Abstract
The hydration of selected amino acids, alanine, glycine, proline, valine, isoleucine and phenylalanine, has been studied in aqueous solutions by means of FTIR spectra of HDO isotopically diluted in H2O. The difference spectra procedure and the chemometric method have been applied to remove the contribution of bulk water and thus to separate the spectra of solute-affected HDO. To support interpretation of obtained spectral results, molecular dynamics simulations of amino acids were performed. The structural-energetic characteristic of these solute-affected water molecules shows that, on average, water affected by amino acids forms stronger and shorter H-bonds than those in pure water. Differences in the influence of amino acids on water structure have been noticed. The effect of the hydrophobic side chain of an amino acid on the solvent interactions seems to be enhanced because of the specific cooperative coupling of water strong H-bond chain, connecting the carboxyl and amino groups, with the clathrate-like H-bond network surrounding the hydrocarbon side chain. The parameter derived from the spectral data, which corresponds to the contributions of the population of weak hydrogen bonds of water molecules which have been substituted by the stronger ones in the hydration sphere of amino acids, correlated well with the amino acid hydrophobicity indexes.
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References
Anjum F, Rishi V, Ahmad F (2000) Compatibility of osmolytes with Gibbs energy of stabilization of proteins. BBA Protein Struct M 1476:75–84. doi:10.1016/s0167-4838(99)00215-0
Arakawa T, Timasheff SN (1985) The stabilization of proteins by osmolytes. Biophys J 47:411–414
Arakawa T, Tsumoto K, Kita Y, Chang B, Ejima D (2007) Biotechnology applications of amino acids in protein purification and formulations. Amino Acids 33:587–605. doi:10.1007/s00726-007-0506-3
Badger RM, Bauer SH (1937) Spectroscopic studies of the hydrogen bond. II. The shift of the O–H vibrational frequency in the formation of the hydrogen bond. J Chem Phys 5:839–851
Balabin RM (2010) The first step in glycine solvation: the glycine–water complex. J Phys Chem B 114:15075–15078. doi:10.1021/jp107539z
Bennion BJ, Daggett V (2004) Counteraction of urea-induced protein denaturation by trimethylamine N-oxide: a chemical chaperone at atomic resolution. Proc Natl Acad Sci USA 101:6433–6438. doi:10.1073/pnas.0308633101
Berendsen HJC, Postma JPM, Vangunsteren WF, Dinola A, Haak JR (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81:3684–3690. doi:10.1063/1.448118
Berglund B, Lindgren J, Tegenfeldt J (1978) O–H and O–D stretching vibrations in isotopically dilute hdo molecules in some solid hydrates. J Mol Struct 43:169–177. doi:10.1016/0022-2860(78)80004-0
Bergstrom PA, Lindgren J, Kristiansson O (1991) An IR study of the hydration of CLO4-, NO3 −, Br−, Cl−, and SO4 2− anions in aqueous solution. J Phys Chem 95:8575–8580. doi:10.1021/j100175a031
Bodor N, Gabanyi Z, Wong CK (1989) A new method for the estimation of partition coefficient. J Am Chem Soc 111:3783–3786. doi:10.1021/ja00193a003
Bolen DW, Baskakov IV (2001) The osmophobic effect: natural selection of a thermodynamic force in protein folding. J Mol Biol 310:955–963. doi:10.1006/jmbi.2001.4819
Bratos S, Leicknam JC, Pommeret S (2009) Relation between the OH stretching frequency and the OO distance in time-resolved infrared spectroscopy of hydrogen bonding. Chem Phys 359:53–57. doi:10.1016/j.chemphys.2009.03.016
Bruździak P, Panuszko A, Stangret J (2010) Chemometric determination of solute-affected solvent vibrational spectra as a superior way of information extraction on solute solvation phenomena. Vib Spectrosc 54:65–71. doi:10.1016/j.vibspec.2010.06.006
Bruździak P, Rakowska PW, Stangret J (2012) Chemometric method of spectra analysis leading to isolation of lysozyme and CtDNA spectra affected by osmolytes. Appl Spectrosc 66:1302–1310. doi:10.1366/11-06581
Bruździak P, Panuszko A, Stangret J (2013) Influence of osmolytes on protein and water structure: a step to understanding the mechanism of protein stabilization. J Phys Chem B 117:11502–11508
Burakowski A, Gliński J (2010) Hydration of amino acids from ultrasonic measurements. J Phys Chem B 114:12157–12161. doi:10.1021/jp105255b
Campo MG (2006) Molecular dynamics simulation of glycine zwitterion in aqueous solution. J Chem Phys 125:114511. doi:10.1063/1.2352756
Chaudhari A, Sahu PK, Lee SL (2004) Microsolvation effect on alanine: a many-body interaction study using ab initio method. Theochem J Mol Struc 683:115–119. doi:10.1016/j.theochem.2004.06.024
Chothia C (1976) Nature of accessible and buried surfaces in proteins. J Mol Biol 105:1–14. doi:10.1016/0022-2836(76)90191-1
Cid H, Bunster M, Canales M, Gazitua F (1992) Hydrophobicity and structural classes in proteins. Protein Eng 5:373–375. doi:10.1093/protein/5.5.373
Cornette JL, Cease KB, Margalit H, Spouge JL, Berzofsky JA, Delisi C (1987) Hydrophobicity scales and computational techniques for detecting amphipathic structures in proteins. J Mol Biol 195:659–685. doi:10.1016/0022-2836(87)90189-6
Daggett V (2006) Protein folding-simulation. Chem Rev 106:1898–1916. doi:10.1021/cr0404242
Darden T, York D, Pedersen L (1993) Particle mesh ewald: an N log(N) method for ewald sums in large systems. J Chem Phys 98:10089–10092. doi:10.1063/1.464397
Eriksson PO, Lindblom G, Burnell EE, Tiddy GJT (1988) Influence of organic solutes on the self-diffusion of water as studied by nuclear magnetic-resonance spectroscopy. J Chem Soc Faraday Trans I 84:3129–3139. doi:10.1039/f19888403129
Finney JL (1996) Hydration processes in biological and macromolecular systems. Faraday Discuss 103:1–18. doi:10.1039/fd9960300001
Finney JL, Soper AK (1994) Solvent structure and perturbations in solutions of chemical and biological importance. Chem Soc Rev 23:1–10. doi:10.1039/cs9942300001
Galamba N (2013) Water’s Structure around hydrophobic solutes and the iceberg model. J Phys Chem B 117:2153–2159. doi:10.1021/jp310649n
Gavezzotti A (1983) The calculation of molecular volumes and the use of volume analysis in the investigation of structured media and of solid-state organic-reactivity. J Am Chem Soc 105:5220–5225. doi:10.1021/ja00354a007
Glew DN, Rath NS (1971) H2O, HDO, and CH3OH infrared spectra and correlation with solvent basicity and hydrogen bonding. Can J Chem 49:837. doi:10.1139/v71-142
Gojlo E, Śmiechowski M, Stangret J (2005) The common effect of hydrophobic and electrophilic types of hydration dependent on protonation in the sec-butylamine/HCl/H2O system studied by FTIR spectroscopy. J Mol Struct 744:809–814. doi:10.1016/j.molstruc.2004.11.005
Gojlo E, Gampe T, Krakowiak J, Stangret J (2007) Hydration of aprotic donor solvents studied by means of FTIR spectroscopy. J Phys Chem A 111:1827–1834. doi:10.1021/jp065599p
Gojlo E, Śmiechowski M, Panuszko A, Stangret J (2009) Hydration of carboxylate anions: infrared spectroscopy of aqueous solutions. J Phys Chem B 113:8128–8136. doi:10.1021/jp811346x
Head-Gordon T (1995) Is water structure around hydrophobic groups clathrate-like? Proc Natl Acad Sci USA 92:8308–8312. doi:10.1073/pnas.92.18.8308
Hecht D, Tadesse L, Walters L (1993) Correlating hydration shell structure with amino acid hydrophobicity. J Am Chem Soc 115:3336–3337. doi:10.1021/ja00061a045
Hernandez B, Pfluger F, Nsangou M, Ghomi M (2009) Vibrational analysis of amino acids and short peptides in hydrated media. IV. Amino acids with hydrophobic side chains: l-Alanine, l-Valine, and L-Isoleucine. J Phys Chem B 113:3169–3178. doi:10.1021/jp809204d
Hess B, Kutzner C, van der Spoel D, Lindahl E (2008) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Comput 4:435–447. doi:10.1021/ct700301q
Hessa T, Kim H, Bihlmaier K, Lundin C, Boekel J, Andersson H, Nilsson I, White SH, von Heijne G (2005) Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433:377–381. doi:10.1038/nature03216
Ide M, Maeda Y, Kitano H (1997) Effect of hydrophobicity of amino acids on the structure of water. J Phys Chem B 101:7022–7026. doi:10.1021/jp971334m
Jamal S, Poddar NK, Singh LR, Dar TA, Rishi V, Ahmad F (2009) Relationship between functional activity and protein stability in the presence of all classes of stabilizing osmolytes. FEBS J 276:6024–6032. doi:10.1111/j.1742-4658.2009.07317.x
Kumar S, Rai AK, Singh VB, Rai SB (2005) Vibrational spectrum of glycine molecule. Spectrochim Acta 61:2741–2746. doi:10.1016/j.saa.2004.09.029
Kumar R, Schmidt JR, Skinner JL (2007) Hydrogen bonding definitions and dynamics in liquid water. J Chem Phys 126:204107. doi:10.1063/1.2742385
Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132. doi:10.1016/0022-2836(82)90515-0
Liu YF, Bolen DW (1995) The peptide backbone plays a dominant role in protein stabilization by naturally-occurring osmolytes. Biochemistry 34:12884–12891. doi:10.1021/bi00039a051
McLain SE, Soper AK, Terry AE, Watts A (2007) Structure and hydration of l-proline in aqueous solutions. J Phys Chem B 111:4568–4580. doi:10.1021/jp068340f
McMullan R, Jeffrey GA (1959) Hydrates of the tetra N-butyl and tetra I-amyl quaternary ammonium salts. J Chem Phys 31:1231–1234. doi:10.1063/1.1730574
McMullan RK, Bonamico M, Jeffrey GA (1963) Polyhedral clathrate hydrates. V. Structure of tetra-N-butyl ammonium fluoride hydrate. J Chem Phys 39:3295–3310. doi:10.1063/1.1734193
Michaux C, Wouters J, Perpete EA, Jacquemin D (2009) Ab initio investigation of the hydration of deprotonated amino acids. J Am Soc Mass Spectr 20:632–638. doi:10.1016/j.jasms.2008.11.025
Mullin JM, Gordon MS (2009) Alanine: then there was water. J Phys Chem B 113:8657–8669. doi:10.1021/jp901459y
Niehues G, Heyden M, Schmidt DA, Havenith M (2011) Exploring hydrophobicity by THz absorption spectroscopy of solvated amino acids. Faraday Discuss 150:193–207. doi:10.1039/c0fd00007h
Olsztynska S, Komorowska M, Vrielynck L, Dupuy N (2001) Vibrational spectroscopic study of l-phenylalanine: effect of pH. Appl Spectrosc 55:901–907. doi:10.1366/0003702011952703
Oostenbrink C, Soares TA, van der Vegt NFA, van Gunsteren WF (2005) Validation of the 53A6 GROMOS force field. Eur Biophys J Biophy 34:273–284. doi:10.1007/s00249-004-0448-6
Pacios LF (2001) Distinct molecular surfaces and hydrophobicity of amino acid residues in proteins. J Chem Inf Comp Sci 41:1427–1435. doi:10.1021/ci010369n
Panuszko A, Gojlo E, Zielkiewicz J, Śmiechowski M, Krakowiak J, Stangret J (2008) Hydration of simple amides. FTIR spectra of HDO and theoretical studies. J Phys Chem B 112:2483–2493. doi:10.1021/jp7099509
Panuszko A, Bruździak P, Zielkiewicz J, Wyrzykowski D, Stangret J (2009) Effects of urea and trimethylamine-N-oxide on the properties of water and the secondary structure of hen egg white lysozyme. J Phys Chem B 113:14797–14809. doi:10.1021/jp904001m
Panuszko A, Śmiechowski M, Stangret J (2011) Fourier transform infrared spectroscopic and theoretical study of water interactions with glycine and its N-methylated derivatives. J Chem Phys 134:115104. doi:10.1063/1.3567202
Panuszko A, Wojciechowski M, Bruździak P, Rakowska PW, Stangret J (2012) Characteristics of hydration water around hen egg lysozyme as the protein model in aqueous solution. FTIR spectroscopy and molecular dynamics simulation. Phys Chem Chem Phys 14:15765–15773. doi:10.1039/c2cp42229h
Pieniazek PA, Stangret J (2005) Hydration of tetraethylammonium tetrafluoroborate derived from FTIR spectroscopy. Vib Spectrosc 39:81–87. doi:10.1016/j.vibspec.2004.11.004
Praprotnik M, Janezic D, Mavri J (2004) Temperature dependence of water vibrational spectrum: a molecular dynamics simulation study. J Phys Chem A 108:11056–11062. doi:10.1021/jp046158d
Shiraki K, Kudou M, Fujiwara S, Imanaka T, Takagi M (2002) Biophysical effect of amino acids on the prevention of protein aggregation. J Biochem 132:591–595
Shirts MR, Pande VS (2005) Solvation free energies of amino acid side chain analogs for common molecular mechanics water models. J Chem Phys 122:134508. doi:10.1063/1.1877132
Śmiechowski M, Stangret J (2007) Molecular picture of hydroxide anion hydration in aqueous solutions studied by FT-IR ATR spectroscopy. J Mol Struct 834:239–248. doi:10.1016/j.molstruc.2006.09.040
Śmiechowski M, Stangret J (2008) ATR FT-IR H2O spectra of acidic aqueous solutions. Insights about proton hydration. J Mol Struct 878:104–115. doi:10.1016/j.molstruc.2007.08.001
Śmiechowski M, Stangret J (2010) Vibrational spectroscopy of semiheavy water (HDO) as a probe of solute hydration. Pure Appl Chem 82:1869–1887. doi:10.1351/pac-con-09-10-14
Soper AK, Castner EW, Luzar A (2003) Impact of urea on water structure: a clue to its properties as a denaturant? Biophys Chem 105:649–666. doi:10.1016/s0301-4622(03)00095-4
Stangret J (1988) Solute-affected vibrational-spectra of water in Ca(ClO4)2 aqueous-solutions. Spectrosc Lett 21:369–381. doi:10.1080/00387018808082314
Stangret J, Gampe T (1999) Hydration sphere of tetrabutylammonium cation. FTIR studies of HDO spectra. J Phys Chem B 103:3778–3783. doi:10.1021/jp983199z
Stangret J, Gampe T (2005) Hydration of tetrahydrofuran derived from FTIR spectroscopy. J Mol Struct 734:183–190. doi:10.1016/j.molstruc.2004.09.021
Sun J, Niehues G, Forbert H, Decka D, Schwaab G, Marx D, Havenith M (2014) Understanding thz spectra of aqueous solutions: glycine in light and heavy water. J Am Chem Soc 136:5031–5038. doi:10.1021/ja4129857
Taneja S, Ahmad F (1994) Increased thermal-stability of proteins in the presence of amino acids. Biochem J 303:147–153
Timasheff SN (2002) Protein-solvent preferential interactions, protein hydration, and the modulation of biochemical reactions by solvent components. Proc Natl Acad Sci USA 99:9721–9726. doi:10.1073/pnas.122225399
Troitzsch RZ, Martyna GJ, McLain SE, Soper AK, Crain J (2007) Structure of aqueous proline via parallel tempering molecular dynamics and neutron diffraction. J Phys Chem B 111:8210–8222. doi:10.1021/jp0714973
Turner J, Soper AK (1994) The effect of apolar solutes on water-structure—alcohols and tetraalkylammonium ions. J Chem Phys 101:6116–6125. doi:10.1063/1.467327
van der Spoel D, Lindahl E, Hess B, van Buuren AR, Apol E, Meulenhoff PJ, Tieleman DP, Sijbers ALTM, Feenstra KA, van Drunen R et al. (2010) Gromacs User Manual version 4.5.4, www.gromacs.org
Wang AJ, Bolen DW (1996) Effect of proline on lactate dehydrogenase activity: testing the generality and scope of the compatibility paradigm. Biophys J 71:2117–2122
Wang AJ, Bolen DW (1997) A naturally occurring protective system in urea-rich cells: mechanism of osmolyte protection of proteins against urea denaturation. Biochemistry 36:9101–9108. doi:10.1021/bi970247h
Wolfenden R, Andersson L, Cullis PM, Southgate CCB (1981) Affinities of amino-acid side-chains for solvent water. Biochemistry 20:849–855. doi:10.1021/bi00507a030
Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water-stress—evolution of osmolyte systems. Science 217:1214–1222. doi:10.1126/science.7112124
Zhu GY, Zhu X, Fan Q, Wan XL (2011) Raman spectra of amino acids and their aqueous solutions. Spectrochim Acta A 78:1187–1195. doi:10.1016/j.saa.2010.12.079
Acknowledgments
Thank are due to Dr. Piotr Bruździak for performance of chemometric analysis of FTIR spectra. This research was partially supported by the PL-Grid Infrastructure and TASK Computational Centre. This work was supported from the Republic of Poland scientific funds as a research project, within Grant No. 2013/11/B/NZ1/02258.
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Panuszko, A., Adamczak, B., Czub, J. et al. Hydration of amino acids: FTIR spectra and molecular dynamics studies. Amino Acids 47, 2265–2278 (2015). https://doi.org/10.1007/s00726-015-2005-2
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DOI: https://doi.org/10.1007/s00726-015-2005-2