Skip to main content
SpringerLink
Log in

The glassy state of water: A ‘stop and go’ device for biological processes

  • Chapter
Water and the Cell

  • 1068 Accesses

Abstract

What is unique about the properties of intracellular water that prevent its replacement by another compound? We tackle this question by combining experimental techniques as diverse as Electron Spin Resonance, Thermally Stimulated Depolarization Current, broadband dielectric spectroscopy, and neutron diffraction to a set of samples, namely a globular enzyme, intact plant seeds, and porous silica glasses, largely differing in terms of composition and complexity. Results indicate that interfacial and intracellular water is directly involved in the formation of amorphous matrices, with glass-like structural and dynamical properties. We propose that this glassiness of water, geometrically confined by the presence of solid intracellular surfaces, is a key characteristic that has been exploited by Nature in setting up a mechanism able to match the quite different time scales of protein and solvent dynamics, namely to slow down fast solvent dynamics to make it overlap with the much slower protein turnover times in order to sustain biological functions. Additionally and equally important, the same mechanism can be used to completely stop or slow down biological processes, as a protection against extreme conditions such as low temperature or dehydration

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Angell CA, Tucker JC (1979) Heat capacity changes in glass-forming aqueous solutions and the glass transition in vitreous water. J Phys Chem 84:268–272

    Article  Google Scholar 

  • Angell CA, Ngai KL, McKenna GB, McMillan PF, Martin SW (2000) Relaxation in glassforming liquids and amorphous solids. J Appl Phys 88:3113–3157

    Article  CAS  Google Scholar 

  • Arcangeli C, Bizzarri AR, Cannistraro S (1998) Role of interfacial water in the molecular dynamics-simulated dynamical transition of plastocyanin. Chem Phys Letters 291:7–14

    Article  CAS  Google Scholar 

  • Bizzarri AR, Rocchi C, Cannistraro S (1996) Origin of the anomalous diffusion observed by MD simulation at the protein-water interface. Chem Phys Letters 263:559–566

    Article  CAS  Google Scholar 

  • Bizzarri AR, Paciaroni A, Cannistraro S (2000) Glasslike dynamical behavior of the plastocyanin hydration water. Phys Rev E 62:3991–3999

    Article  CAS  Google Scholar 

  • Bizzarri AR, Cannistraro S (2002) Molecular Dynamics of Water at the Protein-Solvent Interface. J Phys Chem B 106:6617–6633

    Article  CAS  Google Scholar 

  • Botti A, Bruni F, Imberti S, Ricci MA, Soper AK (2004) Ions in water: The microscopic structure of concentrated NaOH solutions. J Chem Phys 120:10154–10162

    Article  PubMed  CAS  Google Scholar 

  • Bruni F, Careri G, Clegg JS (1989) Dielectric properties of Artemia cysts at low water contents. Evidence for a percolative transition. Biophys J 55:331–338

    PubMed  CAS  Google Scholar 

  • Bruni F, Careri G, Leopold AC (1989) Critical exponents of protonic percolation in maize seeds. Phys Rev A 40:2803–2805

    Article  PubMed  CAS  Google Scholar 

  • Bruni F, Leopold AC (1991) Glass transitions in soybean seed. Relevance to anhydrous biology. Plant Physiol 96:660–663

    PubMed  Google Scholar 

  • Bruni F, Ricci MA, Soper AK (1998) Water confined in Vycor glass. I. A neutron diffraction study. J Chem Phys 109:1478–1485

    Article  CAS  Google Scholar 

  • Bruni F, Pagnotta SE (2004) Dielectric investigation of the temperature dependence of the dynamics of a hydrated protein. Phys Chem Chem Phys 6:1912–1919

    Article  CAS  Google Scholar 

  • Bucci C, Fieschi R (1966) Ionic thermocurrents in dielectrics. Phys Rev 148:816–823

    Article  CAS  Google Scholar 

  • Buitink J, van den Dries I, Hoeckstra FA, Alberda M, Hemminga MA (2000) High critical temperature above Tg may contribute to the stability of biological systems. Biophys J 79:1119–1128

    PubMed  CAS  Google Scholar 

  • Bulone D, San Biagio PL, Palma-Vittorelli MB, Palma MU (1993) The role of water in hemoglobin function and stability. Science 259:1335–1336

    Article  PubMed  CAS  Google Scholar 

  • Bundle A, Haulin S (eds) (1991) Fractals and Disordered Systems. Springer, Berlin

    Google Scholar 

  • Caliskan G, Mechtani D, Roh JH, Kisliuk A, Sokolov AP, Azzam S et al (2004) Protein and solvent dynamics: How strongly are they coupled? J Chem Phys 121:1978–1983

    Article  PubMed  CAS  Google Scholar 

  • Clegg JS, Drost-Hansen W (1991) On the biochemistry and cell physiology of water. In: Hochachka A, Mommsen B (eds), Biochemistry and Molecular Biology of Fishes. Elsevier, pp 1–23

    Google Scholar 

  • Colombo MF, Rau DC, Parsegian VA (1992) Protein solvation in allosteric regulation: A water effect on hemoglobin. Science 256:655–659

    Article  PubMed  CAS  Google Scholar 

  • Courtens E (1984) Vogel-Fulcher scaling of the susceptibility in a mixed-crystal proton glass. Phys Rev Lett 52:69–72

    Article  CAS  Google Scholar 

  • Courtens E (1986) Scaling dielectric data on Rb1-x(NH_4)H_2PO_4 structural glasses and their deuterated isomorphs. Phys Rev B 33:2975–2978

    Article  CAS  Google Scholar 

  • Cusack S, Doster W (1990) Temperature dependence of the low frequency dynamics of myoglobin. Measurement of the vibrational frequency distribution by inelastic neutron scattering. Biophys J 58:243–251

    PubMed  CAS  Google Scholar 

  • Daniel RM, Finney JL, Réat V, Dunn R, Ferrand M, Smith JC (1999) Enzyme dynamics and activity: Time-scale dependence of dynamical transitions in glutamate dehydrogenase solution. Biophys J 77:2184–2190

    PubMed  CAS  Google Scholar 

  • Daniel RM, Finney JL, Stoneham M (2004) The molecular basis of life. Is life possible without water? Phil trans R Soc Lond B 359:1143

    Article  Google Scholar 

  • Doster W, Bachleitner A, Dunau R, Hiebl M, Lüscher E (1986) Thermal properties of water in myoglobin crystals and solutions at subzero temperatures. Biophys J 50:213–219

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Diehl M, Doster W, Petry W, Schober H (1997) Water-coupled low-frequency modes of myoglobin and lysozyme observed by inelastic neutron scattering. Biophys J 73:2726–2732

    PubMed  CAS  Google Scholar 

  • Drukker K, de Leeuw SW, Hammes-Schiffer S (1998) Proton transport along water chains in an electric field. J Chem Phys 108:6799–6808

    Article  CAS  Google Scholar 

  • Ediger MD, Angell CA, Nagel SR (1996) Supercooled liquids and glasses. J Phys Chem 100:13200–13212

    Article  CAS  Google Scholar 

  • Fenmore PW, Frauenfelder H, McMahon BH, Young RD (2004) Bulk-solvent and hydration-shell fluctuations, similar to α- and β-fluctuations in glasses, control protein motions and functions. Proc Natl Acad Sci USA 101:14408–14413

    Article  Google Scholar 

  • Finney JL (1982) Solvent effects in biomolecular processes. In: Franks F, Mathias SF (eds), Biophysics of Water. John Wiley & Sons, New York, pp 55–58

    Google Scholar 

  • Finney JL (2004) Water? What’s so special about it? Phil Trans R Soc Lond B 359:1145–1165

    Article  CAS  Google Scholar 

  • Fitter J (1999) The temperature dependence of internal molecular motions in hydrated and dry α Amylase: the role of hydration water in the dynamical transition of proteins. Biophys J 76:1034–1042

    PubMed  CAS  Google Scholar 

  • Franks F (1985) Biophysics and Biochemistry at Low Temperatures. Cambridge University Press, Cambridge

    Google Scholar 

  • Frauenfelder H (1989) New looks at protein motions. Nature 338:623–624

    Article  Google Scholar 

  • Frauenfelder H, Sligar SG, Wolynes PG (1991) The energy landscapes and motions of proteins. Science 254:1598–1603

    Article  PubMed  CAS  Google Scholar 

  • Green JL, Angell CA (1989) Phase relations and vitrification in saccharide-water solutions and the trehalose anomaly. J Phys Chem 93:2880–2882

    Article  CAS  Google Scholar 

  • Green JL, Fan J, Angell CA (1994) The protein-glass analogy: Some insights from homopeptide comparison. J Phys Chem 98:13780–13790

    Article  CAS  Google Scholar 

  • Gregory RB (1995) Protein hydration and glass transition behavior. In: Gregory RB (ed), Protein-Solvent Interactions. Marcel Dekker, Inc., New York, pp 191–264

    Google Scholar 

  • Iben IET, Braunstein D, Doster W, Frauenfelder H, Hong MK, Johnson JB et al (1989) Glassy behavior of proteins. Phys Rev Lett 62:1916–1919

    Article  PubMed  CAS  Google Scholar 

  • Kohen A, Cannio R, Bartolucci S, Klinman JP (1999) Enzyme dynamics and hydrogen tunneling in a thermophilic alcohol dehydrogenase. Nature 399:496–499

    Article  PubMed  CAS  Google Scholar 

  • Kuntz ID Jr, Kauzmann W (1974) Hydration of proteins and polypeptides. Adv Protein Chem 28:239–345

    PubMed  CAS  Google Scholar 

  • Kunst M, Warman JM (1980) Proton mobility in ice. Nature 288:465–467

    Article  CAS  Google Scholar 

  • Kutnjak Z, Filipic C, Levstik A, Pirc R (1993) Glassy dynamics of Rb0.4(ND_4)0.6OD_2PO_4. Phys Rev Lett 70:4015–4018

    Article  PubMed  CAS  Google Scholar 

  • Kuznetsov AM, Ulstrup J (1994) Dynamics of low-barrier proton transfer in polar solvents and protein media. Chem Phys 188:131–141

    Article  CAS  Google Scholar 

  • Lemke N, Campbell IA (1996) Random walks in a closed space. Physica A 230:554–562

    Article  CAS  Google Scholar 

  • Levstik A, Kutnjak Z, Filipic C, Pirc R Phys. Rev. B (1998), 57:11204.

    Google Scholar 

  • Lobaugh J, Voth GA (1996) The quantum dynamics of an excess proton in water. J Chem Phys 104:2056–2069

    Article  CAS  Google Scholar 

  • MacKenzie AP (1977) Non-equilibrium freezing behavior of aqueous systems. Phil Trans R Soc London B 278:167–189

    Article  CAS  Google Scholar 

  • Marx D, Tuckerman ME, Hutter J, Parrinello M (1999) The nature of the hydrated excess proton in water. Nature 397:601–604

    Article  CAS  Google Scholar 

  • Mascarenhas S (1987) Bioelectrets: Electrets in biomaterials and biopolymers. In: Sessler GM (ed), Electrets. Springer-Verlag, Berlin, pp 321–346

    Google Scholar 

  • Merzel F, Smith JC (2002) Is the first hydration shell of lysozyme of higher density than bulk water? Proc Natl Acad Sci USA 99:5378–5383

    Article  PubMed  CAS  Google Scholar 

  • Nienhaus GU, Müller JD, MacMahon BH, Frauenfelder H (1997) Exploring the conformational energy landscape of proteins. Physica D 107:297–311

    Article  CAS  Google Scholar 

  • Oleinikova A, Smolin N, Brovchenko I, Geiger A, Winter R (2005) Formation of spanning water networks on protein surfaces via 2D percolation transition. J Phys Chem B 109:1988–1998

    Article  PubMed  CAS  Google Scholar 

  • Pagnotta SE, Gargana R, Bruni F, Bocedi A (2005) Glassy dynamics of a percolative water-protein system. Phys Rev E 71:031506

    Article  CAS  Google Scholar 

  • Pérez J, Zanotti J-M, Durand D (1999) Evolution of internal dynamics of two globular proteins from dry powder to solution. Biophys J 77:454–469

    PubMed  Google Scholar 

  • Pertsemlidis A, Saxena AM, Soper AK, Head-Gordon T, Glaeser M (1996) Direct evidence for modified nsolvent structure within the hydration shell of a hydrophobic amino acid. Proc Natl Acad Sci USA 93:10769–10774

    Article  PubMed  CAS  Google Scholar 

  • Peyrard M (2001) Glass transition in protein hydration water. Phys Rev E 64:011109

    Article  CAS  Google Scholar 

  • Pizzitutti F, Bruni F (2001) Glassy dynamics and enzymatic activity of lysozyme. Phys Rev E 64:052905

    Article  CAS  Google Scholar 

  • Rupley JA, Siemankowski L, Careri G, Bruni F (1988) Two-dimensional protonic percolation on lightly hydrated purple membrane. Proc Natl Acad Sci USA 85:9022–9025

    Article  PubMed  CAS  Google Scholar 

  • Rupley JA, Careri G (1991) Protein hydration and function. Adv Protein Chem 41:37–172

    Article  PubMed  CAS  Google Scholar 

  • Sartor G, Hallbrucker A, Mayer E (1995) Characterizing the secondary hydration shell on hydrated myoglobin, hemoglobin, and lysozyme powders by its vitrification behavior on cooling and its calorimetric glass-liquid transition and crystallization behavior on reheating. Biophys J 69:2679

    PubMed  CAS  Google Scholar 

  • Singh GP, Parak F, Hunklinger S, Dransfeld K (1981) Role of adsorbed water in the dynamics of metmyoglobin. Phys Rev Lett 47:685–688

    Article  CAS  Google Scholar 

  • Smedarchina Z, Slebrand W, Fernàndez-Ramos A (2000) A direct-dynamics study of proton transfer through water bridges in guanine and 7-azaindole. J Chem Phys 112:566–573

    Article  CAS  Google Scholar 

  • Smolin N, Oleinikova A, Brovchenko I, Geiger A, Winter R (2005) Properties of spanning water networks at protein surfaces. J Phys Chem B 109:10995–11005

    Article  PubMed  CAS  Google Scholar 

  • Soper AK, Bruni F, Ricci MA (1998) Water confined in Vycor glass. II. Excluded volume effects on the radial distribution functions. J Chem Phys 109:1486–1494

    Article  CAS  Google Scholar 

  • Stauffer D, Aharony A (1992) Introduction to Percolation Theory, Taylor and Francis, London.

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Takahashi T, Hirsh A (1985) Calorimetric studies of the state of water in deeply frozen human monocytes. Biophys J 47:373–380

    Article  PubMed  CAS  Google Scholar 

  • Van Turnhout J (1987) Thermally stimulated discharge of electrets. In: Sessler GN (ed), Electrets. Springer-Verlag, Berlin, pp 81–215

    Google Scholar 

  • Vertucci CW (1989) Effects of cooling rate on seeds exposed to liquid nitrogen temperatures. Plant Physiol 90:1478–1485

    PubMed  Google Scholar 

  • Walters C (2004) Temperature dependency of molecular mobility in preserved seeds. Biophys J 86:1253–1258

    PubMed  CAS  Google Scholar 

  • Williams RJ, Leopold AC (1989) The glassy state in corn embryos. Plant Physiol 89:977–981

    Article  PubMed  Google Scholar 

  • Wilson G, Hecht L, Barron LD (1997) Evidence for a new cooperative transition in native lysozyme from temperature-dependent Raman optical activity. J Phys Chem B 101:694–698

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Dipartimento di Medicina Sperimentale e Scienze Biochimiche, Universitá degli Studi di Roma ‘‘Tor Vergata’’, Via Montpellier, 00100 Roma, Italy

    S.E. Pagnotta

  2. Dipartimento di Fisica ‘‘E. Amaldi’’, Universitá degli Studi di Roma Tre Via della Vasca Navale 84, 00146 Roma, Italy

    F. Bruni

Authors
  1. S.E. Pagnotta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Bruni
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to F. Bruni .

Editor information

Editors and Affiliations

  1. Department of Bioengineering, University of Washington, Seattle WA, USA

    Gerald H. Pollack

  2. Department of Cellular and Structural Biology, UTHSCSA, San Antonio, TX, USA

    Ivan L. Cameron

  3. BioMedES, Aberdeen, UK

    Denys N. Wheatley

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Springer

About this chapter

Cite this chapter

Pagnotta, S., Bruni, F. (2006). The glassy state of water: A ‘stop and go’ device for biological processes. In: Pollack, G.H., Cameron, I.L., Wheatley, D.N. (eds) Water and the Cell. Springer, Dordrecht. https://doi.org/10.1007/1-4020-4927-7_4

Download citation

Publish with us

Policies and ethics

Search

Navigation