 7
Femtosecond Biology
journal, June 1992
- Martin, J. L.; Vos, M. H.
- Annual Review of Biophysics and Biomolecular Structure, Vol. 21, Issue 1
Observation of coherent reaction dynamics in heme proteins
journal, October 1994
- Zhu, L.; Sage, J.; Champion, P.
- Science, Vol. 266, Issue 5185
Tracking the structural dynamics of proteins in solution using time-resolved wide-angle X-ray scattering
journal, September 2008
- Cammarata, Marco; Levantino, Matteo; Schotte, Friedrich
- Nature Methods, Vol. 5, Issue 10
Picosecond time-resolved Raman studies of photodissociated carboxymyoglobin
journal, May 1985
- Findsen, Eric W.; Scott, Thomas W.; Chance, Mark R.
- Journal of the American Chemical Society, Vol. 107, Issue 11
Protein states and proteinquakes.
journal, August 1985
- Ansari, A.; Berendzen, J.; Bowne, S. F.
- Proceedings of the National Academy of Sciences, Vol. 82, Issue 15
Measurements of the Photodissociation Quantum Yields of MbNO and MbO 2 and the Vibrational Relaxation of the Six-Coordinate Heme Species
journal, May 2002
- Ye, Xiong; Demidov, Andrey; Champion, Paul M.
- Journal of the American Chemical Society, Vol. 124, Issue 20
Primary protein response after ligand photodissociation in carbonmonoxy myoglobin
journal, May 2007
- Sato, A.; Gao, Y.; Kitagawa, T.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 23
Molecular dynamics simulation of NO recombination to myoglobin mutants.
journal, August 1993
- Li, H.; Elber, R.; Straub, J. E.
- Journal of Biological Chemistry, Vol. 268, Issue 24
Calculations of electron inelastic mean free paths. V. Data for 14 organic compounds over the 50-2000 eV range
journal, March 1994
- Tanuma, S.; Powell, C. J.; Penn, D. R.
- Surface and Interface Analysis, Vol. 21, Issue 3
X-ray absorption spectra: K-edges of 3d transition metals, L-edges of 3d and 4d metals, and M-edges of palladium
journal, May 1982
- Müller, J. E.; Jepsen, O.; Wilkins, J. W.
- Solid State Communications, Vol. 42, Issue 5
Fluorescence detection of EXAFS: Sensitivity enhancement for dilute species and thin films
journal, December 1993
- Jaklevic, J.; Kirby, J. A.; Klein, M. P.
- Solid State Communications, Vol. 88, Issue 11-12
New insight into metalloporphyrin excited state structures and axial ligand binding from X-ray transient absorption spectroscopic studies
journal, October 2014
- Shelby, Megan L.; Mara, Michael W.; Chen, Lin X.
- Coordination Chemistry Reviews, Vol. 277-278
X-ray absorption spectroscopy of biological photolysis products: kilohertz photolysis and soft X-ray applications
journal, April 2005
- Wang, Hongxin; Peng, Gang; Cramer, Stephen P.
- Journal of Electron Spectroscopy and Related Phenomena, Vol. 143, Issue 1
Heme Photolysis Occurs by Ultrafast Excited State Metal-to-Ring Charge Transfer
journal, May 2001
- Franzen, Stefan; Kiger, Laurent; Poyart, Claude
- Biophysical Journal, Vol. 80, Issue 5
The effect of iron displacement out of the porphyrin plane on the resonance Raman spectra of heme proteins and iron porphyrins
journal, November 1993
- Stavrov, S. S.
- Biophysical Journal, Vol. 65, Issue 5
Evidence for sub-picosecond heme doming in hemoglobin and myoglobin: a time-resolved resonance Raman comparison of carbonmonoxy and deoxy species
journal, January 1995
- Franzen, S.; Bohn, B.; Poyart, C.
- Biochemistry, Vol. 34, Issue 4
Ligand binding and protein relaxation in heme proteins: a room temperature analysis of nitric oxide geminate recombination
journal, April 1991
- Petrich, J. W.; Lambry, J. C.; Kuczera, K.
- Biochemistry, Vol. 30, Issue 16
Photophysics and reactivity of heme proteins: a femtosecond absorption study of hemoglobin, myoglobin, and protoheme
journal, May 1988
- Petrich, J. W.; Poyart, C.; Martin, J. L.
- Biochemistry, Vol. 27, Issue 11
Picosecond Raman study of energy flow in a photoexcited heme protein
journal, November 1991
- Lingle, Robert; Xu, Xiaobing; Zhu, Huiping
- The Journal of Physical Chemistry, Vol. 95, Issue 23
Picosecond time-resolved Raman studies of photodissociated carboxymyoglobin
journal, May 1985
- Findsen, Eric W.; Scott, Thomas W.; Chance, Mark R.
- Journal of the American Chemical Society, Vol. 107, Issue 11
Measurements of the Photodissociation Quantum Yields of MbNO and MbO 2 and the Vibrational Relaxation of the Six-Coordinate Heme Species
journal, May 2002
- Ye, Xiong; Demidov, Andrey; Champion, Paul M.
- Journal of the American Chemical Society, Vol. 124, Issue 20
Ultrafast Structural Relaxation of Myoglobin Following Photodissociation of Carbon Monoxide Probed by Time-Resolved Resonance Raman Spectroscopy
journal, November 2001
- Mizutani, Yasuhisa; Kitagawa, Teizo
- The Journal of Physical Chemistry B, Vol. 105, Issue 44
Molecular Dynamics Study on the Solvent Dependent Heme Cooling Following Ligand Photolysis in Carbonmonoxy Myoglobin
journal, March 2007
- Zhang, Yong; Fujisaki, Hiroshi; Straub, John E.
- The Journal of Physical Chemistry B, Vol. 111, Issue 12
Femtosecond X-ray Absorption Spectroscopy at a Hard X-ray Free Electron Laser: Application to Spin Crossover Dynamics
journal, January 2013
- Lemke, Henrik T.; Bressler, Christian; Chen, Lin X.
- The Journal of Physical Chemistry A, Vol. 117, Issue 4
Tracking the structural dynamics of proteins in solution using time-resolved wide-angle X-ray scattering
journal, September 2008
- Cammarata, Marco; Levantino, Matteo; Schotte, Friedrich
- Nature Methods, Vol. 5, Issue 10
Achieving few-femtosecond time-sorting at hard X-ray free-electron lasers
journal, February 2013
- Harmand, M.; Coffee, R.; Bionta, M. R.
- Nature Photonics, Vol. 7, Issue 3
Photolysis-induced structural changes in single crystals of carbonmonoxy myoglobin at 40 K
journal, October 1994
- Teng, T. -Y.; Šrajer, V.; Moffat, K.
- Nature Structural & Molecular Biology, Vol. 1, Issue 10
Probing the electronic and geometric structure of ferric and ferrous myoglobins in physiological solutions by Fe K-edge absorption spectroscopy
journal, January 2014
- Lima, Frederico A.; Penfold, Thomas J.; van der Veen, Renske M.
- Phys. Chem. Chem. Phys., Vol. 16, Issue 4
Primary protein response after ligand photodissociation in carbonmonoxy myoglobin
journal, May 2007
- Sato, A.; Gao, Y.; Kitagawa, T.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 23
Complex landscape of protein structural dynamics unveiled by nanosecond Laue crystallography
journal, July 2003
- Bourgeois, D.; Vallone, B.; Schotte, F.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 15
Femtosecond photolysis of CO-ligated protoheme and hemoproteins: appearance of deoxy species with a 350-fsec time constant.
journal, January 1983
- Martin, J. L.; Migus, A.; Poyart, C.
- Proceedings of the National Academy of Sciences, Vol. 80, Issue 1
Protein states and proteinquakes.
journal, August 1985
- Ansari, A.; Berendzen, J.; Bowne, S. F.
- Proceedings of the National Academy of Sciences, Vol. 82, Issue 15
Molecular dynamics simulation of photodissociation of carbon monoxide from hemoglobin.
journal, April 1985
- Henry, E. R.; Levitt, M.; Eaton, W. A.
- Proceedings of the National Academy of Sciences, Vol. 82, Issue 7
Molecular dynamics simulations of cooling in laser-excited heme proteins.
journal, December 1986
- Henry, E. R.; Eaton, W. A.; Hochstrasser, R. M.
- Proceedings of the National Academy of Sciences, Vol. 83, Issue 23
Quantitative Analysis of X-Ray Absorption Near Edge Structure Data by a Full Multiple Scattering Procedure: The Fe-CO Geometry in Photolyzed Carbonmonoxy-Myoglobin Single Crystal
journal, September 2001
- Longa, S. Della; Arcovito, A.; Girasole, M.
- Physical Review Letters, Vol. 87, Issue 15
Femtosecond XANES Study of the Light-Induced Spin Crossover Dynamics in an Iron(II) Complex
journal, January 2009
- Bressler, Ch.; Milne, C.; Pham, V. -T.
- Science, Vol. 323, Issue 5913
Direct Observation of Cooling of Heme Upon Photodissociation of Carbonmonoxy Myoglobin
journal, October 1997
- Mizutani, Y.
- Science, Vol. 278, Issue 5337
Observation of coherent reaction dynamics in heme proteins
journal, October 1994
- Zhu, L.; Sage, J.; Champion, P.
- Science, Vol. 266, Issue 5185
Femtosecond Biology
journal, June 1992
- Martin, J. L.; Vos, M. H.
- Annual Review of Biophysics and Biomolecular Structure, Vol. 21, Issue 1
Light-Induced Relaxation of Photolyzed Carbonmonoxy Myoglobin: A Temperature-Dependent X-Ray Absorption Near-Edge Structure (XANES) Study
journal, April 2005
- Arcovito, A.; Lamb, D. C.; Nienhaus, G. U.
- Biophysical Journal, Vol. 88, Issue 4
Works referencing / citing this record:
Activation of coherent lattice phonon following ultrafast molecular spin-state photo-switching: A molecule-to-lattice energy transfer
journal, November 2015
- Marino, A.; Cammarata, M.; Matar, S. F.
- Structural Dynamics, Vol. 3, Issue 2
Direct observation of ultrafast collective motions in CO myoglobin upon ligand dissociation
journal, September 2015
- Barends, T. R. M.; Foucar, L.; Ardevol, A.
- Science, Vol. 350, Issue 6259
Time-resolved X-ray spectroscopies of chemical systems: New perspectives
journal, May 2016
- Chergui, Majed
- Structural Dynamics, Vol. 3, Issue 3
Short-wavelength free-electron laser sources and science: a review
journal, October 2017
- Seddon, E. A.; Clarke, J. A.; Dunning, D. J.
- Reports on Progress in Physics, Vol. 80, Issue 11
Resolving structures of transition metal complex reaction intermediates with femtosecond EXAFS
journal, January 2020
- Britz, Alexander; Abraham, Baxter; Biasin, Elisa
- Physical Chemistry Chemical Physics, Vol. 22, Issue 5
Perspective: Opportunities for ultrafast science at SwissFEL
text, January 2017
- Abela, Rafael; Beaud, Paul; Van Bokhoven, Jeroen A.
- AIP Publishing
Disentangling Ultrafast Electronic and Structural Dynamics with X-Ray Lasers
journal, September 2018
- Collet, Eric; Cammarata, Marco
- Chemistry - A European Journal, Vol. 24, Issue 59
Ultrafast carbon monoxide photolysis and heme spin-crossover in myoglobin via nonadiabatic quantum dynamics
journal, October 2018
- Falahati, Konstantin; Tamura, Hiroyuki; Burghardt, Irene
- Nature Communications, Vol. 9, Issue 1
Short-wavelength free-electron laser sources and science: a review
text, January 2017
- Seddon, E. A.; Clarke, J. A.; Dunning, D. J.
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Dynamics of proteins in solution
journal, January 2019
- Grimaldo, Marco; Roosen-Runge, Felix; Zhang, Fajun
- Quarterly Reviews of Biophysics, Vol. 52
Perspective: Opportunities for ultrafast science at SwissFEL
journal, November 2017
- Abela, Rafael; Beaud, Paul; van Bokhoven, Jeroen A.
- Structural Dynamics, Vol. 4, Issue 6
Linac Coherent Light Source: The first five years
journal, March 2016
- Bostedt, Christoph; Boutet, Sébastien; Fritz, David M.
- Reviews of Modern Physics, Vol. 88, Issue 1
Ultrafast carbon monoxide photolysis and heme spin-crossover in myoglobin via nonadiabatic quantum dynamics
text, January 2017
- Falahati, K.; Tamura, H.; Burghardt, H.
- arXiv
Perspective: Opportunities for ultrafast science at SwissFEL
text, January 2017
- Abela, Rafael; Beaud, Paul; Van Bokhoven, Jeroen A.
- ETH Zurich
Activation of coherent lattice phonon following ultrafast molecular spin-state photo-switching: A molecule-to-lattice energy transfer
journal, November 2015
- Marino, A.; Cammarata, M.; Matar, S. F.
- Structural Dynamics, Vol. 3, Issue 2
Time-resolved X-ray spectroscopies of chemical systems: New perspectives
journal, May 2016
- Chergui, Majed
- Structural Dynamics, Vol. 3, Issue 3