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Title: Observation of Terahertz Vibrations in Pyrococcus Furiosus Rubredoxin Via Impulsive Coherent Vibrational Spectroscopy and Nuclear Resonance Vibrational Spectroscopy – Interpretation by Molecular Mechanics

Abstract

The research described in this product was performed in part in the Environmental Molecular Sciences Laboratory, a national scientific user facility sponsored by the Department of Energy's Office of Biological and Environmental Research and located at Pacific Northwest National Laboratory. We have used impulsive coherent vibrational spectroscopy (ICVS) to study the Fe(S-Cys)4 site in oxidized rubredoxin (Rd) from Pyrococcus furiosus (Pf). In this experiment, a 15 fs visible laser pulse is used to coherently pump the sample to an excited electronic state, and a second <10 fs pulse is used to probe the change in transmission as a function of the time delay. PfRd was observed to relax to the ground state by a single exponential decay with time constants of ~255–275 fs. Superimposed on this relaxation are oscillations caused by coherent excitation of vibrational modes in both excited and ground electronic states. Fourier transformation reveals the frequencies of these modes. The strongest ICV mode with 570 nm excitation is the symmetric Fe–S stretching mode near 310 cm⁻1, compared to 313 cm⁻1 in the low temperature resonance Raman. If the rubredoxin is pumped at 520 nm, a set of strong bands occurs between 20 and 110 cm⁻1. Finally, there ismore » a mode at ~500 cm⁻1 which is similar to features near 508 cm⁻1 in blue Cu proteins that have been attributed to excited state vibrations. Normal mode analysis using 488 protein atoms and 558 waters gave calculated spectra that are in good agreement with previous nuclear resonance vibrational spectra (NRVS) results. The lowest frequency normal modes are identified as collective motions of the entire protein or large segments of polypeptide. Motion in these modes may affect the polar environment of the redox site and thus tune the electron transfer functions in rubredoxins.« less

Authors:
; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1001565
DOE Contract Number:
AC05-76RL01830
Resource Type:
Journal Article
Resource Relation:
Journal Name: Journal of Inorganic Biochemistry, 101(3):375-384; Journal Volume: 101; Journal Issue: 3
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 99 GENERAL AND MISCELLANEOUS//MATHEMATICS, COMPUTING, AND INFORMATION SCIENCE; ATOMS; DECAY; ELECTRON TRANSFER; EXCITATION; EXCITED STATES; FOURIER TRANSFORMATION; GROUND STATES; LASERS; NORMAL-MODE ANALYSIS; OSCILLATIONS; PROBES; PROTEINS; RELAXATION; RESONANCE; RUBREDOXIN; SPECTRA; SPECTROSCOPY; TIME DELAY; Environmental Molecular Sciences Laboratory

Citation Formats

Tan, Ming-Liang, Bizzarri, Anna R., Xiao, Yuming, Cannistraro, Salvatore, Ichiye, Toshiko, Manzoni, Cristian, Cerullo, Giulio, Adams, Michael W., Jenney, Francis E., and Cramer, Stephen P.. Observation of Terahertz Vibrations in Pyrococcus Furiosus Rubredoxin Via Impulsive Coherent Vibrational Spectroscopy and Nuclear Resonance Vibrational Spectroscopy – Interpretation by Molecular Mechanics. United States: N. p., 2007. Web. doi:10.1016/j.jinorgbio.2006.09.031.
Tan, Ming-Liang, Bizzarri, Anna R., Xiao, Yuming, Cannistraro, Salvatore, Ichiye, Toshiko, Manzoni, Cristian, Cerullo, Giulio, Adams, Michael W., Jenney, Francis E., & Cramer, Stephen P.. Observation of Terahertz Vibrations in Pyrococcus Furiosus Rubredoxin Via Impulsive Coherent Vibrational Spectroscopy and Nuclear Resonance Vibrational Spectroscopy – Interpretation by Molecular Mechanics. United States. doi:10.1016/j.jinorgbio.2006.09.031.
Tan, Ming-Liang, Bizzarri, Anna R., Xiao, Yuming, Cannistraro, Salvatore, Ichiye, Toshiko, Manzoni, Cristian, Cerullo, Giulio, Adams, Michael W., Jenney, Francis E., and Cramer, Stephen P.. Thu . "Observation of Terahertz Vibrations in Pyrococcus Furiosus Rubredoxin Via Impulsive Coherent Vibrational Spectroscopy and Nuclear Resonance Vibrational Spectroscopy – Interpretation by Molecular Mechanics". United States. doi:10.1016/j.jinorgbio.2006.09.031.
@article{osti_1001565,
title = {Observation of Terahertz Vibrations in Pyrococcus Furiosus Rubredoxin Via Impulsive Coherent Vibrational Spectroscopy and Nuclear Resonance Vibrational Spectroscopy – Interpretation by Molecular Mechanics},
author = {Tan, Ming-Liang and Bizzarri, Anna R. and Xiao, Yuming and Cannistraro, Salvatore and Ichiye, Toshiko and Manzoni, Cristian and Cerullo, Giulio and Adams, Michael W. and Jenney, Francis E. and Cramer, Stephen P.},
abstractNote = {The research described in this product was performed in part in the Environmental Molecular Sciences Laboratory, a national scientific user facility sponsored by the Department of Energy's Office of Biological and Environmental Research and located at Pacific Northwest National Laboratory. We have used impulsive coherent vibrational spectroscopy (ICVS) to study the Fe(S-Cys)4 site in oxidized rubredoxin (Rd) from Pyrococcus furiosus (Pf). In this experiment, a 15 fs visible laser pulse is used to coherently pump the sample to an excited electronic state, and a second <10 fs pulse is used to probe the change in transmission as a function of the time delay. PfRd was observed to relax to the ground state by a single exponential decay with time constants of ~255–275 fs. Superimposed on this relaxation are oscillations caused by coherent excitation of vibrational modes in both excited and ground electronic states. Fourier transformation reveals the frequencies of these modes. The strongest ICV mode with 570 nm excitation is the symmetric Fe–S stretching mode near 310 cm⁻1, compared to 313 cm⁻1 in the low temperature resonance Raman. If the rubredoxin is pumped at 520 nm, a set of strong bands occurs between 20 and 110 cm⁻1. Finally, there is a mode at ~500 cm⁻1 which is similar to features near 508 cm⁻1 in blue Cu proteins that have been attributed to excited state vibrations. Normal mode analysis using 488 protein atoms and 558 waters gave calculated spectra that are in good agreement with previous nuclear resonance vibrational spectra (NRVS) results. The lowest frequency normal modes are identified as collective motions of the entire protein or large segments of polypeptide. Motion in these modes may affect the polar environment of the redox site and thus tune the electron transfer functions in rubredoxins.},
doi = {10.1016/j.jinorgbio.2006.09.031},
journal = {Journal of Inorganic Biochemistry, 101(3):375-384},
number = 3,
volume = 101,
place = {United States},
year = {Thu Mar 01 00:00:00 EST 2007},
month = {Thu Mar 01 00:00:00 EST 2007}
}
  • We have used {sup 57}Fe nuclear resonance vibrational spectroscopy (NRVS) to study the Fe(S{sub cys})4 site in reduced and oxidized rubredoxin (Rd) from Pyrococcus furiosus (Pf). The oxidized form has also been investigated by resonance Raman spectroscopy. In the oxidized Rd NRVS, strong asymmetric Fe-S stretching modes are observed between 355 and 375 cm{sup -1}; upon reduction these modes shift to 300-320 cm{sup -1}. This is the first observation of Fe-S stretching modes in a reduced Rd. The peak in S-Fe-S bend mode intensity is at {approx}150 cm{sup -1} for the oxidized protein and only slightly lower in the reducedmore » case. A third band occurs near 70 cm{sup -1} for both samples; this is assigned primarily as a collective motion of entire cysteine residues with respect to the central Fe. The {sup 57}Fe partial vibrational density of states (PVDOS) were interpreted by normal mode analysis with optimization of Urey-Bradley force fields. The three main bands were qualitatively reproduced using a D{sub 2d} Fe(SC){sub 4} model. A C{sub 1} Fe(SCC){sub 4} model based on crystallographic coordinates was then used to simulate the splitting of the asymmetric stretching band into at least 3 components. Finally, a model employing complete cysteines and 2 additional neighboring atoms was used to reproduce the detailed structure of the PVDOS in the Fe-S stretch region. These results confirm the delocalization of the dynamic properties of the redox-active Fe site. Depending on the molecular model employed, the force constant KFe-S for Fe-S stretching modes ranged from 1.24 to 1.32 mdyn/Angstrom. KFe-S is clearly diminished in reduced Rd; values from {approx}0.89 to 1.00 mdyn/Angstrom were derived from different models. In contrast, in the final models the force constants for S-Fe-S bending motion, HS-Fe-S, were 0.18 mdyn/Angstrom for oxidized Rd and 0.15 mdyn/Angstrom for reduced Rd. The NRVS technique demonstrates great promise for the observation and quantitative interpretation of the dynamical properties of Fe-S proteins.« less
  • No abstract prepared.
  • In this communication the authors present new experiments and theoretical simulations, using iron L-edge X-ray absorption spectroscopy, to study the metalloprotein Pyrococcus furiosus rubredoxin. the 3d transition metal L-edges are found between 400 and 1100 eV, in the soft X-ray region. Synchrotron radiation beam lines producing the high photon flux and high-energy resolution necessary to observe and resolve 3d transition metal L-edge spectra have only become available in the last few years. L-edge spectra are interesting not only because of the 3-4-fold-higher energy resolution (vs K-edges) but also for the sensitivity to spin state, oxidation state, and ligand field offeredmore » by p{r_arrow}d transitions. In addition, the X-ray magnetic circular dichroism (XMCD) of transition metal L-edges is predicted to be strong, and experiments have confirmed these predictions. 21 refs., 1 fig.« less
  • Neutron crystallography is used to locate hydrogen atoms in biological materials and can distinguish between negatively scattering hydrogen and positively scattering deuterium substituted positions in isomorphous neutron structures. Recently, Hauptman and Langs (2003) have shown that neutron diffraction data can be used to solve macromolecular structures by direct methods and that solution is aided by the presence of negatively scattering hydrogen atoms in the structure. Selective labeling protocols allow the design and production of H/D-labeled macromolecular structures in which the ratio of hydrogen to deuterium atoms can be precisely controlled. We have applied methyl-selective labeling protocols to introduce (1H-delta methyl)-leucinemore » and (1H-gamma methyl)-valine into deuterated rubredoxin from Pyrococcus furiosus (PfRd). Here we report on the production, crystallization, and preliminary neutron analysis of the selectively CH3-protonated, deuterated PfRd sample, which provided a high quality neutron data set extending to 1.75 resolution at the new LADI-III instrument at the Insititut Laue-Langevin. Preliminary analysis of neutron density maps allows unambiguous assignment of the positions of hydrogen atoms at the methyl groups of the valine and leucine residues in the otherwise deuterated rubredoxin structure.« less