Monitoring Long-Range Electron Transfer Pathways in Proteins by Stimulated Attosecond Broadband X-ray Raman Spectroscopy
Abstract
In this study, long-range electron transfer (ET) plays a key role in many biological energy conversion and synthesis processes. We show that nonlinear spectroscopy with attosecond X-ray pulses provides a real time movie of the evolving oxidation states and electron densities around atoms, and can probe these processes with high spatial and temporal resolution. This is demonstrated in a simulation study of the stimulated X-ray Raman (SXRS) signals in Re-modified azurin, which had long served as a benchmark for long-range ET in proteins. Nonlinear SXRS signals are sensitive to the local electronic structure and should offer a novel window for long-range ET.
- Authors:
-
- Department of Chemistry, University of California, 450 Rowland Hall, Irvine, California 92697, United States
- William R. Wiley Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, P.O. Box 999, Richland, Washington 99352, United States
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (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:
- 1163490
- Alternate Identifier(s):
- OSTI ID: 1167649
- Report Number(s):
- PNNL-SA-102075
Journal ID: ISSN 1948-7185
- Grant/Contract Number:
- ER15571; AC05-76RL01830
- Resource Type:
- Published Article
- Journal Name:
- Journal of Physical Chemistry Letters
- Additional Journal Information:
- Journal Name: Journal of Physical Chemistry Letters Journal Volume: 5 Journal Issue: 21; Journal ID: ISSN 1948-7185
- Publisher:
- American Chemical Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; attosecond; X-ray; Raman; spectroscopy; electron transfer; oxidation; Environmental Molecular Sciences Laboratory
Citation Formats
Zhang, Yu, Biggs, Jason D., Govind, Niranjan, and Mukamel, Shaul. Monitoring Long-Range Electron Transfer Pathways in Proteins by Stimulated Attosecond Broadband X-ray Raman Spectroscopy. United States: N. p., 2014.
Web. doi:10.1021/jz501966h.
Zhang, Yu, Biggs, Jason D., Govind, Niranjan, & Mukamel, Shaul. Monitoring Long-Range Electron Transfer Pathways in Proteins by Stimulated Attosecond Broadband X-ray Raman Spectroscopy. United States. https://doi.org/10.1021/jz501966h
Zhang, Yu, Biggs, Jason D., Govind, Niranjan, and Mukamel, Shaul. Tue .
"Monitoring Long-Range Electron Transfer Pathways in Proteins by Stimulated Attosecond Broadband X-ray Raman Spectroscopy". United States. https://doi.org/10.1021/jz501966h.
@article{osti_1163490,
title = {Monitoring Long-Range Electron Transfer Pathways in Proteins by Stimulated Attosecond Broadband X-ray Raman Spectroscopy},
author = {Zhang, Yu and Biggs, Jason D. and Govind, Niranjan and Mukamel, Shaul},
abstractNote = {In this study, long-range electron transfer (ET) plays a key role in many biological energy conversion and synthesis processes. We show that nonlinear spectroscopy with attosecond X-ray pulses provides a real time movie of the evolving oxidation states and electron densities around atoms, and can probe these processes with high spatial and temporal resolution. This is demonstrated in a simulation study of the stimulated X-ray Raman (SXRS) signals in Re-modified azurin, which had long served as a benchmark for long-range ET in proteins. Nonlinear SXRS signals are sensitive to the local electronic structure and should offer a novel window for long-range ET.},
doi = {10.1021/jz501966h},
journal = {Journal of Physical Chemistry Letters},
number = 21,
volume = 5,
place = {United States},
year = {Tue Oct 14 00:00:00 EDT 2014},
month = {Tue Oct 14 00:00:00 EDT 2014}
}
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https://doi.org/10.1021/jz501966h
https://doi.org/10.1021/jz501966h
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Cited by: 16 works
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Works referenced in this record:
Proteins as Electronic Materials: Electron Transport through Solid-State Protein Monolayer Junctions
journal, March 2010
- Ron, Izhar; Sepunaru, Lior; Itzhakov, Stella
- Journal of the American Chemical Society, Vol. 132, Issue 12
Tryptophan-Accelerated Electron Flow Through Proteins
journal, June 2008
- Shih, C.; Museth, A. K.; Abrahamsson, M.
- Science, Vol. 320, Issue 5884
Solvent Reorganization in Long-Range Electron Transfer: Density Matrix Approach
journal, February 1998
- Okada, Akira; Chernyak, Vladimir; Mukamel, Shaul
- The Journal of Physical Chemistry A, Vol. 102, Issue 8
Electron hopping through proteins
journal, November 2012
- Warren, Jeffrey J.; Ener, Maraia E.; Vlček, Antonín
- Coordination Chemistry Reviews, Vol. 256, Issue 21-22
Molecular Imaging Using X-Ray Free-Electron Lasers
journal, April 2013
- Barty, Anton; Küpper, Jochen; Chapman, Henry N.
- Annual Review of Physical Chemistry, Vol. 64, Issue 1
Electron transfers in chemistry and biology
journal, August 1985
- Marcus, R. A.; Sutin, Norman
- Biochimica et Biophysica Acta (BBA) - Reviews on Bioenergetics, Vol. 811, Issue 3
Radical Initiation in the Class I Ribonucleotide Reductase: Long-Range Proton-Coupled Electron Transfer?
journal, June 2003
- Stubbe, JoAnne; Nocera, Daniel G.; Yee, Cyril S.
- Chemical Reviews, Vol. 103, Issue 6
Long-range photoinduced electron transfer through a DNA helix
journal, November 1993
- Murphy, C.; Arkin, M.; Jenkins, Y.
- Science, Vol. 262, Issue 5136
First lasing and operation of an ångstrom-wavelength free-electron laser
journal, August 2010
- Emma, P.; Akre, R.; Arthur, J.
- Nature Photonics, Vol. 4, Issue 9
Molecular bioelectronics
journal, January 2005
- Davis, J. J.; Morgan, D. A.; Wrathmell, C. L.
- Journal of Materials Chemistry, Vol. 15, Issue 22
Long-Range Electron Tunneling
journal, February 2014
- Winkler, Jay R.; Gray, Harry B.
- Journal of the American Chemical Society, Vol. 136, Issue 8
Applications of 2D IR Spectroscopy to Peptides, Proteins, and Hydrogen-Bond Dynamics †
journal, June 2009
- Kim, Yung Sam; Hochstrasser, Robin M.
- The Journal of Physical Chemistry B, Vol. 113, Issue 24
Properties of Photogenerated Tryptophan and Tyrosyl Radicals in Structurally Characterized Proteins Containing Rhenium(I) Tricarbonyl Diimines
journal, April 2001
- Di Bilio, Angel J.; Crane, Brian R.; Wehbi, William A.
- Journal of the American Chemical Society, Vol. 123, Issue 13
Molecular scale bioelectrochemistry
journal, September 2011
- Patil, A. V.; Davis, J. J.
- Coordination Chemistry Reviews, Vol. 255, Issue 17-18
Energy Conversion in Photosynthesis: A Paradigm for Solar Fuel Production
journal, March 2011
- Moore, Gary F.; Brudvig, Gary W.
- Annual Review of Condensed Matter Physics, Vol. 2, Issue 1
Two-dimensional stimulated resonance Raman spectroscopy of molecules with broadband x-ray pulses
journal, May 2012
- Biggs, Jason D.; Zhang, Yu; Healion, Daniel
- The Journal of Chemical Physics, Vol. 136, Issue 17, Article No. 174117
Multidimensional x-ray spectroscopy of valence and core excitations in cysteine
journal, April 2013
- Biggs, Jason D.; Zhang, Yu; Healion, Daniel
- The Journal of Chemical Physics, Vol. 138, Issue 14
The kinetics of electron transfer between pseudomonas aeruginosa cytochrome c-551 and its oxidase
journal, May 1982
- Silvestrini, M. C.; Tordi, M. G.; Colosimo, A.
- Biochemical Journal, Vol. 203, Issue 2
Femtosecond Stimulated Raman Spectroscopy
journal, May 2007
- Kukura, Philipp; McCamant, David W.; Mathies, Richard A.
- Annual Review of Physical Chemistry, Vol. 58, Issue 1
Experimental Demonstration of Femtosecond Two-Color X-Ray Free-Electron Lasers
journal, March 2013
- Lutman, A. A.; Coffee, R.; Ding, Y.
- Physical Review Letters, Vol. 110, Issue 13
Stimulated X-ray emission for materials science
journal, August 2013
- Beye, M.; Schreck, S.; Sorgenfrei, F.
- Nature, Vol. 501, Issue 7466
Proton-Coupled Electron Transfer in Cytochrome Oxidase
journal, December 2010
- Kaila, Ville R. I.; Verkhovsky, Michael I.; Wikström, Mårten
- Chemical Reviews, Vol. 110, Issue 12
Structure and Function of DNA Photolyase and Cryptochrome Blue-Light Photoreceptors
journal, June 2003
- Sancar, Aziz
- Chemical Reviews, Vol. 103, Issue 6
Tryptophan-Accelerated Electron Flow Across a Protein–Protein Interface
journal, October 2013
- Takematsu, Kana; Williamson, Heather; Blanco-Rodríguez, Ana María
- Journal of the American Chemical Society, Vol. 135, Issue 41
Multidimensional Attosecond Resonant X-Ray Spectroscopy of Molecules: Lessons from the Optical Regime
journal, April 2013
- Mukamel, Shaul; Healion, Daniel; Zhang, Yu
- Annual Review of Physical Chemistry, Vol. 64, Issue 1
Photochemical Processes Revealed by X-ray Transient Absorption Spectroscopy
journal, November 2013
- Chen, Lin X.; Zhang, Xiaoyi
- The Journal of Physical Chemistry Letters, Vol. 4, Issue 22
Long-range charge hopping in DNA
journal, October 1999
- Bixon, M.; Giese, B.; Wessely, S.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 21
Phototriggering Electron Flow through Re I ‐modified Pseudomonas aeruginosa Azurins
journal, April 2011
- Blanco‐Rodríguez, Ana María; Di Bilio, Angel J.; Shih, Crystal
- Chemistry – A European Journal, Vol. 17, Issue 19
Femtosecond Crystallography with Ultrabright Electrons and X-rays: Capturing Chemistry in Action
journal, March 2014
- Miller, R. J. D.
- Science, Vol. 343, Issue 6175