skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Dynamical disparity between hydration shell water and RNA in a hydrated RNA system

Abstract

We have performed large-scale molecular dynamics simulations on hammerhead RNA in water and observed disparity in the dynamical properties between water and RNA. The simulations are carried out above the dynamical transition temperature of RNA and is varied from below freezing to ambient temperature. Using this model, we observed different types of relaxation dynamics for water and RNA. While RNA shows a single stretched exponential decay, the water molecules show a double-exponential decay. Both water and RNA dynamics show temperature and spatial dependence on relaxation times. The RNA relaxations are many orders of magnitude slower compared to water for all temperature and spatial length scales. RNA relaxations show predominantly heterogeneous dynamics. Water dynamics in the hydration shell show a combination of interfacial water and bulk-like water properties and the water dynamics are decoupled from the RNA dynamics. Furthermore, these results explain the dynamics of water in the hydration shell and that of RNA.

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1496008
Alternate Identifier(s):
OSTI ID: 1486904
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Physical Review E
Additional Journal Information:
Journal Volume: 98; Journal Issue: 6; Journal ID: ISSN 2470-0045
Publisher:
American Physical Society (APS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Bhowmik, Debsindhu, Ganesh, Panchapakesan, Sumpter, Bobby G., and Goswami, Monojoy. Dynamical disparity between hydration shell water and RNA in a hydrated RNA system. United States: N. p., 2018. Web. doi:10.1103/PhysRevE.98.062407.
Bhowmik, Debsindhu, Ganesh, Panchapakesan, Sumpter, Bobby G., & Goswami, Monojoy. Dynamical disparity between hydration shell water and RNA in a hydrated RNA system. United States. doi:10.1103/PhysRevE.98.062407.
Bhowmik, Debsindhu, Ganesh, Panchapakesan, Sumpter, Bobby G., and Goswami, Monojoy. Fri . "Dynamical disparity between hydration shell water and RNA in a hydrated RNA system". United States. doi:10.1103/PhysRevE.98.062407. https://www.osti.gov/servlets/purl/1496008.
@article{osti_1496008,
title = {Dynamical disparity between hydration shell water and RNA in a hydrated RNA system},
author = {Bhowmik, Debsindhu and Ganesh, Panchapakesan and Sumpter, Bobby G. and Goswami, Monojoy},
abstractNote = {We have performed large-scale molecular dynamics simulations on hammerhead RNA in water and observed disparity in the dynamical properties between water and RNA. The simulations are carried out above the dynamical transition temperature of RNA and is varied from below freezing to ambient temperature. Using this model, we observed different types of relaxation dynamics for water and RNA. While RNA shows a single stretched exponential decay, the water molecules show a double-exponential decay. Both water and RNA dynamics show temperature and spatial dependence on relaxation times. The RNA relaxations are many orders of magnitude slower compared to water for all temperature and spatial length scales. RNA relaxations show predominantly heterogeneous dynamics. Water dynamics in the hydration shell show a combination of interfacial water and bulk-like water properties and the water dynamics are decoupled from the RNA dynamics. Furthermore, these results explain the dynamics of water in the hydration shell and that of RNA.},
doi = {10.1103/PhysRevE.98.062407},
journal = {Physical Review E},
number = 6,
volume = 98,
place = {United States},
year = {2018},
month = {12}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Save / Share:

Works referenced in this record:

Dynamics of Biological Macromolecules: Not a Simple Slaving by Hydration Water
journal, April 2010


Dynamic heterogeneity in supercooled ortho-terphenyl studied by multidimensional deuteron NMR
journal, October 1996


Correlation spectroscopy with coherent X-rays
journal, January 2004


Correlating Structural Dynamics and Function in Single Ribozyme Molecules
journal, May 2002


Kinetic Mechanism of the Hairpin Ribozyme: IDENTIFICATION AND CHARACTERIZATION OF TWO NONEXCHANGEABLE CONFORMATIONS
journal, May 1997

  • Esteban, José A.; Banerjee, Aloke Raj; Burke, John M.
  • Journal of Biological Chemistry, Vol. 272, Issue 21
  • DOI: 10.1074/jbc.272.21.13629

Neutron scattering perspectives for protein dynamics
journal, January 2011


Scalable molecular dynamics with NAMD
journal, January 2005

  • Phillips, James C.; Braun, Rosemary; Wang, Wei
  • Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802
  • DOI: 10.1002/jcc.20289

Structural basis for heterogeneous kinetics: Reengineering the hairpin ribozyme
journal, May 1998

  • Esteban, J. A.; Walter, N. G.; Kotzorek, G.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 11
  • DOI: 10.1073/pnas.95.11.6091

Water Rotational Relaxation and Diffusion in Hydrated Lysozyme
journal, June 2002

  • Marchi, Massimo; Sterpone, Fabio; Ceccarelli, Matteo
  • Journal of the American Chemical Society, Vol. 124, Issue 23
  • DOI: 10.1021/ja025905m

Observation of a dynamic crossover in RNA hydration water which triggers a dynamic transition in the biopolymer
journal, January 2008


Water as an Active Constituent in Cell Biology
journal, January 2008


Molecular dynamics simulation evidence of anomalous diffusion of protein hydration water
journal, April 1996


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
  • DOI: 10.1063/1.445869

Delivery materials for siRNA therapeutics
journal, October 2013

  • Kanasty, Rosemary; Dorkin, Joseph Robert; Vegas, Arturo
  • Nature Materials, Vol. 12, Issue 11
  • DOI: 10.1038/nmat3765

Water Dynamics in the Hydration Shells of Biomolecules
journal, March 2017


Role of Water and Ions on the Dynamical Transition of RNA
journal, September 2013

  • Zhang, Hailiang; Khodadadi, Sheila; Fiedler, Steven L.
  • The Journal of Physical Chemistry Letters, Vol. 4, Issue 19
  • DOI: 10.1021/jz401406c

Dynamics of Protein and its Hydration Water: Neutron Scattering Studies on Fully Deuterated GFP
journal, October 2012


Theory of Slow Neutron Scattering by Liquids. I
journal, May 1962


Comment on “Dynamics of Glass-Forming Polymers: `Homogeneous' versus `Heterogeneous' Scenario”
journal, February 1999


Arbe et al. Reply:
journal, February 1999


Influence of Water Clustering on the Dynamics of Hydration Water at the Surface of a Lysozyme
journal, November 2007


The fluctuating ribosome: thermal molecular dynamics characterized by neutron scattering
journal, November 2016

  • Zaccai, Giuseppe; Natali, Francesca; Peters, Judith
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep37138

CHARMM: The biomolecular simulation program
journal, July 2009

  • Brooks, B. R.; Brooks, C. L.; Mackerell, A. D.
  • Journal of Computational Chemistry, Vol. 30, Issue 10
  • DOI: 10.1002/jcc.21287

More than one dynamic crossover in protein hydration water
journal, November 2011

  • Mazza, M. G.; Stokely, K.; Pagnotta, S. E.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 50
  • DOI: 10.1073/pnas.1104299108

Dynamical transition of myoglobin revealed by inelastic neutron scattering
journal, February 1989

  • Doster, Wolfgang; Cusack, Stephen; Petry, Winfried
  • Nature, Vol. 337, Issue 6209
  • DOI: 10.1038/337754a0

Structure and Dynamics of the TIP3P, SPC, and SPC/E Water Models at 298 K
journal, November 2001

  • Mark, Pekka; Nilsson, Lennart
  • The Journal of Physical Chemistry A, Vol. 105, Issue 43
  • DOI: 10.1021/jp003020w

Dynamic Transition in tRNA is Solvent Induced
journal, January 2006

  • Caliskan, Gokhan; Briber, Robert M.; Thirumalai, D.
  • Journal of the American Chemical Society, Vol. 128, Issue 1
  • DOI: 10.1021/ja056444i

Diffusive dynamics during the high-to-low density transition in amorphous ice
journal, June 2017

  • Perakis, Fivos; Amann-Winkel, Katrin; Lehmkühler, Felix
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 31
  • DOI: 10.1073/pnas.1705303114

Dynamic heterogeneity controls diffusion and viscosity near biological interfaces
journal, January 2014

  • Pronk, Sander; Lindahl, Erik; Kasson, Peter M.
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms4034

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
  • DOI: 10.1073/pnas.212637899

Water Determines the Structure and Dynamics of Proteins
journal, April 2016

  • Bellissent-Funel, Marie-Claire; Hassanali, Ali; Havenith, Martina
  • Chemical Reviews, Vol. 116, Issue 13
  • DOI: 10.1021/acs.chemrev.5b00664

Mapping hydration dynamics around a protein surface
journal, November 2007

  • Zhang, L.; Wang, L.; Kao, Y. -T.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 47
  • DOI: 10.1073/pnas.0707647104

Dynamics of Water near a Protein Surface
journal, November 2003

  • Bhattacharyya, Sarika M.; Wang, Zhen-Gang; Zewail, Ahmed H.
  • The Journal of Physical Chemistry B, Vol. 107, Issue 47
  • DOI: 10.1021/jp030943t

n Moldyn: A program package for a neutron scattering oriented analysis of molecular dynamics simulations
journal, March 2003

  • Róg, T.; Murzyn, K.; Hinsen, K.
  • Journal of Computational Chemistry, Vol. 24, Issue 5
  • DOI: 10.1002/jcc.10243

Long-time mean-square displacements in proteins
journal, November 2013


Computation of the mean residence time of water in the hydration shells of biomolecules: TIME-RELAXATION BEHAVIOR
journal, November 1993

  • García, Angel E.; Stiller, Lewis
  • Journal of Computational Chemistry, Vol. 14, Issue 11
  • DOI: 10.1002/jcc.540141116

Water Mediation in Protein Folding and Molecular Recognition
journal, June 2006


Protein and solvent dynamics: How strongly are they coupled?
journal, July 2004

  • Caliskan, G.; Mechtani, D.; Roh, J. H.
  • The Journal of Chemical Physics, Vol. 121, Issue 4
  • DOI: 10.1063/1.1764491

Enhanced Dynamics of Hydrated tRNA on Nanodiamond Surfaces: A Combined Neutron Scattering and MD Simulation Study
journal, September 2016

  • Dhindsa, Gurpreet K.; Bhowmik, Debsindhu; Goswami, Monojoy
  • The Journal of Physical Chemistry B, Vol. 120, Issue 38
  • DOI: 10.1021/acs.jpcb.6b07511

Dynamical Coupling of Intrinsically Disordered Proteins and Their Hydration Water: Comparison with Folded Soluble and Membrane Proteins
journal, July 2012


Reorientation and Allied Dynamics in Water and Aqueous Solutions
journal, May 2011


Residence Times of Water Molecules in the Hydration Sites of Myoglobin
journal, December 2000


Hydration and Dynamics of a Tetramethylammonium Ion in Water:  A Computer Simulation Study
journal, September 1998

  • García-Tarrés, L.; Guàrdia, E.
  • The Journal of Physical Chemistry B, Vol. 102, Issue 38
  • DOI: 10.1021/jp981427j

Amplitudes and Frequencies of Protein Dynamics:  Analysis of Discrepancies between Neutron Scattering and Molecular Dynamics Simulations
journal, October 2000

  • Tarek, Mounir; Martyna, Glenn J.; Tobias, Douglas J.
  • Journal of the American Chemical Society, Vol. 122, Issue 42
  • DOI: 10.1021/ja0016506

Hydration, slaving and protein function
journal, July 2002


Internal Water and Microsecond Dynamics in Myoglobin
journal, November 2013

  • Kaieda, Shuji; Halle, Bertil
  • The Journal of Physical Chemistry B, Vol. 117, Issue 47
  • DOI: 10.1021/jp409234g

Are Waters around RNA More than Just a Solvent? – An Insight from Molecular Dynamics Simulations
journal, November 2013

  • Kührová, Petra; Otyepka, Michal; Šponer, Jiří
  • Journal of Chemical Theory and Computation, Vol. 10, Issue 1
  • DOI: 10.1021/ct400663s

Nonresonant Spectral Hole Burning in the Slow Dielectric Response of Supercooled Liquids
journal, November 1996


Rate Memory of Structural Relaxation in Glasses and Its Detection by Multidimensional NMR
journal, October 1995


How Protein Surfaces Induce Anomalous Dynamics of Hydration Water
journal, July 2007

  • Pizzitutti, Francesco; Marchi, Massimo; Sterpone, Fabio
  • The Journal of Physical Chemistry B, Vol. 111, Issue 26
  • DOI: 10.1021/jp0717185

Influence of Hydration on the Dynamics of Lysozyme
journal, October 2006


Molecular Dynamics of Water at the Protein−Solvent Interface
journal, July 2002

  • Bizzarri, Anna Rita; Cannistraro, Salvatore
  • The Journal of Physical Chemistry B, Vol. 106, Issue 26
  • DOI: 10.1021/jp020100m

Water residence times around copper plastocyanin: a molecular dynamics simulation approach
journal, January 1997


Dynamical Transition and Heterogeneous Hydration Dynamics in RNA
journal, May 2014

  • Yoon, Jeseong; Lin, Jong-Chin; Hyeon, Changbong
  • The Journal of Physical Chemistry B, Vol. 118, Issue 28
  • DOI: 10.1021/jp500643u

Glass Transition in Biomolecules and the Liquid-Liquid Critical Point of Water
journal, October 2006


Molecular Dynamics and Quantum Mechanics of RNA: Conformational and Chemical Change We Can Believe In
journal, January 2010

  • Ditzler, Mark A.; Otyepka, Michal; Šponer, Jiřì
  • Accounts of Chemical Research, Vol. 43, Issue 1
  • DOI: 10.1021/ar900093g

Dynamics of tRNA at Different Levels of Hydration
journal, April 2009


When is a single molecule heterogeneous? A multidimensional answer and its application to dynamics near the glass transition
journal, July 2015

  • Verma, Sachin Dev; Vanden Bout, David A.; Berg, Mark A.
  • The Journal of Chemical Physics, Vol. 143, Issue 2
  • DOI: 10.1063/1.4926463

Onsets of Anharmonicity in Protein Dynamics
journal, July 2005


Dynamics of Glass-Forming Polymers: “Homogeneous” versus “Heterogeneous” Scenario
journal, July 1998


Time-dependent diffusion of water in a biological model system.
journal, February 1994

  • Latour, L. L.; Svoboda, K.; Mitra, P. P.
  • Proceedings of the National Academy of Sciences, Vol. 91, Issue 4
  • DOI: 10.1073/pnas.91.4.1229

VMD: Visual molecular dynamics
journal, February 1996


The emerging field of RNA nanotechnology
journal, November 2010


RNA solvation: A molecular dynamics simulation perspective
journal, January 2000