Abstract
It is commonly assumed that the structure of water at a lipid-water interface is influenced mostly in the first hydration layer. However, recent results from different experimental methods show that perturbation extends through several hydration layers. Due to its low light penetration depth, attenuated total reflection Fourier transform infrared (ATR-FTIR) spectroscopy is specifically suited to study interlamellar water structure in multibilayers. Results obtained by this technique confirm the long-range water structure disturbance. Consequently, in confined membrane environments nearly all water molecules can be perturbed. It is important to note that the behavior of confined water molecules differs significantly in samples prepared in excess water and in partially hydrated samples. We show in what manner the interlamellar water perturbation is influenced by the hydration level and how it is sequentially modified with a step-by-step dehydration of samples either by water evaporation or by osmotic pressure. Our results also indicate that besides different levels of hydration the lipid-water interaction is modulated by different lipid headgroups and different lipid phases as well. Therefore, modification of interlamellar water properties may clarify the role of water-mediated effects in biological processes.
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Arnold K, Pratsch L, Gawrisch K (1983) Effect of poly(ethylene glycol) on phospholipid hydration and polarity of the external phase. Biochim Biophys Acta 728:121–128
Arrondo J, Goni F, Macarulla J (1984) Infrared spectroscopy of phosphatidylcholines in aqueous suspension a study of the phosphate group vibrations. Biochim Biophys Acta 794:165–168
Arsov Z, Quaroni L (2007) Direct interaction between cholesterol and phosphatidylcholines in hydrated membranes revealed by ATR-FTIR spectroscopy. Chem Phys Lipids 150:35–48
Arsov Z, Rappolt M, Grdadolnik J (2009) Weakened hydrogen bonds in water confined between lipid bilayers: the existence of a long-range attractive hydration force. Chemphyschem 10:1438–1441
Ball P (2008a) Water as a biomolecule. Chemphyschem 9:2677–2685
Ball P (2008b) Water as an active constituent in cell biology. Chem Rev 108:74–108
Beranová L, Humpolíčková J, Sýkora J et al (2012) Effect of heavy water on phospholipid membranes: experimental confirmation of molecular dynamics simulations. Phys Chem Chem Phys 14:14516–14522
Berger C, Desbat B, Kellay H et al (2003) Water confinement effects in black soap films. Langmuir 19:1–5
Bergmann U, Nordlund D, Wernet P et al (2007) Isotope effects in liquid water probed by x-ray Raman spectroscopy. Phys Rev B 76:024202
Berkowitz ML, Vácha R (2012) Aqueous solutions at the interface with phospholipid bilayers. Acc Chem Res 45:74–82
Berkowitz ML, Bostick DL, Pandit S (2006) Aqueous solutions next to phospholipid membrane surfaces: insights from simulations. Chem Rev 106:1527–1539
Bhide SY, Berkowitz ML (2005) Structure and dynamics of water at the interface with phospholipid bilayers. J Chem Phys 123:224702
Binder H (2003) The molecular architecture of lipid membranes—new insights from hydration-tuning infrared linear dichroism spectroscopy. Appl Spectrosc Rev 38:15–69
Binder H (2007) Water near lipid membranes as seen by infrared spectroscopy. Eur Biophys J 36:265–279
Binder H, Arnold K, Ulrich AS, Zschörnig O (2001) Interaction of Zn2+ with phospholipid membranes. Biophys Chem 90:57–74
Boissière C, Brubach JB, Mermet A et al (2002) Water confined in lamellar structures of AOT surfactants: an infrared investigation. J Phys Chem B 106:1032–1035
Bonn M, Bakker HJ, Tong Y, Backus EHG (2012) No ice-like water at aqueous biological interfaces. Biointerphases 7:20
Bouchet AM, Frías MA, Lairion F et al (2009) Structural and dynamical surface properties of phosphatidylethanolamine containing membranes. Biochim Biophys Acta 1788:918–925
Brubach J-B, Mermet A, Filabozzi A et al (2005) Signatures of the hydrogen bonding in the infrared bands of water. J Chem Phys 122:184509
Casal H, Mantsch H (1984) Polymorphic phase behaviour of phospholipid membranes studied by infrared spectroscopy. Biochim Biophys Acta Rev Biomembr 779:381–401
Cavaille D, Combes D, Zwick A (1996) Effect of high hydrostatic pressure and additives on the dynamics of water: a Raman spectroscopy study. J Raman Spectrosc 27:853–857
Chakraborty S, Bandyopadhyay S (2008) Dynamics of water in the hydration layer of a partially unfolded structure of the protein HP-36. J Phys Chem B 112:6500–6507
Chaplin M (2006) Do we underestimate the importance of water in cell biology? Nat Rev Mol Cell Biol 7:861–866
Chen X, Hua W, Huang Z, Allen HC (2010) Interfacial water structure associated with phospholipid membranes studied by phase-sensitive vibrational sum frequency generation spectroscopy. J Am Chem Soc 132:11336–11342
Cheng J-X, Pautot S, Weitz DA, Xie XS (2003) Ordering of water molecules between phospholipid bilayers visualized by coherent anti-Stokes Raman scattering microscopy. Proc Natl Acad Sci U S A 100:9826–9830
Costigan SC, Booth PJ, Templer RH (2000) Estimations of lipid bilayer geometry in fluid lamellar phases. Biochim Biophys Acta 1468:41–54
Cringus D, Lindner J, Milder MTW et al (2005) Femtosecond water dynamics in reverse-micellar nanodroplets. Chem Phys Lett 408:162–168
Damodaran K, Merz K (1993) Head group-water interactions in lipid bilayers: a comparison between DMPC-and DLPE-based lipid bilayers. Langmuir 9:1179–1183
Debnath A, Mukherjee B, Ayappa KG et al (2010) Entropy and dynamics of water in hydration layers of a bilayer. J Chem Phys 133:174704
Disalvo EA, Frias MA (2013) Water state and carbonyl distribution populations in confined regions of lipid bilayers observed by FTIR spectroscopy. Langmuir 29:6969–6974
Disalvo EA, Lairion F, Martini F et al (2008) Structural and functional properties of hydration and confined water in membrane interfaces. Biochim Biophys Acta 1778:2655–2670
Disalvo EA, Bouchet AM, Frias MA (2013) Connected and isolated CH2 populations in acyl chains and its relation to pockets of confined water in lipid membranes as observed by FTIR spectrometry. Biochim Biophys Acta 1828:1683–1689
Ebbinghaus S, Kim SJ, Heyden M et al (2007) An extended dynamical hydration shell around proteins. Proc Natl Acad Sci U S A 104:20749–20752
Faure C, Bonakdar L, Dufourc EJ (1997) Determination of DMPC hydration in the Lα and Lβ′ phases by 2H solid state NMR of D2O. FEBS Lett 405:263–266
Finer E, Darke A (1974) Phospholipid hydration studied by deuteron magnetic resonance spectroscopy. Chem Phys Lipids 12:1–16
Fitter J, Lechner RE, Dencher NA (1999) Interactions of hydration water and biological membranes studied by neutron scattering. J Phys Chem B 103:8036–8050
Fringeli UP, Günthard HH (1981) Infrared membrane spectroscopy. In: Grell E (ed) Membrane spectroscopy. Springer, Berlin, pp 270–332
Fukuma T, Higgins MJ, Jarvis SP (2007) Direct imaging of individual intrinsic hydration layers on lipid bilayers at Angstrom resolution. Biophys J 92:3603–3609
Gallová J, Uhríková D, Kučerka N et al (2011) The effects of cholesterol and β-sitosterol on the structure of saturated diacylphosphatidylcholine bilayers. Eur Biophys J 40:153–163
Gauger DR, Andrushchenko VV, Bour P, Pohle W (2010) A spectroscopic method to estimate the binding potency of amphiphile assemblies. Anal Bioanal Chem 398:1109–1123
Goormaghtigh E, Raussens V, Ruysschaert JM (1999) Attenuated total reflection infrared spectroscopy of proteins and lipids in biological membranes. Biochim Biophys Acta 1422:105–185
Grdadolnik J, Kidrič J, Hadži D (1991) Hydration of phosphatidylcholine reverse micelles and multilayers—an infrared spectroscopic study. Chem Phys Lipids 59:57–68
Grdadolnik J, Kidrič J, Hadži D (1994) An FT-IR study of water hydrating dipalmitoylphosphatidylcholine multibilayers and reversed micelles. J Mol Struct 322:93–102
Guo Y, Yui H, Minamikawa H et al (2005) FT-IR study of the interlamellar water confined in glycolipid nanotube walls. Langmuir 21:4610–4614
Hansen FY, Peters GH, Taub H, Miskowiec A (2012) Diffusion of water and selected atoms in DMPC lipid bilayer membranes. J Chem Phys 137:204910
Harrick NJ (1987) Internal reflection spectroscopy, 3rd edn. Harrick Scientific Corporation, New York
Higgins MJ, Polcik M, Fukuma T et al (2006) Structured water layers adjacent to biological membranes. Biophys J 91:2532–2542
Hishida M, Tanaka K (2011) Long-range hydration effect of lipid membrane studied by terahertz time-domain spectroscopy. Phys Rev Lett 106:158102
Hodzic A, Rappolt M, Amenitsch H et al (2008) Differential modulation of membrane structure and fluctuations by plant sterols and cholesterol. Biophys J 94:3935–3944
Hübner W, Blume A (1998) Interactions at the lipid–water interface. Chem Phys Lipids 96:99–123
Ipsen JH, Karlström G, Mourtisen OG et al (1987) Phase equilibria in the phosphatidylcholine-cholesterol system. Biochim Biophys Acta Biomembr 905:162–172
Janiak M, Small D, Shipley G (1979) Temperature and compositional dependence of the structure of hydrated dimyristoyl lecithin. J Biol Chem 254:6068–6078
Jendrasiak G (1996) The hydration of phospholipids and its biological significance. J Nutr Biochem 7:599–609
Kasson PM, Lindahl E, Pande VS (2011) Water ordering at membrane interfaces controls fusion dynamics. J Am Chem Soc 133:3812–3815
Katsaras J (1997) Highly aligned lipid membrane systems in the physiologically relevant “excess water” condition. Biophys J 73:2924–2929
Kim J, Lu W, Qiu W et al (2006) Ultrafast hydration dynamics in the lipidic cubic phase: discrete water structures in nanochannels. J Phys Chem B 110:21994–22000
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 286:195–202
Kodama M, Aoki H, Takahashi H, Hatta I (1997) Interlamellar waters in dimyristoylphosphatidylethanolamine-water system as studied by calorimetry and X-ray diffraction. Biochim Biophys Acta 1329:61–73
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 64:219–230
Kodama M, Kawasaki Y, Aoki H, Furukawa Y (2004) Components and fractions for differently bound water molecules of dipalmitoylphosphatidylcholine-water system as studied by DSC and 2H-NMR spectroscopy. Biochim Biophys Acta 1667:56–66
Kucerka N, Liu Y, Chu N et al (2005) Structure of fully hydrated fluid phase DMPC and DLPC lipid bilayers using X-ray scattering from oriented multilamellar arrays and from unilamellar vesicles. Biophys J 88:2626–2637
Kuntz ID, Kauzmann W (1974) Hydration of proteins and polypeptides. Adv Protein Chem 28:239–345
Lafleur M, Pigeon M, Pezolet M, Caille J-P (1989) Raman spectrum of interstitial water in biological systems. J Phys Chem 93:1522–1526
Lefèvre T, Toscani S, Picquart M, Dugué J (2002) Crystallization of water in multilamellar vesicles. Eur Biophys J 31:126–135
Levinger N (2002) Water in confinement. Science 298:1722–1723
Lewis RNAH, McElhaney RN (2007) Fourier transform infrared spectroscopy in the study of lipid phase transitions in model and biological membranes: practical considerations. Methods Mol Biol 400:207–226
Libnau FO, Toft J, Christy AA, Kvalheim OM (1994) Structure of liquid water determined from infrared temperature profiling and evolutionary curve resolution. J Am Chem Soc 116:8311–8316
Lucent D, Vishal V, Pande VS (2007) Protein folding under confinement: a role for solvent. Proc Natl Acad Sci U S A 104:10430–10434
Mallikarjunaiah KJ, Leftin A, Kinnun JJ et al (2011) Solid-state 2H NMR shows equivalence of dehydration and osmotic pressures in lipid membrane deformation. Biophys J 100:98–107
Manciu M, Ruckenstein E (2007) On possible microscopic origins of the swelling of neutral lipid bilayers induced by simple salts. J Colloid Interface Sci 309:56–67
Mantsch H (1984) Biological applications of Fourier transform infrared spectroscopy: a study of phase transitions in biomembranes. J Mol Struct 113:201–212
Mantsch HH, McElhaney RN (1991) Phospholipid phase transitions in model and biological membranes as studied by infrared spectroscopy. Chem Phys Lipids 57:213–226
Maréchal Y (1991) Infrared spectra of water. I. Effect of temperature and of H/D isotopic dilution. J Chem Phys 95:5565–5573
Marinov R, Dufourc E (1996) Thermotropism and hydration properties of POPE and POPE-cholesterol systems as revealed by solid state 2H and 31P-NMR. Eur Biophys J 24:423–431
Markova N, Sparr E, Wadsö L, Wennerström H (2000) A calorimetric study of phospholipid hydration. Simultaneous monitoring of enthalpy and free energy. J Phys Chem B 104:8053–8060
McIntosh TJ, Simon SA (1986) Hydration force and bilayer deformation: a reevaluation. Biochemistry 25:4058–4066
McIntosh T, Simon S (1994) Hydration and steric pressures between phospholipid bilayers. Annu Rev Biophys Biomol Struct 23:27–51
McIntosh TJ, Simon SA (1996) Adhesion between phosphatidylethanolamine bilayers. Langmuir 12:1622–1630
Mennicke U, Salditt T (2002) Preparation of solid-supported lipid bilayers by spin-coating. Langmuir 18:8172–8177
Milhaud J (2004) New insights into water-phospholipid model membrane interactions. Biochim Biophys Acta 1663:19–51
Miller IR, Bach D (1999) Hydration of phosphatidyl serine multilayers and its modulation by conformational change induced by correlated electrostatic interaction. Bioelectrochem Bioenerg 48:361–367
Mills M, Orr BG, Banaszak Holl MM, Andricioaei I (2013) Attractive hydration forces in DNA-dendrimer interactions on the nanometer scale. J Phys Chem B 117:973–981
Murzyn K, Zhao W, Karttunen M et al (2006) Dynamics of water at membrane surfaces: effect of headgroup structure. Biointerphases 1:98–105
Nagle J, Katsaras J (1999) Absence of a vestigial vapor pressure paradox. Phys Rev E 59:7018–7024
Nagle JF, Tristram-Nagle S (2000) Structure of lipid bilayers. Biochim Biophys Acta Rev Biomembr 1469:159–195
Némethy G, Scheraga HA (1964) Structure of water and hydrophobic bonding in proteins. IV. The thermodynamic properties of liquid deuterium oxide. J Chem Phys 41:680–689
Okamura E, Umemura J, Takenaka T (1990) Orientation studies of hydrated dipalmitoylphosphatidylcholine multibilayers by polarized FTIR-ATR spectroscopy. Biochim Biophys Acta 1025:94–98
Omta AW, Kropman MF, Woutersen S, Bakker HJ (2003) Influence of ions on the hydrogen-bond structure in liquid water. J Chem Phys 119:12457–12461
Pandit SA, Bostick D, Berkowitz ML (2003) An algorithm to describe molecular scale rugged surfaces and its application to the study of a water/lipid bilayer interface. J Chem Phys 119:2199–2205
Parasassi T, De Stasio G, Ravagnan G et al (1991) Quantitation of lipid phases in phospholipid vesicles by the generalized polarization of Laurdan fluorescence. Biophys J 60:179–189
Paré C, Lafleur M (1998) Polymorphism of POPE/cholesterol system: a 2H nuclear magnetic resonance and infrared spectroscopic investigation. Biophys J 74:899–909
Parsegian VA, Zemb T (2011) Hydration forces: observations, explanations, expectations, questions. Curr Opin Colloid Interface Sci 16:618–624
Parsegian V, Rand R, Fuller N, Rau D (1986) Osmotic stress for the direct measurement of intermolecular forces. Methods Enzymol 127:400–416
Pasenkiewicz-Gierula M, Takaoka Y, Miyagawa H et al (1997) Hydrogen bonding of water to phosphatidylcholine in the membrane as studied by a molecular dynamics simulation: location, geometry, and lipid-lipid bridging via hydrogen-bonded water. J Phys Chem A 101:3677–3691
Petrache H, Gouliaev N, Tristram-Nagle S et al (1998a) Interbilayer interactions from high-resolution x-ray scattering. Phys Rev E 57:7014–7024
Petrache HI, Tristram-Nagle S, Nagle JF (1998b) Fluid phase structure of EPC and DMPC bilayers. Chem Phys Lipids 95:83–94
Pfeiffer H, Klose G, Heremans K (2013) Reorientation of hydration water during the thermotropic main phase transition of 1-palmitoyl-2-oleolyl-sn-glycero-3-phosphocholine (POPC) bilayers at low degrees of hydration. Chem Phys Lett 572:120–124
Piletic IR, Moilanen DE, Levinger NE, Fayer MD (2006) What nonlinear-IR experiments can tell you about water that the IR spectrum cannot. J Am Chem Soc 128:10366–10367
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 108:2027–2036
Pohle W, Selle C (1996) Fourier-transform infrared spectroscopic evidence for a novel lyotropic phase transition occurring in dioleoylphosphatidylethanolamine. Chem Phys Lipids 82:191–198
Pohle W, Selle C, Fritzsche H, Bohl M (1997) Comparative FTIR spectroscopic study upon the hydration of lecithins and cephalins. J Mol Struct 408–409:273–277
Pohle W, Selle C, Fritzsche H, Binder H (1998) Fourier transform infrared spectroscopy as a probe for the study of the hydration of lipid self assemblies. I. Methodology and general phenomena. Biospectroscopy 4:267–280
Pohle W, Selle C, Gauger DR, Brandenburg K (2001) Lyotropic phase transitions in phospholipids as evidenced by small-angle synchrotron X-ray scattering. J Biomol Struct Dyn 19:351–364
Rand RP, Fuller NL (1994) Structural dimensions and their changes in a reentrant hexagonal-lamellar transition of phospholipids. Biophys J 66:2127–2138
Rand RP, Parsegian VA (1989) Hydration forces between phospholipid bilayers. Biochim Biophys Acta Rev Biomembr 988:351–376
Rand RP, Fuller N, Parsegian VA, Rau DC (1988) Variation in hydration forces between neutral phospholipid bilayers: evidence for hydration attraction. Biochemistry 27:7711–7722
Rappolt M, Hickel A, Bringezu F, Lohner K (2003) Mechanism of the lamellar/inverse hexagonal phase transition examined by high resolution x-ray diffraction. Biophys J 84:3111–3122
Riemenschneider J, Holzmann J, Ludwig R (2008) Salt effects on the structure of water probed by attenuated total reflection infrared spectroscopy and molecular dynamics simulations. Chemphyschem 9:2731–2736
Róg T, Murzyn K, Milhaud J et al (2009) Water isotope effect on the phosphatidylcholine bilayer properties: a molecular dynamics simulation study. J Phys Chem B 113:2378–2387
Selle C, Pohle W (1998) Fourier transform infrared spectroscopy as a probe for the study of the hydration of lipid self-assemblies. II. Water binding versus phase transitions. Biospectroscopy 4:281–294
Selle C, Pohle W, Fritzsche H (1999) FTIR spectroscopic features of lyotropically induced phase transitions in phospholipid model membranes. J Mol Struct 480–481:401–405
Sheikh KH, Jarvis SP (2011) Crystalline hydration structure at the membrane-fluid interface of model lipid rafts indicates a highly reactive boundary region. J Am Chem Soc 133:18296–18303
Skinner JL, Auer BM, Lin YS (2009) Vibrational line shapes, spectral diffusion, and hydrogen bonding in liquid water. Adv Chem Phys 142:59–103
Sokołowska A, Kęcki Z (1986) Inter- and intra-molecular coupling and Fermi resonance in the Raman spectra of liquid water. J Raman Spectrosc 17:29–33
Sovago M, Campen RK, Wurpel GWH et al (2008) Vibrational response of hydrogen-bonded interfacial water is dominated by intramolecular coupling. Phys Rev Lett 100:173901
Stepniewski M, Bunker A, Pasenkiewicz-Gierula M et al (2010) Effects of the lipid bilayer phase state on the water membrane interface. J Phys Chem B 114:11784–11792
Štrancar J, Arsov Z (2008) Application of spin-labeling EPR and ATR-FTIR spectroscopies to the study of membrane heterogeneity. In: Leitmannova Liu A (ed) Advances in planar lipid bilayers and liposomes, vol 6. Elsevier, Amsterdam, pp 16–139
Tamm LK, Han X (2000) Viral fusion peptides: a tool set to disrupt and connect biological membranes. Biosci Rep 20:501–518
Tamm LK, Tatulian SA (1997) Infrared spectroscopy of proteins and peptides in lipid bilayers. Q Rev Biophys 30:365–429
Tayebi L, Ma Y, Vashaee D et al (2012) Long-range interlayer alignment of intralayer domains in stacked lipid bilayers. Nat Mater 11:1074–1080
Ter-Minassian-Saraga L, Okamura E, Umemura J, Takenaka T (1988) Fourier transform infrared-attenuated total reflection spectroscopy of hydration of dimyristoylphosphatidyl-choline multibilayers. Biochim Biophys Acta 946:417–423
Tielrooij KJ, Paparo D, Piatkowski L et al (2009) Dielectric relaxation dynamics of water in model membranes probed by terahertz spectroscopy. Biophys J 97:2484–2492
Tiwari S, Ando M, Hamaguchi H (2013) Investigation of organelle-specific intracellular water structures with Raman microspectroscopy. J Raman Spectrosc 44:167–169
Tristram-Nagle S, Liu Y, Legleiter J, Nagle JF (2002) Structure of gel phase DMPC determined by X-ray diffraction. Biophys J 83:3324–3335
Volkov VV, Palmer DJ, Righini R (2007a) Heterogeneity of water at the phospholipid membrane interface. J Phys Chem B 111:1377–1383
Volkov VV, Palmer DJ, Righini R (2007b) Distinct water species confined at the interface of a phospholipid membrane. Phys Rev Lett 99:078302
Wennerström H, Sparr E (2003) Thermodynamics of membrane lipid hydration. Pure Appl Chem 75:905–912
Wurpel GWH, Müller M (2006) Water confined by lipid bilayers: a multiplex CARS study. Chem Phys Lett 425:336–341
Zhang Z, Berkowitz ML (2009) Orientational dynamics of water in phospholipid bilayers with different hydration levels. J Phys Chem B 113:7676–7680
Zhong D, Pal SK, Zewail AH (2011) Biological water: a critique. Chem Phys Lett 503:1–11
Acknowledgments
The financial support from the state budget by the Slovenian Research Agency (program No. P1-0060) is acknowledged. The author appreciates collaboration or helpful discussions with Luca Quaroni, Michael Rappolt, Joze Grdadolnik, Primoz Ziherl and Rudolf Podgornik. The author also thanks Iztok Urbancic for carefully reading this manuscript.
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Arsov, Z. (2015). Long-Range Lipid-Water Interaction as Observed by ATR-FTIR Spectroscopy. In: Disalvo, E. (eds) Membrane Hydration. Subcellular Biochemistry, vol 71. Springer, Cham. https://doi.org/10.1007/978-3-319-19060-0_6
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