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Mean-squared atomic displacements in hydrated lysozyme, native and denatured

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Abstract

We use elastic neutron scattering to demonstrate that a sharp increase in the mean-squared atomic displacements, commonly observed in hydrated proteins above 200 K and often referred to as the dynamical transition, is present in the hydrated state of both native and denatured lysozyme. A direct comparison of the native and denatured protein thus confirms that the presence of the transition in the mean-squared atomic displacements is not specific to biologically functional molecules.

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References

  1. Parak, F., Formanek, H.: Study on vibration and crystal lattice fault of temperature factor in myoglobin by comparative Mossbauer absorption measurements with X-ray structure data. Acta Crystallogr. A 27, 573–578 (1971)

    Article  ADS  Google Scholar 

  2. Keller, H., Debrunner, P.G.: Evidence for conformational and diffusional mean-square displacements in frozen aqueous-solution of oxymyoglobin. Phys. Rev. Lett. 45, 68–71 (1980)

    Article  ADS  Google Scholar 

  3. Parak, F., Knapp, E.W., Kucheida, D.: Protein dynamics–Mossbauer–spectroscopy on deoxymyoglobin crystals. J. Mol. Biol. 161, 177–194 (1982)

    Article  Google Scholar 

  4. Doster, W., Cusack, S., Petry, W.: Dynamical transition of myoglobin revealed by inelastic neutron-scattering. Nature 337, 754–756 (1989)

    Article  ADS  Google Scholar 

  5. Paciaroni, A., Cinelli, S., Cornicchi, E., De Francesco, A., Onori, G.: Fast fluctuations in protein powders: the role of hydration. Chem. Phys. Lett. 410, 400–403 (2005)

    Article  ADS  Google Scholar 

  6. Cornicchi, E., Onori, G., Paciaroni, A.: Picosecond-time-scale fluctuations of proteins in glassy matrices: the role of viscosity. Phys. Rev. Lett. 95, 158104 (2005)

    Article  ADS  Google Scholar 

  7. Roh, J.H., Novikov, V.N., Gregory, R.B., Curtis, J.E., Chowdhuri, Z., Sokolov, A.P.: Onsets of anharmonicity in protein dynamics. Phys. Rev. Lett. 95, 038101 (2005)

    Article  ADS  Google Scholar 

  8. Roh, J.H., Curtis, J.E., Azzam, S., Novikov, V.N., Peral, I., Chowdhuri, Z., Gregory, R.B., Sokolov, A.P.: Influence of hydration on the dynamics of lysozyme. Biophys. J. 91, 2573–2588 (2006)

    Article  ADS  Google Scholar 

  9. Cornicchi, E., Marconi, M., Onori, G., Paciaroni, A.: Controlling the protein dynamical transition with sugar-based bioprotectant matrices: a neutron scattering study. Biophys. J. 91, 289–297 (2006)

    Article  ADS  Google Scholar 

  10. Caliskan, G., Briber, R.M., Thirumalai, D., Garcia-Sakai, V., Woodson, S.A., Sokolov, A.P.: Dynamic transition in tRNA is solvent induced. J. Am. Chem. Soc. 128, 32–33 (2006)

    Article  Google Scholar 

  11. Cornicchi, E., Capponi, S., Marconi, M., Onori, G., Paciaroni, A.: Temperature dependence of fast fluctuations in single- and double-stranded DNA molecules: a neutron scattering investigation. Philos. Mag. 87, 509–515 (2007)

    Article  ADS  Google Scholar 

  12. Roh, J.H., Briber, R.M., Damjanovic, A., Thirumalai, D., Woodson, S.A., Sokolov, A.P.: Dynamics of tRNA at different levels of hydration. Biophys. J. 96, 2755–2762 (2009)

    Article  ADS  Google Scholar 

  13. Daniel, R.M., Smith, J.C., Ferrand, M., Hery, S., Dunn, R., Finney, J.L.: Enzyme activity below the dynamical transition at 220 K. Biophys. J. 75, 2504–2507 (1998)

    Article  Google Scholar 

  14. Daniel, R.M., Finney, J.L., Reat, V., Dunn, R., Ferrand, M., Smith, J.C.: Enzyme dynamics and activity: time-scale dependence of dynamical transitions in glutamate dehydrogenase solution. Biophys. J. 77, 2184–2190 (1999)

    Article  Google Scholar 

  15. Sokolov, A.P., Grimm, H., Kisliuk, A., Dianoux, A.J.: Slow relaxation process in DNA. J. Biol. Phys. 27, 313–327 (2001)

    Article  Google Scholar 

  16. Fenimore, P.W., Frauenfelder, H., McMahon, B.H., Parak, F.G.: Slaving: Solvent fluctuations dominate protein dynamics and functions. Proc. Natl. Acad. Sci. USA 99, 16047–16051 (2002)

    Article  ADS  Google Scholar 

  17. Daniel, R.M., Finney, J.M., Smith, J.C.: The dynamic transition in proteins may have a simple explanation. Faraday Discuss. 122, 163–169 (2002)

    Article  Google Scholar 

  18. Becker, T., Hayward, J.A., Finney, J.L., Daniel, R.M., Smith, J.C.: Neutron frequency windows and the protein dynamical transition. Biophys. J. 87, 1436–1444 (2004)

    Article  ADS  Google Scholar 

  19. Fenimore, P.W., Frauenfelder, H., McMahon, B.H., Young, R.D.: Bulk-solvent and hydration-shell fluctuations, similar to alpha- and beta-fluctuations in glasses, control protein motions and functions. Proc. Natl. Acad. Sci. USA 101, 14408–14413 (2004)

    Article  ADS  Google Scholar 

  20. Chen, S.H., Liu, L., Fratini, E., Baglioni, P., Faraone, A., Mamontov, E.: Observation of fragile-to-strong dynamic crossover in protein hydration water. Proc. Natl. Acad. Sci. USA 103, 9012–9016 (2006)

    Article  ADS  Google Scholar 

  21. Kumar, P., Yan, Z., Xu, L., Mazza, M.G., Buldyrev, S.V., Chen, S.H., Sastry, S., Stanley, H.E.: Glass transition in biomolecules and the liquid-liquid critical point of water. Phys. Rev. Lett. 97, 177802 (2006)

    Article  ADS  Google Scholar 

  22. Chen, S.H., Liu, L., Chu, X., Zhang, Y., Fratini, E., Baglioni, P., Faraone, A., Mamontov, E.: Experimental evidence of fragile-to-strong dynamic crossover in DNA hydration water. J. Chem. Phys. 125, 171103 (2006)

    Article  ADS  Google Scholar 

  23. Chu, X.Q., Fratini, E., Baglioni, P., Faraone, A., Chen, S.H.: Observation of a dynamic crossover in RNA hydration water which triggers a dynamic transition in the biopolymer. Phys. Rev. E 77, 011908 (2008)

    Article  ADS  Google Scholar 

  24. Khodadadi, S., Pawlus, S., Roh, J.H., Garcia-Sakai, V., Mamontov, E., Sokolov, A.P.: The origin of the dynamic transition in proteins. J. Chem. Phys. 128, 195106 (2008)

    Article  ADS  Google Scholar 

  25. Khodadadi, S., Pawlus, S., Sokolov, A.P.: Influence of hydration on protein dynamics: combining dielectric and neutron scattering spectroscopy data. J. Phys. Chem. B 112, 14273–14280 (2008)

    Article  Google Scholar 

  26. Chen, G., Fenimore, P.W., Frauenfelder, H., Mezei, F., Swenson, J., Young, R.D.: Protein fluctuations explored by inelastic neutron scattering and dielectric relaxation spectroscopy. Philos. Mag. 88, 3877–3883 (2008)

    Article  Google Scholar 

  27. Sokolov, A.P., Roh, J.H., Mamontov, E., Garcia-Sakai, V.: Role of hydration water in dynamics of biological macromolecules. Chem. Phys. 345, 212–218 (2008)

    Article  ADS  Google Scholar 

  28. Frauenfelder, H., Ghen, G., Berendzen, J., Fenimore, P.W., Jansson, H., McMahon, B.H., Stroe, I.R., Swenson, J., Young, R.D.: A unified model of protein dynamics. Proc. Natl. Acad. Sci. USA 106, 5129–5134 (2009)

    Article  ADS  Google Scholar 

  29. Parak, F., Knapp, E.W.: A consistent picture of protein dynamics. Proc. Natl. Acad. Sci. USA 81, 7088–7092 (1984)

    Article  ADS  Google Scholar 

  30. Rasmussen, B.F., Stock, A.M., Ringe, D., Petsko, G.A.: Crystalline ribonuclease-A loses function below the dynamic transition at 220K. Nature 357, 423–424 (1992)

    Article  ADS  Google Scholar 

  31. Ferrand, M., Dianoux, A.J., Petry, W., Zaccai, G.: Thermal motions and function of bacteriorhodopsin in purple membranes—effects of temperature and hydration studied by neutron-scattering. Proc. Natl. Acad. Sci. USA 90, 9668–9672 (1993)

    Article  ADS  Google Scholar 

  32. Ostermann, A., Waschipky, R., Parak, F.G., Nienhaus, G.U.: Ligand binding and conformational motions in myoglobin. Nature 404, 205–208 (2000)

    Article  ADS  Google Scholar 

  33. Dunn, R.V., Reat, V., Finney, J., Ferrand, M., Smith, J.C., Daniel, R.M.: Enzyme activity and dynamics: xylanase activity in the absence of fast anharmonic dynamics. Biochem. J. 346, 355–358 (2000)

    Article  Google Scholar 

  34. Bragger, J.M., Dunn, R.V., Daniel, R.M.: Enzyme activity down to −100 degrees C. Biochim. Biophys. Acta 1480, 278–282 (2000)

    Google Scholar 

  35. He, Y.F., Ku, P.I., Knab, J.R., Chen, J.Y., Markelz, A.G.: Protein dynamical transition does not require protein structure. Phys. Rev. Lett. 101, 178103 (2008)

    Article  ADS  Google Scholar 

  36. Mamontov, E., Zamponi, M., Hammons, S., Keener, W.S., Hagen, M., Herwig, K.W.: BASIS: A new backscattering spectrometer at the SNS. Neutron News 19, 22–24 (2008)

    Article  Google Scholar 

  37. Mamontov, E., Luo, H., Dai, S.: Proton dynamics in N,N,Nʹ,Nʹ-Tetramethylguanidinium Bis(perfluoroethylsulfonyl)imide protic ionic liquid probed by quasielastic neutron scattering. J. Phys. Chem. B 113, 159–169 (2009)

    Article  Google Scholar 

  38. Provencher, S.W., Glockner, J.: Estimation of globular protein secondary structure from circular dichroism. Biochem. 20, 33–37 (1981)

    Article  Google Scholar 

  39. Van Stokkum, I.H.M., Spoelder, H.J.W., Bloemendal, M., Van Grondelle, R., Groen, F.C.A.: Estimation of protein secondary structure and error analysis from CD spectra. Anal. Biochem. 191, 110–118 (1990)

    Article  Google Scholar 

  40. Whitmore, L., Wallace, B.A.: Protein secondary structure analysis from circular dichroism spectroscopy: methods and reference databases. Biopolymers 89, 392–400 (2008)

    Article  Google Scholar 

  41. Bée, M.: Quasielastic Neutron Scattering. Adam Hilger, Philadelphia (1988)

    Google Scholar 

  42. Nakagawa, H., Joti, Y., Kitao, A., Kataoka, M.: Hydration affects both harmonic and anharmonic nature of protein dynamics. Biophys. J. 95, 2916–2923 (2008)

    Article  ADS  Google Scholar 

  43. Receveur, V., Calmettes, P., Smith, J.C., Desmadril, M., Coddens, G., Durand, D.: Picosecond dynamical changes on denaturation of yeast phosphoglycerate kinase revealed by quasielastic neutron scattering. Proteins: Struct. Funct. Bioinformatics 28, 380–387 (1997)

    Article  Google Scholar 

  44. Zaccai, G.: How soft is a protein? A protein dynamics force constant measured by neutron scattering. Science 288, 1604–1607 (2000)

    Article  ADS  Google Scholar 

  45. Parak, F.G.: Physical aspects of protein dynamics. Rep. Prog. Phys. 66, 103–129 (2003)

    Article  ADS  Google Scholar 

  46. Frauenfelder, H., Fenimore, P.W., Chen, G., McMahon, B.H.: Protein folding is slaved to solvent motions. Proc. Natl. Acad. Sci. USA 103, 15469–15472 (2006)

    Article  ADS  Google Scholar 

  47. Tsai, A.M., Neumann, D.A., Bell, L.N.: Molecular dynamics of solid-state lysozyme as affected by glycerol and water: a neutron scattering study. Biophys. J. 79, 2728–2732 (2000)

    Article  Google Scholar 

  48. Tarek, M., Tobias, D.J.: Role of protein-water hydrogen bond dynamics in the protein dynamical transition. Phys. Rev. Lett. 88, 138101 (2002)

    Article  ADS  Google Scholar 

  49. Tournier, A.L., Xu, J., Smith, J.C.: Translational hydration water dynamics drives the protein glass transition. Biophys. J. 85, 1871–1875 (2003)

    Article  Google Scholar 

  50. Doster, W.: The dynamical transition of proteins, concepts and misconceptions. Eur. Biophys. J. 37, 591–602 (2008)

    Article  Google Scholar 

  51. Mamontov, E., Vlcek, L., Wesolowski, D.J., Cummings, P.T., Rosenqvist, J., Wang, W., Cole, D.R., Anovitz, L.M., Gasparovic, G.: Suppression of the dynamic transition in surface water at low hydration levels: a study of water on rutile. Phys. Rev. E 79, 051504 (2009)

    Article  ADS  Google Scholar 

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Acknowledgements

The authors are thankful to K. W. Herwig and C. Hoffmann for critical reading of the manuscript, and K. L. Weiss for useful technical discussions. This work was supported by the US Department of Energy Basic Energy Sciences and the Office of Biological and Environmental Research, using facilities supported by Oak Ridge National Laboratory, and managed by UT-Battelle, LLC, for the US DOE under Contract No. DE-AC05-00OR22725.

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Authors and Affiliations

  1. Neutron Scattering Science Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831-6473, USA

    Eugene Mamontov

  2. Center for Structural Molecular Biology, Chemical Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831-6142, USA

    Hugh O’Neill

  3. Bio-deuteration Laboratory, Center for Structural Molecular Biology, Chemical Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831-6142, USA

    Qiu Zhang

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  1. Eugene Mamontov
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Correspondence to Eugene Mamontov.

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Mamontov, E., O’Neill, H. & Zhang, Q. Mean-squared atomic displacements in hydrated lysozyme, native and denatured. J Biol Phys 36, 291–297 (2010). https://doi.org/10.1007/s10867-009-9184-6

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  • DOI: https://doi.org/10.1007/s10867-009-9184-6

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