High-pressure dynamics of hydrated protein in bioprotective trehalose environment
Abstract
Here we present a pressure-dependence study of the dynamics of lysozyme protein powder immersed in deuterated , α-trehalose environment via quasielastic neutron scattering (QENS). The goal is to assess the baroprotective benefits of trehalose on biomolecules by comparing the findings with those of a trehalose-free reference study. While the mean-square displacement of the trehalose-free protein (hydrated to dD₂O ≃40 w%) as a whole, is reduced by increasing pressure, the actual observable relaxation dynamics in the picoseconds to nanoseconds time range remains largely unaffected by pressure up to the maximum investigated pressure of 2.78(2) Kbar. Our observation is independent of whether or not the protein is mixed with the deuterated sugar. This suggests that the hydrated protein s conformational states at atmospheric pressure remain unaltered by hydrostatic pressures, below 2.78 Kbar. We also found the QENS response to be totally recoverable after ambient pressure conditions are restored. Small-angle neutron diffraction measurements confirm that the protein-protein correlation remains undisturbed.We observe, however, a clear narrowing of the QENS response as the temperature is decreased from 290 to 230 K in both cases, which we parametrize using the Kohlrausch-Williams-Watts stretched exponential model. Finally, only the fraction of protons that are immobile on the accessiblemore »
- Authors:
-
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Quantum Condensed Matter Division
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biology and Soft Matter Division
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical and Engineering Science Division
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Spallation Neutron Source (SNS)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1286756
- Alternate Identifier(s):
- OSTI ID: 1181099
- Grant/Contract Number:
- AC05-00OR22725; ERKP291
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Physical Review. E, Statistical, Nonlinear, and Soft Matter Physics
- Additional Journal Information:
- Journal Volume: 90; Journal Issue: 4; Journal ID: ISSN 1539-3755
- Publisher:
- American Physical Society (APS)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; High Pressure; Protein Dynamics; Quasi-elastic neutron scattering
Citation Formats
Diallo, S. O., Zhang, Q., O'Neill, H., and Mamontov, E. High-pressure dynamics of hydrated protein in bioprotective trehalose environment. United States: N. p., 2014.
Web. doi:10.1103/PhysRevE.90.042725.
Diallo, S. O., Zhang, Q., O'Neill, H., & Mamontov, E. High-pressure dynamics of hydrated protein in bioprotective trehalose environment. United States. https://doi.org/10.1103/PhysRevE.90.042725
Diallo, S. O., Zhang, Q., O'Neill, H., and Mamontov, E. Thu .
"High-pressure dynamics of hydrated protein in bioprotective trehalose environment". United States. https://doi.org/10.1103/PhysRevE.90.042725. https://www.osti.gov/servlets/purl/1286756.
@article{osti_1286756,
title = {High-pressure dynamics of hydrated protein in bioprotective trehalose environment},
author = {Diallo, S. O. and Zhang, Q. and O'Neill, H. and Mamontov, E.},
abstractNote = {Here we present a pressure-dependence study of the dynamics of lysozyme protein powder immersed in deuterated , α-trehalose environment via quasielastic neutron scattering (QENS). The goal is to assess the baroprotective benefits of trehalose on biomolecules by comparing the findings with those of a trehalose-free reference study. While the mean-square displacement of the trehalose-free protein (hydrated to dD₂O ≃40 w%) as a whole, is reduced by increasing pressure, the actual observable relaxation dynamics in the picoseconds to nanoseconds time range remains largely unaffected by pressure up to the maximum investigated pressure of 2.78(2) Kbar. Our observation is independent of whether or not the protein is mixed with the deuterated sugar. This suggests that the hydrated protein s conformational states at atmospheric pressure remain unaltered by hydrostatic pressures, below 2.78 Kbar. We also found the QENS response to be totally recoverable after ambient pressure conditions are restored. Small-angle neutron diffraction measurements confirm that the protein-protein correlation remains undisturbed.We observe, however, a clear narrowing of the QENS response as the temperature is decreased from 290 to 230 K in both cases, which we parametrize using the Kohlrausch-Williams-Watts stretched exponential model. Finally, only the fraction of protons that are immobile on the accessible time window of the instrument, referred to as the elastic incoherent structure factor, is observably sensitive to pressure, increasing only marginally but systematically with increasing pressure.},
doi = {10.1103/PhysRevE.90.042725},
journal = {Physical Review. E, Statistical, Nonlinear, and Soft Matter Physics},
number = 4,
volume = 90,
place = {United States},
year = {Thu Oct 30 00:00:00 EDT 2014},
month = {Thu Oct 30 00:00:00 EDT 2014}
}
Web of Science
Works referenced in this record:
Preservation of Membranes in Anhydrobiotic Organisms: The Role of Trehalose
journal, February 1984
- Crowe, J. H.; Crowe, L. M.; Chapman, D.
- Science, Vol. 223, Issue 4637
Slow dynamics of water molecules on the surface of a globular protein
journal, January 1996
- Bellissent-Funel, Marie-Claire; Zanotti, Jean-Marc; Chen, Sow Hsin
- Faraday Discussions, Vol. 103
Solvent effects on protein fast dynamics: implications for biopreservation
journal, January 2013
- Sakai, Victoria García; Khodadadi, Sheila; Cicerone, Marcus T.
- Soft Matter, Vol. 9, Issue 22
Slow dynamics of supercooled water confined in nanoporous silica materials
journal, October 2004
- Liu, L.; Faraone, A.; Mou, C-Y
- Journal of Physics: Condensed Matter, Vol. 16, Issue 45
High-resolution inelastic neutron scattering from water in mesoporous silica
journal, October 2002
- Mansour, F.; Dimeo, R. M.; Peemoeller, H.
- Physical Review E, Vol. 66, Issue 4
How Soft Is a Protein? A Protein Dynamics Force Constant Measured by Neutron Scattering
journal, June 2000
- Zaccai, G.
- Science, Vol. 288, Issue 5471
A high pressure cell for small angle neutron scattering up to 500MPa in combination with light scattering to investigate liquid samples
journal, December 2007
- Kohlbrecher, J.; Bollhalder, A.; Vavrin, R.
- Review of Scientific Instruments, Vol. 78, Issue 12
Hydration and Mobility of Trehalose in Aqueous Solution
journal, July 2012
- Winther, Louise Revsbech; Qvist, Johan; Halle, Bertil
- The Journal of Physical Chemistry B, Vol. 116, Issue 30
Dynamics in Protein Powders on the Nanosecond–Picosecond Time Scale Are Dominated by Localized Motions
journal, September 2013
- Nickels, Jonathan D.; García Sakai, Victoria; Sokolov, Alexei P.
- The Journal of Physical Chemistry B, Vol. 117, Issue 39
Protein dynamics studied by neutron scattering
journal, November 2002
- Gabel, Frank; Bicout, Dominique; Lehnert, Ursula
- Quarterly Reviews of Biophysics, Vol. 35, Issue 4
Dynamical transition of myoglobin revealed by inelastic neutron scattering
journal, February 1989
- Doster, Wolfgang; Cusack, Stephen; Petry, Winfried
- Nature, Vol. 337, Issue 6209
Incoherent neutron scattering functions for random jump diffusion in bounded and infinite media
journal, February 1981
- Hall, Peter L.; Ross, D. K.
- Molecular Physics, Vol. 42, Issue 3
Physiological roles of trehalose in bacteria and yeasts: a comparative analysis
journal, September 2000
- Argüelles, Juan Carlos
- Archives of Microbiology, Vol. 174, Issue 4
The dynamical transition of proteins, concepts and misconceptions
journal, February 2008
- Doster, Wolfgang
- European Biophysics Journal, Vol. 37, Issue 5
A time-of-flight backscattering spectrometer at the Spallation Neutron Source, BASIS
journal, August 2011
- Mamontov, E.; Herwig, K. W.
- Review of Scientific Instruments, Vol. 82, Issue 8
Phase relations and vitrification in saccharide-water solutions and the trehalose anomaly
journal, April 1989
- Green, J. L.; Angell, C. A.
- The Journal of Physical Chemistry, Vol. 93, Issue 8
DAVE: A Comprehensive Software Suite for the Reduction, Visualization, and Analysis of Low Energy Neutron Spectroscopic Data
journal, November 2009
- Azuah, Richard Tumanjong; Kneller, Larry R.; Qiu, Yiming
- Journal of Research of the National Institute of Standards and Technology, Vol. 114, Issue 6
Combining structure and dynamics: non-denaturing high-pressure effect on lysozyme in solution
journal, June 2009
- Ortore, Maria Grazia; Spinozzi, Francesco; Mariani, Paolo
- Journal of The Royal Society Interface, Vol. 6, Issue suppl_5
Energy resolution and dynamical heterogeneity effects on elastic incoherent neutron scattering from molecular systems
journal, February 2003
- Becker, Torsten; Smith, Jeremy C.
- Physical Review E, Vol. 67, Issue 2
Neutron Scattering Study on Dynamics of Water Molecules in MCM-41. 2. Determination of Translational Diffusion Coefficient
journal, June 2005
- Takahara, Shuichi; Sumiyama, Naoya; Kittaka, Shigeharu
- The Journal of Physical Chemistry B, Vol. 109, Issue 22
Equilibrium cluster formation in concentrated protein solutions and colloids
journal, November 2004
- Stradner, Anna; Sedgwick, Helen; Cardinaux, Frédéric
- Nature, Vol. 432, Issue 7016
Mean Square Displacements from Elastic Incoherent Neutron Scattering Evaluated by Spectrometers Working with Different Energy Resolution on Dry and Hydrated (H 2 O and D 2 O) Lysozyme
journal, June 2010
- Magazù, Salvatore; Migliardo, Federica; Benedetto, Antonio
- The Journal of Physical Chemistry B, Vol. 114, Issue 28
Observation of fragile-to-strong dynamic crossover in protein hydration water
journal, June 2006
- Chen, S. -H.; Liu, L.; Fratini, E.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 24
Protein dynamics in solution and powder measured by incoherent elastic neutron scattering: the influence of Q-range and energy resolution
journal, September 2004
- Gabel, Frank
- European Biophysics Journal, Vol. 34, Issue 1
Influence of pressure on the slow and fast fractional relaxation dynamics in lysozyme: A simulation study
journal, February 2008
- Calandrini, Vania; Kneller, Gerald R.
- The Journal of Chemical Physics, Vol. 128, Issue 6
Influence of Hydration on the Dynamics of Lysozyme
journal, October 2006
- Roh, J. H.; Curtis, J. E.; Azzam, S.
- Biophysical Journal, Vol. 91, Issue 7
Hydration-Coupled Dynamics in Proteins Studied by Neutron Scattering and NMR: The Case of the Typical EF-Hand Calcium-Binding Parvalbumin
journal, May 1999
- Zanotti, Jean-Marc; Bellissent-Funel, Marie-Claire; Parello, Joseph
- Biophysical Journal, Vol. 76, Issue 5
Mean-squared atomic displacements in hydrated lysozyme, native and denatured
journal, January 2010
- Mamontov, Eugene; O’Neill, Hugh; Zhang, Qiu
- Journal of Biological Physics, Vol. 36, Issue 3
Role of cavities and hydration in the pressure unfolding of T4 lysozyme
journal, September 2014
- Nucci, N. V.; Fuglestad, B.; Athanasoula, E. A.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 38
Cryptobiosis — a peculiar state of biological organization
journal, April 2001
- Clegg, James S.
- Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, Vol. 128, Issue 4
How Do Trehalose, Maltose, and Sucrose Influence Some Structural and Dynamical Properties of Lysozyme? Insight from Molecular Dynamics Simulations
journal, August 2007
- Lerbret, A.; Bordat, P.; Affouard, F.
- The Journal of Physical Chemistry B, Vol. 111, Issue 31
Study of the relaxational and vibrational dynamics of bioprotectant glass-forming mixtures by neutron scattering and molecular dynamics simulation
journal, May 2010
- Magazù, S.; Migliardo, F.; Affouard, F.
- The Journal of Chemical Physics, Vol. 132, Issue 18