Membrane Hydration: A Hint to a New Model for Biomembranes

  • E. Anibal DisalvoEmail author
Part of the Subcellular Biochemistry book series (SCBI, volume 71)


The classical view of a biological membrane is based on the Singer-Nicholson mosaic fluid model in which the lipid bilayer is the structural backbone. Under this paradigm, many studies of biological processes such as, permeability, active transport, enzyme activity and adhesion and fusion processes have been rationalized considering the lipid membrane as a low dielectric slab of hydrocarbon chains with polar head groups exposed to water at each side in which oil/water partition prevails. In spite of several analyses and evidence available in relation to membrane hydration, water is not taken into account as a functional component. For this purpose, new insights in the water organization in restricted environments and the thermodynamical and mechanical properties emerging from them are specifically analysed and correlated.

This chapter summarizes the progress of the studies of water in membranes along the book in order to give a more realistic structural and dynamical picture accounting for the membrane functional properties.


Water penetration Interphases Hydration water Confined water Complex systems Membrane models 


  1. Al-Awqati Q (1999) One hundred years of membrane permeability: does Overton still rule? Nat Cell Biol 1(8):E201–E202CrossRefPubMedGoogle Scholar
  2. Almaleck H, Gordillo GJ, Disalvo A (2013) Water defects induced by expansion and electrical fields in DMPC and DMPE monolayers: contribution of hydration and confined water. Colloids Surf B Biointerfaces 102:871–878CrossRefPubMedGoogle Scholar
  3. Antollini SS, Barrantes FJ (1998) Disclosure of discrete sites for phospholipid and sterols at the protein-lipid interface in native acetylcholine receptor-rich membrane. Biochemistry 37:16653–16662CrossRefPubMedGoogle Scholar
  4. Bagatolli LA, Ipsen JH, Simonsen AC, Mouritsen OG (2010) An outlook on organization of lipids in membranes: searching for a realistic connection with the organization of biological membranes. Prog Lipid Res 49(4):378–389CrossRefPubMedGoogle Scholar
  5. Ben-Shaul A (1995) Molecular theory of chain packing, elasticity and lipid-protein interaction in lipid bilayers. In: Lipowsky R, Sackmann E (eds) Handbook of biological physics. Elsevier Science, North-HollandGoogle Scholar
  6. Berkowitz ML, Vácha R (2012) Aqueous solutions at the interface with phospholipid bilayers. Acc Chem Res 45:74–82CrossRefPubMedGoogle Scholar
  7. Berkowitz ML, Bostick DL, Pandit S (2006) Aqueous solutions next to phospholipid membrane surfaces: insights from simulations. Chem Rev 106:1527–1539CrossRefPubMedGoogle Scholar
  8. Bhide SY, Berkowitz ML (2005) Structure and dynamics of water at the interface with phospholipid bilayers. J Chem Phys 123:224702CrossRefPubMedGoogle Scholar
  9. Chaplin MF (1999) A proposal for structuring of water. Biophys Chem 83:211–221CrossRefGoogle Scholar
  10. Chapman D, Urbina J, Keough K (1974) Studies of lipid-water systems using differential scanning calorimetry. J Biol Chem 249(8):2512–2521PubMedGoogle Scholar
  11. Chapmann D (1971) Liquid crystalline properties of phospholipids and biological membranes. Symp Faraday Soc 5:163–174CrossRefGoogle Scholar
  12. de Gier J (1989) Chapter 4: Osmotic properties of liposomes. In: Benga G (ed) Water transport in biological membranes, vol I. CRC Press, Boca RatonGoogle Scholar
  13. de Gier J, Mandersloot JG, Hupkes JV, McElhaney RNM, Van Beek NP (1971). On the mechanism of non electrolyte permeation through lipid bilayers and through biomembranes. Biochim Biophys Acta 223:610–618CrossRefGoogle Scholar
  14. Deamer DW, Volkov AG (1995) Chapter 8: Proton permeability of lipid bilayers. In: Disalvo EA, Simon SA (eds) Permeability and stability of lipid bilayers. CRC Press, Boca Raton, pp 161–178Google Scholar
  15. Debnath A, Mukherjee B, Ayappa KG et al (2010) Entropy and dynamics of water in hydration layers of a bilayer. J Chem Phys 133:174704CrossRefPubMedGoogle Scholar
  16. Disalvo EA (1986) Permeation of water and polar solutes in lipid bilayers. Adv Colloid Interf Sci 29:141–170CrossRefGoogle Scholar
  17. Disalvo EA, De Gier J (1983) Contribution of aqueous interphases to the permeability barrier of lipid bilayer for non-electrolytes. Chem Phys Lipids 32:39–47CrossRefGoogle Scholar
  18. Disalvo EA, Frías MA (2013) Water state and carbonyl distribution populations in confined regions of lipid bilayers observed by FTIR spectroscopy. Langmuir 29(23):6969–6974CrossRefPubMedGoogle Scholar
  19. Disalvo EA, Lairion F, Martini F, Tymczyszyn E, Frías M, Almaleck H, Gordillo GJ (2008) Structural and functional properties of hydration and confined water in membrane interfaces. Biochim Biophys Acta 1778:2655–2670CrossRefPubMedGoogle Scholar
  20. Disalvo EA, Bouchet AM, Frias MA (2013) Connected and isolated CH populations in acyl chains and its relation to pockets of confined water in lipid membranes as observed by FTIR spectrometry. Biochim Biophys Acta 1828:1683–1689CrossRefPubMedGoogle Scholar
  21. Evans EA, Skalak R (1980) Mechanics and thermodynamics of biomembranes. CRC Press, Boca Raton, pp 67–91Google Scholar
  22. Flory PJ (1969) Statistical mechanics of chain molecules. Interscience, New YorkGoogle Scholar
  23. Ge MT, Freed JH (2003) Hydration, structure, and molecular interactions in the headgroup region of dioleoylphosphatidylcholine bilayers: an electron spin resonance study. Biophys J 85:4023–4040PubMedCentralCrossRefPubMedGoogle Scholar
  24. Goñi FM (2014) The basic structure and dynamics of cell membranes: an update of the Singer-Nicolson model. Biochim Biophys Acta 1838(6):1467–1476CrossRefPubMedGoogle Scholar
  25. Goñi FM, Arrondo JLR (1986) A study of phospholipid 410 phosphate groups in model membranes by Fourier transform infrared 411 spectroscopy. Faraday Discuss Chem Soc 81:117–126CrossRefPubMedGoogle Scholar
  26. Gordeliy VI (1996) Possibility of direct experimental check up of the theory of repulsion forces between amphiphilic surfaces via neutron and X-ray diffraction. Langmuir 12:3498–3502CrossRefGoogle Scholar
  27. Gordeliy VI, Cherezov VG, Teixeira J (1996) Evidence of entropic contribution to “hydration” forces between membranes Part II. Temperature dependence of the “hydration” force: a small angle neutron scattering study. J Mol Struct 383:117–124CrossRefGoogle Scholar
  28. Griffith OH, Dehlinger PJ, Van SP (1974) Shape of the hydrophobic barrier of phospholipid bilayers (evidence for water penetration in biological membranes). J Membr Biol 15:159–192CrossRefPubMedGoogle Scholar
  29. Haines T, Liebovitch LS (1995) Chapter 6: A molecular mechanism for the transport of water across phospholipid bilayers. In: Disalvo EA, Simon SA (eds) Permeability and stability of lipid bilayers. CRC Press, Boca Raton, pp 137–160Google Scholar
  30. Heimburg T (2010) Lipid ion channels (review). Biophys Chem 150(1–3):2–22CrossRefPubMedGoogle Scholar
  31. Herrera FE, Bouchet A, Lairion F, Disalvo EA, Pantano S (2012) Molecular dynamics study of the interaction of arginine with phosphatidylcholine and phosphatidylethanolamine bilayers. J Phys Chem B 116:4476–4483CrossRefPubMedGoogle Scholar
  32. Ipsen JH, Mouritsen OG, Bloom M (1990) Relationships between lipid membrane area, hydrophobic thickness, and acyl- chain orientational order. Biophys J 57:405–412PubMedCentralCrossRefPubMedGoogle Scholar
  33. Israelachvili JN (1977) Refinement of the fluid-mosaic model of membrane structure. Biochim Biophys Acta 469:221–225CrossRefPubMedGoogle Scholar
  34. Israelachvili J, Wennerström H (1996) Role of hydration and water structure in biological and colloidal interactions. Nature 379(6562):219–225CrossRefPubMedGoogle Scholar
  35. Jendrasiak GL, Hasty JH (1974) The hydration of phospholipids. Biochim Biophys Acta 337(1):79–91CrossRefPubMedGoogle Scholar
  36. Jendrasiak GL, Smith RL, Shaw W (1996) The water adsorption characteristics of charged phospholipids. Biochim Biophys Acta 1279:63–69CrossRefPubMedGoogle Scholar
  37. Kedem O, Katchalsky A (1958) A thermodynamic analysis of the permeability of biological membranes to non-electrolytes. Biochim Biophys Acta 27:229–246CrossRefPubMedGoogle Scholar
  38. Kiselev M, Lesieur P, Kisselev A et al (1999) DMSO-induced dehydration of DPPC membranes studied by X-ray diffraction, small-angle neutron scattering, and calorimetry. J Alloys Compd 286:195–202CrossRefGoogle Scholar
  39. Kodama M, Kato H, Aoki H (2001) Comparison of differently bound molecules in the gel and subgel phases of a phospholipid bilayer system. J Therm Anal Calorim 64:219–230CrossRefGoogle Scholar
  40. Kuntz ID, Kauzmann W (1974) Hydration of proteins and polypeptides. Adv Protein Chem 28:239–345CrossRefPubMedGoogle Scholar
  41. Luzardo MC, Amalfa F, Nuñez AM, Díaz S, Biondi De Lopez AC, Disalvo EA (2000) Effect of trehalose and sucrose on the hydration and dipole potential of lipid bilayers. Biophys J 78(5):2452–2458PubMedCentralCrossRefPubMedGoogle Scholar
  42. MacCallum L, Bennett WF, Tieleman DP (2008) Distribution of amino acids in a lipid bilayer from computer simulations. Biophys J 94:3393–3404PubMedCentralCrossRefPubMedGoogle Scholar
  43. Malaspina DC, Rodriguez Fris JA, Appignanesi GA, Sciortino F (2009) Identifying a causal link between structure and dynamics in supercooled water. Europhys Lett 88:16003CrossRefGoogle Scholar
  44. Mathai JC, Tristram-Nagle S, Nagle JF (2008) Structural determinants of water permeability through the lipid membrane. J Gen Physiol 131(1):69–76PubMedCentralCrossRefPubMedGoogle Scholar
  45. McElhaney RN, de Gier J, van der Neut-Kok ECM (1973) The effect of alterations in fatty acid composition and cholesterol content on the nonelectrolyte permeability of Acholeplasma laidlawii B cells and derived liposomes. Biochim Biophys Acta 298:500–512CrossRefPubMedGoogle Scholar
  46. McIntosh TJ, Simon SA, Dilger JP et al (1989) Chapter 1: Location of water-hydrocarbon interface in lipid bilayers. In: Benga G (ed) Water transport in biological membranes, vol 1. CRC Press, Boca RatonGoogle Scholar
  47. Murzyn K, Zhao W, Karttunen M et al (2006) Dynamics of water at membrane surfaces: effect of headgroup structure. Biointerphases 1:98–105CrossRefPubMedGoogle Scholar
  48. Nagle JF, Tristram-Nagle S (2000) Structure of lipid bilayers. Biochim Biophys Acta Rev Biomembr 1469(3):159–195CrossRefGoogle Scholar
  49. Overton E (1889) Über die allgemeinen osmotischen Eigenschaften der Zelle, ihre vermutlichen Ursachen und ihre Bedeutung für die Physiologie. Vierteljahrsschr Natur-forsch Ges Zürich 44:88–135Google Scholar
  50. Parasassi T, Gratton E (1995) Membrane lipid domains and dynamics as detected by LAURDAN fluorescence. J Fluoresc 5:59–69CrossRefPubMedGoogle Scholar
  51. Parasassi T, Gratton E, Yu WM, Wilson P, Levi M (1997) Two-photon fluorescence microscopy of laurdan generalized polarization domains in model and natural membranes. Biophys J 72:2413–2429PubMedCentralCrossRefPubMedGoogle Scholar
  52. Pinnick ER, Erramilli S, Wang F (2010) Computational investigation of lipid hydration water of L α 1-palmitoyl-2-oleoyl- sn -glycero-3-phosphocholine at three hydration levels. Mol Phys 108:2027–2036CrossRefGoogle Scholar
  53. Preston Moon C, Fleming KG (2011) Side-chain hydrophobicity scale derived from transmembrane protein folding into lipid bilayers. Proc Natl Acad Sci U S A 108(25):10174–10177PubMedCentralCrossRefPubMedGoogle Scholar
  54. Simon SA, McIntosh TJ (1986) Depth of water penetration into lipid bilayers. Methods Enzymol 127:511–521CrossRefPubMedGoogle Scholar
  55. Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175(23):720–723CrossRefPubMedGoogle Scholar
  56. Sovago M, Vartiainen E, Bonn M (2009) Observation of buried water molecules in phospholipid membranes by surface sum-frequency generation spectroscopy. J Chem Phys 131:161107–161111CrossRefPubMedGoogle Scholar
  57. Sparr E, Wennerström H (2001) Responding phospholipid membranes—interplay between hydration and permeability. Biophys J 81(2):1014–1028PubMedCentralCrossRefPubMedGoogle Scholar
  58. Ti Tien H, Ottova AL (2001) The lipid bilayer concept and its experimental realization: from soap bubbles, kitchen sink, to bilayer lipid membranes. J Membr Sci 189:83–117CrossRefGoogle Scholar
  59. Träuble H (1971) The movement of molecules across lipid membranes: a molecular theory. J Membr Biol 4(1):193–208CrossRefPubMedGoogle Scholar
  60. Van Zoelen EJJ, Blok MC, De Gier J (1976) An improved method for the description of non-electrolyte permeation through liposomes, based on irreversible thermodynamics. Biochim Biophys Acta Biomembr 436(2):301–306CrossRefGoogle Scholar
  61. Viera LI, Alonso-Romanowski S, Borovyagin V, Feliz MR, Disalvo EA (1993) Properties of gel phase lipid-trehalose bilayers upon rehydration. Biochim Biophys Acta 1145(1):157–167CrossRefPubMedGoogle Scholar
  62. Villarreal MA, Díaz SB, Disalvo EA, Montich GG (2004) Molecular dynamics simulation study of the interaction of trehalose with lipid membranes. Langmuir 20:7844–7851CrossRefPubMedGoogle Scholar
  63. White SH (1976) The lipid bilayer as a “solvent” for small hydrophobic molecules. Nature 262:421–422CrossRefPubMedGoogle Scholar
  64. Wimley C, White SH (1996) Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat Struct Biol 3:842–848CrossRefPubMedGoogle Scholar
  65. Yeagle PL (2004) The structure of biological membranes, 2nd edn. CRC Press, Boca Raton (FL).Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Laboratorio de Biointerfases y Sistemas BiomimeticosCentro de Investigacion y Transferencia de Santiago del Estero, Universidad Nacional de Santiago del Estero-Consejo Nacional de Investigaciones Científicas y TécnicasSantiago del EsteroArgentina

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