Dynamical Transition of Collective Motions in Dry Proteins
Abstract
Water is widely assumed to be essential for protein dynamics and function. In particular, the well-documented “dynamical” transition at ~ 200 K , at which the protein changes from a rigid, nonfunctional form to a flexible, functional state, as detected in hydrogenated protein by incoherent neutron scattering, requires hydration. We report on coherent neutron scattering experiments on perdeuterated proteins and reveal that a transition occurs in dry proteins at the same temperature resulting primarily from the collective heavy-atom motions. Furthermore, the dynamical transition discovered is intrinsic to the energy landscape of dry proteins.
- Authors:
-
- Shanghai Jiao Tong Univ. (China)
- National Inst. of Standards and Technology (NIST), Shanghai (China)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Spallation Neutron Source (SNS)
- Univ. of Tennessee, Knoxville, TN (United States)
- Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1376609
- Alternate Identifier(s):
- OSTI ID: 1372727
- Grant/Contract Number:
- AC05-00OR22725; DMR-1508249
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Physical Review Letters
- Additional Journal Information:
- Journal Volume: 119; Journal Issue: 4; Journal ID: ISSN 0031-9007
- Publisher:
- American Physical Society (APS)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Liu, Zhuo, Huang, Juan, Tyagi, Madhusudan, O’Neill, Hugh, Zhang, Qiu, Mamontov, Eugene, Jain, Nitin, Wang, Yujie, Zhang, Jie, Smith, Jeremy C., and Hong, Liang. Dynamical Transition of Collective Motions in Dry Proteins. United States: N. p., 2017.
Web. doi:10.1103/PhysRevLett.119.048101.
Liu, Zhuo, Huang, Juan, Tyagi, Madhusudan, O’Neill, Hugh, Zhang, Qiu, Mamontov, Eugene, Jain, Nitin, Wang, Yujie, Zhang, Jie, Smith, Jeremy C., & Hong, Liang. Dynamical Transition of Collective Motions in Dry Proteins. United States. https://doi.org/10.1103/PhysRevLett.119.048101
Liu, Zhuo, Huang, Juan, Tyagi, Madhusudan, O’Neill, Hugh, Zhang, Qiu, Mamontov, Eugene, Jain, Nitin, Wang, Yujie, Zhang, Jie, Smith, Jeremy C., and Hong, Liang. Tue .
"Dynamical Transition of Collective Motions in Dry Proteins". United States. https://doi.org/10.1103/PhysRevLett.119.048101. https://www.osti.gov/servlets/purl/1376609.
@article{osti_1376609,
title = {Dynamical Transition of Collective Motions in Dry Proteins},
author = {Liu, Zhuo and Huang, Juan and Tyagi, Madhusudan and O’Neill, Hugh and Zhang, Qiu and Mamontov, Eugene and Jain, Nitin and Wang, Yujie and Zhang, Jie and Smith, Jeremy C. and Hong, Liang},
abstractNote = {Water is widely assumed to be essential for protein dynamics and function. In particular, the well-documented “dynamical” transition at ~ 200 K , at which the protein changes from a rigid, nonfunctional form to a flexible, functional state, as detected in hydrogenated protein by incoherent neutron scattering, requires hydration. We report on coherent neutron scattering experiments on perdeuterated proteins and reveal that a transition occurs in dry proteins at the same temperature resulting primarily from the collective heavy-atom motions. Furthermore, the dynamical transition discovered is intrinsic to the energy landscape of dry proteins.},
doi = {10.1103/PhysRevLett.119.048101},
journal = {Physical Review Letters},
number = 4,
volume = 119,
place = {United States},
year = {Tue Jul 25 00:00:00 EDT 2017},
month = {Tue Jul 25 00:00:00 EDT 2017}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Cited by: 23 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Nuclear magnetic resonance studies of amino acids and proteins. Deuterium nuclear magnetic resonance relaxation of deuteriomethyl-labeled amino acids in crystals and in Halobacterium halobium and Escherichia coli cell membranes
journal, January 1984
- Keniry, Max A.; Kintanar, Agustin; Smith, Rebecca L.
- Biochemistry, Vol. 23, Issue 2
Is the first hydration shell of lysozyme of higher density than bulk water?
journal, April 2002
- Merzel, F.; Smith, J. C.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 8
The GROMOS Biomolecular Simulation Program Package
journal, May 1999
- Scott, Walter R. P.; Hünenberger, Philippe H.; Tironi, Ilario G.
- The Journal of Physical Chemistry A, Vol. 103, Issue 19
Methyl Group Dynamics and the Onset of Anharmonicity in Myoglobin
journal, May 2008
- Krishnan, M.; Kurkal-Siebert, V.; Smith, Jeremy C.
- The Journal of Physical Chemistry B, Vol. 112, Issue 17
de Gennes Narrowing Describes the Relative Motion of Protein Domains
journal, April 2014
- Hong, Liang; Smolin, Nikolai; Smith, Jeremy C.
- Physical Review Letters, Vol. 112, Issue 15
Comparison of simple potential functions for simulating liquid water
journal, July 1983
- Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D.
- The Journal of Chemical Physics, Vol. 79, Issue 2
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
The Role of Dynamics in Enzyme Activity
journal, June 2003
- Daniel, R. M.; Dunn, R. V.; Finney, J. L.
- Annual Review of Biophysics and Biomolecular Structure, Vol. 32, Issue 1
Dynamics of Charged Macromolecules in Solution
journal, May 1974
- Schaefer, Dale W.; Berne, Bruce J.
- Physical Review Letters, Vol. 32, Issue 20
How Soft Is a Protein? A Protein Dynamics Force Constant Measured by Neutron Scattering
journal, June 2000
- Zaccai, G.
- Science, Vol. 288, Issue 5471
All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins †
journal, April 1998
- MacKerell, A. D.; Bashford, D.; Bellott, M.
- The Journal of Physical Chemistry B, Vol. 102, Issue 18
Thermal motions and function of bacteriorhodopsin in purple membranes: effects of temperature and hydration studied by neutron scattering.
journal, October 1993
- Ferrand, M.; Dianoux, A. J.; Petry, W.
- Proceedings of the National Academy of Sciences, Vol. 90, Issue 20
Dynamics and mechanism of ultrafast water–protein interactions
journal, June 2016
- Qin, Yangzhong; Wang, Lijuan; Zhong, Dongping
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 30
Low-temperature, cooperative conformational transition within [Zn-cytochrome c peroxidase, cytochrome c] complexes: variation with cytochrome
journal, August 1991
- Nocek, Judith M.; Stemp, Eric D. A.; Finnegan, Michael G.
- Journal of the American Chemical Society, Vol. 113, Issue 18
A unified model of protein dynamics
journal, February 2009
- Frauenfelder, H.; Chen, G.; Berendzen, J.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 13
Esterase catalysis of substrate vapour: enzyme activity occurs at very low hydration
journal, October 2004
- Lind, Penelope A.; Daniel, Roy M.; Monk, Colin
- Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1702, Issue 1
Role of Protein-Water Hydrogen Bond Dynamics in the Protein Dynamical Transition
journal, March 2002
- Tarek, M.; Tobias, D. J.
- Physical Review Letters, Vol. 88, Issue 13
Dynamical transition of myoglobin revealed by inelastic neutron scattering
journal, February 1989
- Doster, Wolfgang; Cusack, Stephen; Petry, Winfried
- Nature, Vol. 337, Issue 6209
Coincidence of Dynamical Transitions in a Soluble Protein and Its Hydration Water: Direct Measurements by Neutron Scattering and MD Simulations
journal, April 2008
- Wood, Kathleen; Frölich, Andreas; Paciaroni, Alessandro
- Journal of the American Chemical Society, Vol. 130, Issue 14
Direct Evidence of the Amino Acid Side Chain and Backbone Contributions to Protein Anharmonicity
journal, February 2010
- Schiró, Giorgio; Caronna, Chiara; Natali, Francesca
- Journal of the American Chemical Society, Vol. 132, Issue 4
Temperature-Dependent Dynamical Transitions of Different Classes of Amino Acid Residue in a Globular Protein
journal, November 2012
- Miao, Yinglong; Yi, Zheng; Glass, Dennis C.
- Journal of the American Chemical Society, Vol. 134, Issue 48
Slaving: Solvent fluctuations dominate protein dynamics and functions
journal, November 2002
- Fenimore, P. W.; Frauenfelder, H.; McMahon, B. H.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 25
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
Determination of functional collective motions in a protein at atomic resolution using coherent neutron scattering
journal, October 2016
- Hong, Liang; Jain, Nitin; Cheng, Xiaolin
- Science Advances, Vol. 2, Issue 10
Spatial Dependence of Protein-Water Collective Hydrogen-Bond Dynamics
journal, November 2013
- Heyden, Matthias; Tobias, Douglas J.
- Physical Review Letters, Vol. 111, Issue 21
The Low-Temperature Inflection Observed in Neutron Scattering Measurements of Proteins Is Due to Methyl Rotation: Direct Evidence Using Isotope Labeling and Molecular Dynamics Simulations
journal, April 2010
- Wood, Kathleen; Tobias, Douglas J.; Kessler, Brigitte
- Journal of the American Chemical Society, Vol. 132, Issue 14
Canonical sampling through velocity rescaling
journal, January 2007
- Bussi, Giovanni; Donadio, Davide; Parrinello, Michele
- The Journal of Chemical Physics, Vol. 126, Issue 1
Structure and short-time dynamics of polydisperse charge-stabilized suspensions
journal, July 1996
- Phalakornkul, J. K.; Gast, A. P.; Pecora, R.
- Physical Review E, Vol. 54, Issue 1
Elastic and Conformational Softness of a Globular Protein
journal, January 2013
- Hong, Liang; Glass, Dennis C.; Nickels, Jonathan D.
- Physical Review Letters, Vol. 110, Issue 2
Motional Coherence in Fluid Phospholipid Membranes
journal, December 2008
- Rheinstädter, Maikel C.; Das, Jhuma; Flenner, Elijah J.
- Physical Review Letters, Vol. 101, Issue 24
Using polarization analysis to separate the coherent and incoherent scattering from protein samples
journal, January 2010
- Gaspar, Ana M.; Busch, Sebastian; Appavou, Marie-Sousai
- Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1804, Issue 1
Average protein density is a molecular-weight-dependent function
journal, October 2004
- Fischer, Hannes; Polikarpov, Igor; Craievich, Aldo F.
- Protein Science, Vol. 13, Issue 10
Surface Hydration Amplifies Single-Well Protein Atom Diffusion Propagating into the Macromolecular Core
journal, June 2012
- Hong, Liang; Cheng, Xiaolin; Glass, Dennis C.
- Physical Review Letters, Vol. 108, Issue 23
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
The high-flux backscattering spectrometer at the NIST Center for Neutron Research
journal, May 2003
- Meyer, A.; Dimeo, R. M.; Gehring, P. M.
- Review of Scientific Instruments, Vol. 74, Issue 5
Effect of rotational diffusion on quasielastic light scattering from fractal colloid aggregates
journal, September 1988
- Lindsay, H. M.; Klein, R.; Weitz, D. A.
- Physical Review A, Vol. 38, Issue 5
Light scattering study of dynamic and time-averaged correlations in dispersions of charged particles
journal, May 1975
- Brown, J. C.; Pusey, P. N.; Goodwin, J. W.
- Journal of Physics A: Mathematical and General, Vol. 8, Issue 5
Polymorphic transitions in single crystals: A new molecular dynamics method
journal, December 1981
- Parrinello, M.; Rahman, A.
- Journal of Applied Physics, Vol. 52, Issue 12
Overview lecture. Hydration processes in biological and macromolecular systems
journal, January 1996
- Finney, John L.
- Faraday Discussions, Vol. 103
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
Protein Dynamical Transition Does Not Require Protein Structure
journal, October 2008
- He, Yunfen; Ku, Pei I.; Knab, J. R.
- Physical Review Letters, Vol. 101, Issue 17
Liquid dynamics and inelastic scattering of neutrons
journal, January 1959
- De Gennes, P. G.
- Physica, Vol. 25, Issue 7-12
Translational diffusion of hydration water correlates with functional motions in folded and intrinsically disordered proteins
journal, March 2015
- Schirò, Giorgio; Fichou, Yann; Gallat, Francois-Xavier
- Nature Communications, Vol. 6, Issue 1
The Density and Refractive Index of Adsorbing Protein Layers
journal, July 2004
- Vörös, Janos
- Biophysical Journal, Vol. 87, Issue 1
Cold neutron scattering from liquid CD4
journal, October 1966
- Venkataraman, G.; Dasannacharya, B. A.; Rao, K. R.
- Physics Letters, Vol. 23, Issue 3
Crystalline ribonuclease A loses function below the dynamical transition at 220 K
journal, June 1992
- Rasmussen, Bjarne F.; Stock, Ann M.; Ringe, Dagmar
- Nature, Vol. 357, Issue 6377
Derivation of Mean-Square Displacements for Protein Dynamics from Elastic Incoherent Neutron Scattering
journal, April 2012
- Yi, Zheng; Miao, Yinglong; Baudry, Jerome
- The Journal of Physical Chemistry B, Vol. 116, Issue 16
Methyl Group Dynamics in Glassy Polyisoprene: A Neutron Backscattering Investigation
journal, July 1994
- Frick, B.; Fetters, L. J.
- Macromolecules, Vol. 27, Issue 4
Thermal Motions in Bacteriorhodopsin at Different Hydration Levels Studied by Neutron Scattering: Correlation with Kinetics and Light-Induced Conformational Changes
journal, October 1998
- Lehnert, Ursula; Réat, Valérie; Weik, Martin
- Biophysical Journal, Vol. 75, Issue 4
Small Energy Transfer Scattering of Cold Neutrons from Liquid Argon
journal, October 1967
- Sköld, Kurt
- Physical Review Letters, Vol. 19, Issue 18
Does a Dry Protein Undergo a Glass Transition?
journal, March 2014
- Frontzek, Anna V.; Strokov, Serge V.; Embs, Jan Peter
- The Journal of Physical Chemistry B, Vol. 118, Issue 11
P450cam Visits an Open Conformation in the Absence of Substrate ,
journal, April 2010
- Lee, Young-Tae; Wilson, Richard F.; Rupniewski, Igor
- Biochemistry, Vol. 49, Issue 16
A smooth particle mesh Ewald method
journal, November 1995
- Essmann, Ulrich; Perera, Lalith; Berkowitz, Max L.
- The Journal of Chemical Physics, Vol. 103, Issue 19
Activity and Dynamics of an Enzyme, Pig Liver Esterase, in Near-Anhydrous Conditions
journal, October 2010
- Lopez, Murielle; Kurkal-Siebert, Vandana; Dunn, Rachel V.
- Biophysical Journal, Vol. 99, Issue 8
Principal Components of the Protein Dynamical Transition
journal, November 2003
- Tournier, Alexander L.; Smith, Jeremy C.
- Physical Review Letters, Vol. 91, Issue 20
Three Entropic Classes of Side Chain in a Globular Protein
journal, March 2013
- Glass, Dennis C.; Krishnan, Marimuthu; Smith, Jeremy C.
- The Journal of Physical Chemistry B, Vol. 117, Issue 11
Water in enzyme reactions: biophysical aspects of hydration-dehydration processes
journal, July 2000
- Pocker, Y.
- Cellular and Molecular Life Sciences, Vol. 57, Issue 7
Works referencing / citing this record:
The effects of pressure on the energy landscape of proteins
journal, February 2018
- Librizzi, Fabio; Carrotta, Rita; Peters, Judith
- Scientific Reports, Vol. 8, Issue 1
Analysis of elastic incoherent neutron scattering data beyond the Gaussian approximation
journal, December 2018
- Zeller, D.; Telling, M. T. F.; Zamponi, M.
- The Journal of Chemical Physics, Vol. 149, Issue 23
Role of hydration water in the onset of protein structural dynamics
journal, August 2019
- Schirò, Giorgio; Weik, Martin
- Journal of Physics: Condensed Matter, Vol. 31, Issue 46
Evidence of a low-temperature dynamical transition in concentrated microgels
journal, September 2018
- Zanatta, Marco; Tavagnacco, Letizia; Buratti, Elena
- Science Advances, Vol. 4, Issue 9
Evidence of a low-temperature dynamical transition in concentrated microgels
text, January 2018
- Zanatta, Marco; Tavagnacco, Letizia; Buratti, Elena
- arXiv