Dynamical Transition of Collective Motions in Dry Proteins

Liu, Zhuo; Huang, Juan; Tyagi, Madhusudan; O’Neill, Hugh; Zhang, Qiu; Mamontov, Eugene; Jain, Nitin; Wang, Yujie; Zhang, Jie; Smith, Jeremy C.; Hong, Liang

doi:10.1103/PhysRevLett.119.048101

Title: Dynamical Transition of Collective Motions in Dry Proteins

Journal Article · Tue Jul 25 00:00:00 EDT 2017 · Physical Review Letters

DOI:https://doi.org/10.1103/PhysRevLett.119.048101· OSTI ID:1376609

Liu, Zhuo ^[1]; Huang, Juan ^[1]; Tyagi, Madhusudan ^[2]; O’Neill, Hugh ^[3]; Zhang, Qiu ^[3]; Mamontov, Eugene ^[4]; Jain, Nitin ^[5]; Wang, Yujie ^[1]; Zhang, Jie ^[1]; Smith, Jeremy C. ^[6]; Hong, Liang ^[1]

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)

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.

View Accepted Manuscript (DOE)

View Accepted Manuscript (Publisher)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC05-00OR22725; DMR-1508249

OSTI ID:: 1376609

Alternate ID(s):: OSTI ID: 1372727

Journal Information:: Physical Review Letters, Vol. 119, Issue 4; ISSN 0031-9007

Publisher:: American Physical Society (APS)Copyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 23 works

Citation information provided by
Web of Science

References (58)

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 Keniry, Max A.; Kintanar, Agustin; Smith, Rebecca L. Biochemistry, Vol. 23, Issue 2 https://doi.org/10.1021/bi00297a018	journal	January 1984
Is the first hydration shell of lysozyme of higher density than bulk water? Merzel, F.; Smith, J. C. Proceedings of the National Academy of Sciences, Vol. 99, Issue 8 https://doi.org/10.1073/pnas.082335099	journal	April 2002
The GROMOS Biomolecular Simulation Program Package Scott, Walter R. P.; Hünenberger, Philippe H.; Tironi, Ilario G. The Journal of Physical Chemistry A, Vol. 103, Issue 19 https://doi.org/10.1021/jp984217f	journal	May 1999
Methyl Group Dynamics and the Onset of Anharmonicity in Myoglobin Krishnan, M.; Kurkal-Siebert, V.; Smith, Jeremy C. The Journal of Physical Chemistry B, Vol. 112, Issue 17 https://doi.org/10.1021/jp076641z	journal	May 2008
de Gennes Narrowing Describes the Relative Motion of Protein Domains Hong, Liang; Smolin, Nikolai; Smith, Jeremy C. Physical Review Letters, Vol. 112, Issue 15 https://doi.org/10.1103/PhysRevLett.112.158102	journal	April 2014
Comparison of simple potential functions for simulating liquid water Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D. The Journal of Chemical Physics, Vol. 79, Issue 2 https://doi.org/10.1063/1.445869	journal	July 1983
Solvent effects on protein fast dynamics: implications for biopreservation Sakai, Victoria García; Khodadadi, Sheila; Cicerone, Marcus T. Soft Matter, Vol. 9, Issue 22 https://doi.org/10.1039/c3sm50492a	journal	January 2013
The Role of Dynamics in Enzyme Activity Daniel, R. M.; Dunn, R. V.; Finney, J. L. Annual Review of Biophysics and Biomolecular Structure, Vol. 32, Issue 1 https://doi.org/10.1146/annurev.biophys.32.110601.142445	journal	June 2003
Dynamics of Charged Macromolecules in Solution Schaefer, Dale W.; Berne, Bruce J. Physical Review Letters, Vol. 32, Issue 20 https://doi.org/10.1103/PhysRevLett.32.1110	journal	May 1974
How Soft Is a Protein? A Protein Dynamics Force Constant Measured by Neutron Scattering Zaccai, G. Science, Vol. 288, Issue 5471 https://doi.org/10.1126/science.288.5471.1604	journal	June 2000
All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins ^† MacKerell, A. D.; Bashford, D.; Bellott, M. The Journal of Physical Chemistry B, Vol. 102, Issue 18 https://doi.org/10.1021/jp973084f	journal	April 1998
Thermal motions and function of bacteriorhodopsin in purple membranes: effects of temperature and hydration studied by neutron scattering. Ferrand, M.; Dianoux, A. J.; Petry, W. Proceedings of the National Academy of Sciences, Vol. 90, Issue 20 https://doi.org/10.1073/pnas.90.20.9668	journal	October 1993
Dynamics and mechanism of ultrafast water–protein interactions Qin, Yangzhong; Wang, Lijuan; Zhong, Dongping Proceedings of the National Academy of Sciences, Vol. 113, Issue 30 https://doi.org/10.1073/pnas.1602916113	journal	June 2016
Low-temperature, cooperative conformational transition within [Zn-cytochrome c peroxidase, cytochrome c] complexes: variation with cytochrome Nocek, Judith M.; Stemp, Eric D. A.; Finnegan, Michael G. Journal of the American Chemical Society, Vol. 113, Issue 18 https://doi.org/10.1021/ja00018a017	journal	August 1991
A unified model of protein dynamics Frauenfelder, H.; Chen, G.; Berendzen, J. Proceedings of the National Academy of Sciences, Vol. 106, Issue 13 https://doi.org/10.1073/pnas.0900336106	journal	February 2009
Esterase catalysis of substrate vapour: enzyme activity occurs at very low hydration Lind, Penelope A.; Daniel, Roy M.; Monk, Colin Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1702, Issue 1 https://doi.org/10.1016/j.bbapap.2004.08.005	journal	October 2004
Role of Protein-Water Hydrogen Bond Dynamics in the Protein Dynamical Transition Tarek, M.; Tobias, D. J. Physical Review Letters, Vol. 88, Issue 13 https://doi.org/10.1103/PhysRevLett.88.138101	journal	March 2002
Dynamical transition of myoglobin revealed by inelastic neutron scattering Doster, Wolfgang; Cusack, Stephen; Petry, Winfried Nature, Vol. 337, Issue 6209 https://doi.org/10.1038/337754a0	journal	February 1989
Coincidence of Dynamical Transitions in a Soluble Protein and Its Hydration Water: Direct Measurements by Neutron Scattering and MD Simulations Wood, Kathleen; Frölich, Andreas; Paciaroni, Alessandro Journal of the American Chemical Society, Vol. 130, Issue 14 https://doi.org/10.1021/ja710526r	journal	April 2008
Direct Evidence of the Amino Acid Side Chain and Backbone Contributions to Protein Anharmonicity Schiró, Giorgio; Caronna, Chiara; Natali, Francesca Journal of the American Chemical Society, Vol. 132, Issue 4 https://doi.org/10.1021/ja908611p	journal	February 2010
Temperature-Dependent Dynamical Transitions of Different Classes of Amino Acid Residue in a Globular Protein Miao, Yinglong; Yi, Zheng; Glass, Dennis C. Journal of the American Chemical Society, Vol. 134, Issue 48 https://doi.org/10.1021/ja3097898	journal	November 2012
Seeking the solution Ball, Philip Nature, Vol. 436, Issue 7054 https://doi.org/10.1038/4361084a	journal	August 2005
Slaving: Solvent fluctuations dominate protein dynamics and functions Fenimore, P. W.; Frauenfelder, H.; McMahon, B. H. Proceedings of the National Academy of Sciences, Vol. 99, Issue 25 https://doi.org/10.1073/pnas.212637899	journal	November 2002
A time-of-flight backscattering spectrometer at the Spallation Neutron Source, BASIS Mamontov, E.; Herwig, K. W. Review of Scientific Instruments, Vol. 82, Issue 8 https://doi.org/10.1063/1.3626214	journal	August 2011
Determination of functional collective motions in a protein at atomic resolution using coherent neutron scattering Hong, Liang; Jain, Nitin; Cheng, Xiaolin Science Advances, Vol. 2, Issue 10 https://doi.org/10.1126/sciadv.1600886	journal	October 2016
Spatial Dependence of Protein-Water Collective Hydrogen-Bond Dynamics Heyden, Matthias; Tobias, Douglas J. Physical Review Letters, Vol. 111, Issue 21 https://doi.org/10.1103/PhysRevLett.111.218101	journal	November 2013
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 Wood, Kathleen; Tobias, Douglas J.; Kessler, Brigitte Journal of the American Chemical Society, Vol. 132, Issue 14 https://doi.org/10.1021/ja910502g	journal	April 2010
Canonical sampling through velocity rescaling Bussi, Giovanni; Donadio, Davide; Parrinello, Michele The Journal of Chemical Physics, Vol. 126, Issue 1 https://doi.org/10.1063/1.2408420	journal	January 2007
Structure and short-time dynamics of polydisperse charge-stabilized suspensions Phalakornkul, J. K.; Gast, A. P.; Pecora, R. Physical Review E, Vol. 54, Issue 1 https://doi.org/10.1103/PhysRevE.54.661	journal	July 1996
Elastic and Conformational Softness of a Globular Protein Hong, Liang; Glass, Dennis C.; Nickels, Jonathan D. Physical Review Letters, Vol. 110, Issue 2 https://doi.org/10.1103/PhysRevLett.110.028104	journal	January 2013
Motional Coherence in Fluid Phospholipid Membranes Rheinstädter, Maikel C.; Das, Jhuma; Flenner, Elijah J. Physical Review Letters, Vol. 101, Issue 24 https://doi.org/10.1103/PhysRevLett.101.248106	journal	December 2008
Using polarization analysis to separate the coherent and incoherent scattering from protein samples Gaspar, Ana M.; Busch, Sebastian; Appavou, Marie-Sousai Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1804, Issue 1 https://doi.org/10.1016/j.bbapap.2009.06.024	journal	January 2010
Average protein density is a molecular-weight-dependent function Fischer, Hannes; Polikarpov, Igor; Craievich, Aldo F. Protein Science, Vol. 13, Issue 10 https://doi.org/10.1110/ps.04688204	journal	October 2004
Surface Hydration Amplifies Single-Well Protein Atom Diffusion Propagating into the Macromolecular Core Hong, Liang; Cheng, Xiaolin; Glass, Dennis C. Physical Review Letters, Vol. 108, Issue 23 https://doi.org/10.1103/PhysRevLett.108.238102	journal	June 2012
Observation of fragile-to-strong dynamic crossover in protein hydration water Chen, S. -H.; Liu, L.; Fratini, E. Proceedings of the National Academy of Sciences, Vol. 103, Issue 24 https://doi.org/10.1073/pnas.0602474103	journal	June 2006
The high-flux backscattering spectrometer at the NIST Center for Neutron Research Meyer, A.; Dimeo, R. M.; Gehring, P. M. Review of Scientific Instruments, Vol. 74, Issue 5 https://doi.org/10.1063/1.1568557	journal	May 2003
Effect of rotational diffusion on quasielastic light scattering from fractal colloid aggregates Lindsay, H. M.; Klein, R.; Weitz, D. A. Physical Review A, Vol. 38, Issue 5 https://doi.org/10.1103/PhysRevA.38.2614	journal	September 1988
Light scattering study of dynamic and time-averaged correlations in dispersions of charged particles Brown, J. C.; Pusey, P. N.; Goodwin, J. W. Journal of Physics A: Mathematical and General, Vol. 8, Issue 5 https://doi.org/10.1088/0305-4470/8/5/004	journal	May 1975
Polymorphic transitions in single crystals: A new molecular dynamics method Parrinello, M.; Rahman, A. Journal of Applied Physics, Vol. 52, Issue 12 https://doi.org/10.1063/1.328693	journal	December 1981
Overview lecture. Hydration processes in biological and macromolecular systems Finney, John L. Faraday Discussions, Vol. 103 https://doi.org/10.1039/fd9960300001	journal	January 1996
Influence of Hydration on the Dynamics of Lysozyme Roh, J. H.; Curtis, J. E.; Azzam, S. Biophysical Journal, Vol. 91, Issue 7 https://doi.org/10.1529/biophysj.106.082214	journal	October 2006
Protein Dynamical Transition Does Not Require Protein Structure He, Yunfen; Ku, Pei I.; Knab, J. R. Physical Review Letters, Vol. 101, Issue 17 https://doi.org/10.1103/PhysRevLett.101.178103	journal	October 2008
Liquid dynamics and inelastic scattering of neutrons De Gennes, P. G. Physica, Vol. 25, Issue 7-12 https://doi.org/10.1016/0031-8914(59)90006-0	journal	January 1959
Translational diffusion of hydration water correlates with functional motions in folded and intrinsically disordered proteins Schirò, Giorgio; Fichou, Yann; Gallat, Francois-Xavier Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7490	journal	March 2015
The Density and Refractive Index of Adsorbing Protein Layers Vörös, Janos Biophysical Journal, Vol. 87, Issue 1 https://doi.org/10.1529/biophysj.103.030072	journal	July 2004
Cold neutron scattering from liquid CD4 Venkataraman, G.; Dasannacharya, B. A.; Rao, K. R. Physics Letters, Vol. 23, Issue 3 https://doi.org/10.1016/0031-9163(66)90877-8	journal	October 1966
Crystalline ribonuclease A loses function below the dynamical transition at 220 K Rasmussen, Bjarne F.; Stock, Ann M.; Ringe, Dagmar Nature, Vol. 357, Issue 6377 https://doi.org/10.1038/357423a0	journal	June 1992
Derivation of Mean-Square Displacements for Protein Dynamics from Elastic Incoherent Neutron Scattering Yi, Zheng; Miao, Yinglong; Baudry, Jerome The Journal of Physical Chemistry B, Vol. 116, Issue 16 https://doi.org/10.1021/jp2102868	journal	April 2012
Methyl Group Dynamics in Glassy Polyisoprene: A Neutron Backscattering Investigation Frick, B.; Fetters, L. J. Macromolecules, Vol. 27, Issue 4 https://doi.org/10.1021/ma00082a014	journal	July 1994
Thermal Motions in Bacteriorhodopsin at Different Hydration Levels Studied by Neutron Scattering: Correlation with Kinetics and Light-Induced Conformational Changes Lehnert, Ursula; Réat, Valérie; Weik, Martin Biophysical Journal, Vol. 75, Issue 4 https://doi.org/10.1016/S0006-3495(98)77635-0	journal	October 1998
Small Energy Transfer Scattering of Cold Neutrons from Liquid Argon Sköld, Kurt Physical Review Letters, Vol. 19, Issue 18 https://doi.org/10.1103/PhysRevLett.19.1023	journal	October 1967
Does a Dry Protein Undergo a Glass Transition? Frontzek, Anna V.; Strokov, Serge V.; Embs, Jan Peter The Journal of Physical Chemistry B, Vol. 118, Issue 11 https://doi.org/10.1021/jp4104905	journal	March 2014
P450cam Visits an Open Conformation in the Absence of Substrate ^, Lee, Young-Tae; Wilson, Richard F.; Rupniewski, Igor Biochemistry, Vol. 49, Issue 16 https://doi.org/10.1021/bi100183g	journal	April 2010
A smooth particle mesh Ewald method Essmann, Ulrich; Perera, Lalith; Berkowitz, Max L. The Journal of Chemical Physics, Vol. 103, Issue 19 https://doi.org/10.1063/1.470117	journal	November 1995
Activity and Dynamics of an Enzyme, Pig Liver Esterase, in Near-Anhydrous Conditions Lopez, Murielle; Kurkal-Siebert, Vandana; Dunn, Rachel V. Biophysical Journal, Vol. 99, Issue 8 https://doi.org/10.1016/j.bpj.2010.07.066	journal	October 2010
Principal Components of the Protein Dynamical Transition Tournier, Alexander L.; Smith, Jeremy C. Physical Review Letters, Vol. 91, Issue 20 https://doi.org/10.1103/PhysRevLett.91.208106	journal	November 2003
Three Entropic Classes of Side Chain in a Globular Protein Glass, Dennis C.; Krishnan, Marimuthu; Smith, Jeremy C. The Journal of Physical Chemistry B, Vol. 117, Issue 11 https://doi.org/10.1021/jp400564q	journal	March 2013
Water in enzyme reactions: biophysical aspects of hydration-dehydration processes Pocker, Y. Cellular and Molecular Life Sciences, Vol. 57, Issue 7 https://doi.org/10.1007/PL00000741	journal	July 2000

Cited By (5)

The effects of pressure on the energy landscape of proteins Librizzi, Fabio; Carrotta, Rita; Peters, Judith Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-20417-x	journal	February 2018
Analysis of elastic incoherent neutron scattering data beyond the Gaussian approximation Zeller, D.; Telling, M. T. F.; Zamponi, M. The Journal of Chemical Physics, Vol. 149, Issue 23 https://doi.org/10.1063/1.5049938	journal	December 2018
Role of hydration water in the onset of protein structural dynamics Schirò, Giorgio; Weik, Martin Journal of Physics: Condensed Matter, Vol. 31, Issue 46 https://doi.org/10.1088/1361-648x/ab388a	journal	August 2019
Evidence of a low-temperature dynamical transition in concentrated microgels Zanatta, Marco; Tavagnacco, Letizia; Buratti, Elena Science Advances, Vol. 4, Issue 9 https://doi.org/10.1126/sciadv.aat5895	journal	September 2018
Evidence of a low-temperature dynamical transition in concentrated microgels Zanatta, Marco; Tavagnacco, Letizia; Buratti, Elena arXiv https://doi.org/10.48550/arxiv.1802.04841	text	January 2018

Similar Records

Determination of functional collective motions in a protein at atomic resolution using coherent neutron scattering

Journal Article · Fri Oct 14 00:00:00 EDT 2016 · Science Advances · OSTI ID:1376609

Hong, Liang; Jain, Nitin; Cheng, Xiaolin; +3 more

Protein-style dynamical transition in a non-biological polymer and a non-aqueous solvent

Journal Article · Tue Mar 15 00:00:00 EDT 2016 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry · OSTI ID:1376609

Mamontov, E.; Sharma, V. K.; Borreguero, J. M.; +1 more

Structure and collective dynamics of hydrated anti-freeze protein type III from 180 K to 298 K by X-ray diffraction and inelastic X-ray scattering

Journal Article · Thu Apr 07 00:00:00 EDT 2016 · Journal of Chemical Physics · OSTI ID:1376609

Yoshida, Koji; Baron, Alfred Q. R.; Uchiyama, Hiroshi; +2 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Dynamical Transition of Collective Motions in Dry Proteins

Citation Formats

References (58)

Cited By (5)

Similar Records

Related Subjects