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Title: 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:
 [1];  [2];  [3];  [2];  [1];  [4]
  1. Univ. of Palermo, Palermo (Italy)
  2. SLAC National Accelerator Lab., Menlo Park, CA (United States)
  3. CNRS - Institut de Biologie Structurale, Grenoble 38044, France
  4. 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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Citation Metrics:
Cited by: 36 works
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Works referenced in this record:

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Fluorescence detection of EXAFS: Sensitivity enhancement for dilute species and thin films
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New insight into metalloporphyrin excited state structures and axial ligand binding from X-ray transient absorption spectroscopic studies
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Heme Photolysis Occurs by Ultrafast Excited State Metal-to-Ring Charge Transfer
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Picosecond Raman study of energy flow in a photoexcited heme protein
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Picosecond time-resolved Raman studies of photodissociated carboxymyoglobin
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Measurements of the Photodissociation Quantum Yields of MbNO and MbO 2 and the Vibrational Relaxation of the Six-Coordinate Heme Species
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Ultrafast Structural Relaxation of Myoglobin Following Photodissociation of Carbon Monoxide Probed by Time-Resolved Resonance Raman Spectroscopy
journal, November 2001


Molecular Dynamics Study on the Solvent Dependent Heme Cooling Following Ligand Photolysis in Carbonmonoxy Myoglobin
journal, March 2007


Femtosecond X-ray Absorption Spectroscopy at a Hard X-ray Free Electron Laser: Application to Spin Crossover Dynamics
journal, January 2013


Tracking the structural dynamics of proteins in solution using time-resolved wide-angle X-ray scattering
journal, September 2008


Achieving few-femtosecond time-sorting at hard X-ray free-electron lasers
journal, February 2013


Photolysis-induced structural changes in single crystals of carbonmonoxy myoglobin at 40 K
journal, October 1994


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Primary protein response after ligand photodissociation in carbonmonoxy myoglobin
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journal, July 2003


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journal, January 1983


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journal, August 1985


Molecular dynamics simulation of photodissociation of carbon monoxide from hemoglobin.
journal, April 1985


Molecular dynamics simulations of cooling in laser-excited heme proteins.
journal, December 1986


Femtosecond XANES Study of the Light-Induced Spin Crossover Dynamics in an Iron(II) Complex
journal, January 2009


Observation of coherent reaction dynamics in heme proteins
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journal, June 1992


Works referencing / citing this record:

Direct observation of ultrafast collective motions in CO myoglobin upon ligand dissociation
journal, September 2015


Time-resolved X-ray spectroscopies of chemical systems: New perspectives
journal, May 2016


Short-wavelength free-electron laser sources and science: a review
journal, October 2017


Resolving structures of transition metal complex reaction intermediates with femtosecond EXAFS
journal, January 2020


Perspective: Opportunities for ultrafast science at SwissFEL
text, January 2017


Disentangling Ultrafast Electronic and Structural Dynamics with X-Ray Lasers
journal, September 2018


Ultrafast carbon monoxide photolysis and heme spin-crossover in myoglobin via nonadiabatic quantum dynamics
journal, October 2018


Short-wavelength free-electron laser sources and science: a review
text, January 2017


Dynamics of proteins in solution
journal, January 2019


Perspective: Opportunities for ultrafast science at SwissFEL
journal, November 2017


Linac Coherent Light Source: The first five years
journal, March 2016


Perspective: Opportunities for ultrafast science at SwissFEL
text, January 2017


Time-resolved X-ray spectroscopies of chemical systems: New perspectives
journal, May 2016