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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]
+ Show Author Affiliations
  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:
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.
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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
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Levantino, M., Lemke, H. T., Schirò, G., Glownia, M., Cupane, A., and Cammarata, M. Wed . "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.
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@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},
journal = {Structural Dynamics},
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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https://doi.org/10.1063/1.4921907
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X-ray absorption spectra: K-edges of 3d transition metals, L-edges of 3d and 4d metals, and M-edges of palladium
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Fluorescence detection of EXAFS: Sensitivity enhancement for dilute species and thin films
journal, December 1993

New insight into metalloporphyrin excited state structures and axial ligand binding from X-ray transient absorption spectroscopic studies
journal, October 2014

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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
journal, May 2002

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journal, November 2001

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

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  • DOI: 10.1021/jp065877k

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
  • DOI: 10.1021/jp312559h

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
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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

  • Teng, T. -Y.; Šrajer, V.; Moffat, K.
  • Nature Structural & Molecular Biology, Vol. 1, Issue 10
  • DOI: 10.1038/nsb1094-701

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
  • DOI: 10.1039/c3cp53683a

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
  • DOI: 10.1073/pnas.0611560104

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
  • DOI: 10.1073/pnas.1430900100

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
  • DOI: 10.1073/pnas.80.1.173

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
  • DOI: 10.1073/pnas.82.15.5000

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
  • DOI: 10.1073/pnas.82.7.2034

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
  • DOI: 10.1073/pnas.83.23.8982

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
journal, October 1994

Femtosecond Biology
journal, June 1992

Light-Induced Relaxation of Photolyzed Carbonmonoxy Myoglobin: A Temperature-Dependent X-Ray Absorption Near-Edge Structure (XANES) Study
journal, April 2005

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