Water-Hydrophobic Compound Interactions with the Microbial Cell

  • E. M. McCammick
  • V. S. Gomase
  • T. J. McGenity
  • D. J. Timson
  • J. E. Hallsworth


The structural interactions of biological macromolecules, their biochemical activities and, ultimately, the metabolic function of cellular systems are dependent upon weak inter- and intra-molecular forces such as hydrogen bonds, Van der Waals forces, and the hydrophobic effect. Water molecules, and those of hydrophobic substances such as hydrocarbons, can take part in and/or modify these interactions and thereby determine the operational and structural stability of the microbial cell and its macromolecular systems. We explain how the cytosol, plasma membrane and the extracellular solution form a material and energetic continuum; and discuss the behavior of hydrophobic substances of extracellular origin as they migrate into the plasma membrane and into the cell's interior. The adverse effects of substances with a log P octanol-water ≥2, that partition into the hydrophobic domains of biological macromolecules, are discussed in relation to microbial cell function; and we speculate whether the cellular stress that they induce is symmetrical or asymmetrical in nature. In the context of the microbial environment, we take a situational-functional approach to consider how hydrophobic stressors interact with the microbial cell, and what types of evasion tactics microbes can employ to minimize their inhibitory activities. Finally, we discuss the ecological implications of hydrocarbon-induced cellular stress for microbial systems.



We are grateful for thought-provoking discussions with Giuseppe Albano (Edinburgh University, UK), Prashanth Bhaganna and Kalpa D. Gupta (Queen’s University Belfast, Northern Ireland), Ananda Hillis (University of Ulster, UK), Allen Y. Mswaka (University of Harare, Zimbabwe), Mary Palfreyman (Outwood Grange College, UK), Harald J. Ruijssenaars (TNO Quality of Life, The Netherlands), Kenneth N. Timmis (HZI, Germany) and Graham J. C. Underwood (University of Essex, UK). Work on this article was funded by the Kluyver Centre for Genomics of Industrial Fermentation (The Netherlands), EU Fifth-Framework contract QLK3-CT-2002-01933 (LINDANE), Biotechnology and Biological Sciences Research Council (BBSRC, UK) and Natural Environment Research Council (NERC, UK).


  1. Abbasnezhad H, Gray MR, Foght JM (2008) Two different mechanisms for adhesion of Gram-negative bacterium, Pseudomonas fluorescens LP6a, to an oil-water interface. Colloids Surf B Biointerfaces 62: 36–41.PubMedCrossRefGoogle Scholar
  2. Arakawa T, Timasheff SN (1985) The stabilization of proteins by osmolytes. Biophys J 47: 411–414.PubMedCrossRefGoogle Scholar
  3. Bassolino-Klimas D, Alper HE, Stouch TR (1994) Mechanism of solute diffusion through lipid bilayer membranes by molecular dynamics simulation. J Am Chem Soc 117: 4118–4129.CrossRefGoogle Scholar
  4. Battin TJ, Sloan WT, Kjelleberg S, Daims H, Head IM, Curtis TP, Eberl L (2007) Microbial landscapes: new paths to biofilm research. Nat Rev Microbiol 5: 76–81.PubMedCrossRefGoogle Scholar
  5. Bernal P, Segura A, Ramos JL (2007) Compensatory role of the cis-trans-isomerase and cardiolipin synthase in the membrane fluidity of Pseudomonas putida DOT-T1E. Environ Microbiol 9: 1658–1664.PubMedCrossRefGoogle Scholar
  6. Brown, AD (1990) Microbial Water Stress Physiology. Chichester, UK: John Wiley and Sons.Google Scholar
  7. Chandler D (2005) Interfaces and the driving force of hydrophobic assembly. Nature 437: 640–647.PubMedCrossRefGoogle Scholar
  8. Delaney JC, Henderson PT, Helquist SA, Morales JC, Essigmann JM, Kool ET (2003) High fidelity in vivo replication of DNA base shape mimics without Watson-Crick hydrogen bonds. PNAS 100: 4469–4473.PubMedCrossRefGoogle Scholar
  9. Dill KA (1990) Dominant forces in protein folding. Biochemistry 29: 7133–7155.PubMedCrossRefGoogle Scholar
  10. Dill KA, Flory PJ (1980) Interphases of chain molecules: monolayers and lipid bilayer membranes. PNAS 77: 3115–3119.PubMedCrossRefGoogle Scholar
  11. Dohnal V, Costas M, Carrillo-Nava E, Hovorka S (2001) Non-polar solutes in water and in aqueous solutions of protein denaturants. Modeling of solution and transfer process. Biophys Chem 90: 183–202.PubMedCrossRefGoogle Scholar
  12. Dominguez-Cuevas P, Gonzalez-Pastor JE, Marques S, Ramos JL, de Lorenzo V (2006) Transcriptional tradeoff between metabolic and stress-response programs in Pseudomonas putida KT2440 cells exposed to toluene. J Biol Chem 281: 11981–11991.PubMedCrossRefGoogle Scholar
  13. Duda VI, Danilevich VN, Suzina NE, Shorokhova AP, Dmitriev VV, Mokhova ON, Akimov VN (2004) Changes in the fine structure of microbial cells induced by chaotropic salts. Microbiology 73: 341–349.CrossRefGoogle Scholar
  14. Efremov RG, Chugunov AO, Pyrkov TV, Priestle JP, Arseniev AS, Jacoby E (2007) Molecular lipophilicity in protein modeling and drug design. Curr Med Chem 14: 393–415.PubMedCrossRefGoogle Scholar
  15. Eisenberg D, Kauzmann W (1969) The Structure and Properties of Water. London: Oxford University Press.Google Scholar
  16. Erilov DA, Bartucci R, Guzzi R, Shubin AA, Maryasov AG, Marsh D, Dzuba SA, Sportelli L (2005) Water concentration profiles in membranes measured by ESEEM of spin-labeled lipids. J Phys Chem B 109: 12003–12013.PubMedCrossRefGoogle Scholar
  17. Ferro FontÃn C, Chirife J (1981) The evaluation of water activity in aqueous-solutions from freezing-point depression measurements J Food Technol 16: 21–30.Google Scholar
  18. Fersht A (1985) Enzyme Structure and Mechanism, 2nd edn. New York: WH Freeman.Google Scholar
  19. Finney JL (2004) What’s so special about water? Philos Trans R Soc Lond B 359: 1145–1165.CrossRefGoogle Scholar
  20. Gill SJ, Wadsö I (1976) An equation of state describing hydrophobic interactions. Proc Natl Acad Sci USA 73: 2955–2958.PubMedCrossRefGoogle Scholar
  21. Gratkowski H, Lear JD, DeGrado WF (2001) Polar side chains drive the association of model transmembrane peptides. Proc Natl Acad Sci USA 98: 880–885.PubMedCrossRefGoogle Scholar
  22. Gupta A, Chauhan A, Kopelevich DI (2008) Molecular modeling of surfactant covered oil-water interfaces: dynamics, microstructure, and barrier for mass transport. J Chem Phys 128: 234709.PubMedCrossRefGoogle Scholar
  23. Hallsworth JE, Magan N (1994) Effect of carbohydrate type and concentration on polyols and trehalose in conidia of three entomopathogenic fungi. Microbiology-SGM 140: 2705–2713.Google Scholar
  24. Hallsworth, JE (1998) Ethanol-induced water stress in yeast. J Ferment Bioeng 85: 125–137.CrossRefGoogle Scholar
  25. Hallsworth JE, Heim S, Timmis KN (2003) Chaotropic solutes cause water stress in Pseudomonas putida. Environ Microbiol 5: 1270–1280.PubMedCrossRefGoogle Scholar
  26. Hallsworth JE, Yakimov MM, Golyshin PN, Gillion JLM, D’Auria G, Alves FL, Lo Cono V, Genovese M, McKew BA, Hayes SL, Harris G, Giuliano L, Timmis KN, McGenity TJ (2007) Limits of life in MgCl2-containing environments: chaotropicity defines the window. Environ Microbiol 9: 803–813.CrossRefGoogle Scholar
  27. Head IM, Jones DM, Roling WFM (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4: 173–182.PubMedCrossRefGoogle Scholar
  28. Heipieper HJ, Neumann G, Cornelissen S, Friedhelm M (2007) Solvent-tolerant bacteria for biotransformations in two-phase fermentation systems. Appl Microbiol Biotechnol 74: 961–973.PubMedCrossRefGoogle Scholar
  29. Höfinger S, Zerbetto F (2005) Simple models for hydrophobic hydration. Chem Soc Rev 34: 1012–1020.PubMedCrossRefGoogle Scholar
  30. Inoue A, Horikoshi K (1991) Estimation of solvent-tolerance of bacteria by the solvent parameter log P. J Ferment Bioeng 71: 194–196.CrossRefGoogle Scholar
  31. Junker F, Ramos JL (1999) Involvement of the cis/trans isomerase Cti in solvent resistance of Pseudomonas putida DOT-T1E. J Bacteriol 181: 5693–5700.PubMedGoogle Scholar
  32. Kashangura C, Hallsworth JE, Mswaka AY (2006) Phenotypic diversity amongst strains of Pleurotus sajor-caju: implications for cultivation in arid environments. Mycol Res 110: 312–317.PubMedCrossRefGoogle Scholar
  33. Kieboom J, Dennis JJ, de Bont JAM, Zylstra GJ (1998) Identification and molecular characterization of an efflux pump involved in Pseudomonas putida S12 solvent tolerance. J Biol Chem 273: 85–91.PubMedCrossRefGoogle Scholar
  34. Kim IS, Foght JM, Gray MR (2002) Selective transport and accumulation of alkanes by Rhodococcus erythropolis S+14He. Biotechnol Bioeng 80: 650–659.PubMedCrossRefGoogle Scholar
  35. Kobayashi H, Uematsu K, Hirayama H, Horihoshi K (2000) Novel toluene elimination system in a toluene-tolerant microorganism. J Bacteriol 182: 6451–6455.PubMedCrossRefGoogle Scholar
  36. Kulakov LA, Allen CRC, Lipscomba DA, Larkin M (2006) Cloning and characterization of a novel cis-napthalene dihydrodiol dehydrogenase gene (narB) from Rhodococcus sp. NCIMB12038. FEMS Microbiol Lett 182: 327–331.Google Scholar
  37. Kushner DJ (1978) Life at high salt and solute concentrations: halophilic bacteria. In Microbial Life in Extreme Environments. DJ Kushner (ed.). London: Academic Press, pp. 318–368.Google Scholar
  38. Kwon JH, Liljestrand HM, Katz LE (2006) Partitioning of moderately hydrophobic endocrine disruptors between water and synthetic membrane vesicles. Environ Toxicol Chem 25: 1984–1992.PubMedCrossRefGoogle Scholar
  39. Lear JD, Gratkowski H, Adamian L, Liang J, DeGrado WF (2003) Position-dependence of stabilizing polar interactions of asparagine in transmembrane helical bundles. Biochemistry 42: 6400–6407.PubMedCrossRefGoogle Scholar
  40. Liu Y, Li J (2008) Role of Pseudomonas aeruginosa biofilm in the initial adhesion, growth and detachment of Escherichia coli in porous media. Environ Sci Technol 42: 443–449.PubMedCrossRefGoogle Scholar
  41. Lomize AL, Pogozheva ID, Mosberg HI (2004) Quantification of helix-helix binding affinities in micelles and lipid bilayers. Protein Sci 13: 2600–2612.PubMedCrossRefGoogle Scholar
  42. Lünsdorf H, Erb RW, Abraham WR, Timmis KN (2000) “Clay hutches”: a novel interaction between bacteria and clay minerals. Environ Microbiol 2: 161–168.PubMedCrossRefGoogle Scholar
  43. Marqusee JA, Dill KA (1986) Solute partitioning into chain molecule interphases: monolayers, bilayer membranes, and micelles. J Chem Phys 85: 434–444.CrossRefGoogle Scholar
  44. Marrink SJ, Berendsen HJC (1994) Simulation of water transport through a lipid membrane. J Phys Chem 98: 4155–4168.CrossRefGoogle Scholar
  45. Marrink SJ, Berkowitz M, Berendsen HJC (1993) Molecular dynamics simulation of a membrane/water interface: the ordering of water and its relation to the hydration force. Langmuir 9: 3122–3131.CrossRefGoogle Scholar
  46. Matubayasi N, Shinoda W, Nakahara M (2008) Free-energy analysis of the molecular binding into lipid membrane with the method of energy representation. J Chem Phys 128: 195107.PubMedCrossRefGoogle Scholar
  47. Norman KE, Nymeyer H (2006) Indole localization in lipid membranes revealed by molecular simulation. Biophys J 91: 2049–2054.CrossRefGoogle Scholar
  48. North B, Cristian L, Fu Stowell X, Lear JD, Saven JG, Degrado WF (2006) Characterization of a membrane protein folding motif, the Ser zipper, using designed peptides. J Mol Biol 359: 930–939.PubMedCrossRefGoogle Scholar
  49. Peters R, Peters J, Tews KH, Bähr W (1974) A microfluorimetric study of translational diffusion in erythrocyte membranes Biochim Biophys Acta 367: 282–294.PubMedCrossRefGoogle Scholar
  50. Ramos JL, Duque E, Gallegos MT, Godoy P, Ramos-Gonzalez MI, Rojas A, Teran W, Segura A (2002) Mechanisms of solvent tolerance in gram-negative bacteria. Annu Rev Microbiol 56: 743–768.PubMedCrossRefGoogle Scholar
  51. Ritter M, Ravasio A, Jakab M, Chwatal S, Fürst J, Laich A, Gschwentner M, Signorelli S, Burtscher C, Eichmüller S, Paulmichl M (2003) Cell swelling stimulates cytosol to membrane transposition of ICln. J Biol Chem 278: 50163–50174.PubMedCrossRefGoogle Scholar
  52. Schrödinger E (1944) What is Life? The Physical Aspect of the Living Cell. Cambridge, MA: Cambridge University Press.Google Scholar
  53. Sikkema J, De Bont JAM, Poolman B (1994) Interactions of cyclic hydrocarbons with biological membranes. J Biol Chem 269: 8022–8028.PubMedGoogle Scholar
  54. Sikkema J, De Bont JAM, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59: 201–222.PubMedGoogle Scholar
  55. Strevett KA, Chen G (2003) Microbial surface thermodynamics and applications. Res Microbiol 154: 329–335.PubMedCrossRefGoogle Scholar
  56. Tanford C (1973) The Hydrophobic Effect: Formation of Micelles and Biological Membranes. New York: Wiley.Google Scholar
  57. Tanford C (1978) The hydrophobic effect and the organization of living matter. Science 200: 1012–1018.PubMedCrossRefGoogle Scholar
  58. Thomas JC, Berger F, Jacquier M, Bernillon D, Baud-Grasset F, Truffaut N, Normand P, Vogel TM, Simonet P (1996) Isolation and characterization of a novel gamma-Hexachlorocyclohexane-degrading bacterium. J Bacteriol 178: 6049–6055.PubMedGoogle Scholar
  59. Thompson SEM, Taylor AR, Brownlee C, Callow ME, Callow JA (2008) The role of nitric oxide in diatom adhesion in relation to substratum properties. J Phycol 44: 967–976.Google Scholar
  60. Timmis KN (2002) Pseudomonas putida: a cosmopolitan par excellence. Environ Microbiol 4: 779–781.PubMedCrossRefGoogle Scholar
  61. APJ, Trinci JE (eds.) Ryley (1984) Mode of Action of Antifungal Agents. Cambridge, MA: Cambridge University Press.Google Scholar
  62. Usami R, Fukushima T, Mizuki T, Inoue A, Yoshida Y, Horikoshi K (2003) Organic solvent tolerance of halophilic Archaea. Biosci Biotechnol Biochem 67: 1809–1812.PubMedCrossRefGoogle Scholar
  63. Vermuë M, Sikkema J, Verheula A, Bakker R, Tramper J (1993) Toxicity of homologos series of organic-solvents for the gram-positive bacteria Arthrobacter and Nocardia sp. and the gram-negative bacteria Acinetobacter and Pseudomonas sp. Biotechnol Bioeng 42: 747–758.PubMedCrossRefGoogle Scholar
  64. Vijayan K, Discher DE, Lal J, Janmey P, Goulian M (2005) Interactions of membrane-active peptides with thick, neutral, nonzwitterionic bilayers. J Phys Chem B 109: 14356–14364.PubMedCrossRefGoogle Scholar
  65. Washabaugh MW, Collins KD (1986) The systematic characterization by aqueous column chromatography of solutes which affect protein structure. J Biol Chem 261: 12477–12485.PubMedGoogle Scholar
  66. Wagoner J, Baker NA (2004) Solvation forces on biomolecular structures: a comparison of explicit solvent and Poisson-Boltzmann models, J Comput Chem 13: 1623–1629.CrossRefGoogle Scholar
  67. Wiener MC, White SH (1992) Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of x-ray and neutron diffraction data. III. Complete structure . Biophys J 61: 434–447.PubMedCrossRefGoogle Scholar
  68. Xiang TX, Anderson BD (1994) Molecular distribution in interphases: statistical mechanical theory combined with molecular dynamics simulation of a model lipid bilayer. Biophys J 66: 561–573.PubMedCrossRefGoogle Scholar
  69. Yakimov M, Golyshin PN, Lang S, Moore ERB, Abraham WR, Lünsodrf H, Timmis KN (1998) Alcanivorax borkumensis gen. nov., sp. nov., a new, hydrocarbon-degrading and surfactant-producing marine bacterium. Int J Syst Bacteriol 48: 339–348.PubMedGoogle Scholar
  70. Yoshidome T, Kinoshita M, Hirota S, Baden N, Terazima M (2008) Thermodynamics of apoplastocyanin folding: comparison between experimental and theoretical results. J Chem Phys 128: 225104.PubMedCrossRefGoogle Scholar
  71. Zhang J, Lazaridis T (2006) Calculating the free energy of association of transmembrane helices. Biophys J 91: 1710–1723.PubMedCrossRefGoogle Scholar
  72. Zhang Y, Johansson JS (2005) A calorimetric study on the binding of six general anaesthetics to the hydrophobic core of a model protein. Biophys Chem 113: 169–174.PubMedCrossRefGoogle Scholar
  73. Zielkiewicz J (2008) Two-particle entropy and structural ordering in liquid water. J Phys Chem B 112: 7810–7815.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  • E. M. McCammick
    • 1
  • V. S. Gomase
    • 2
  • T. J. McGenity
    • 3
  • D. J. Timson
    • 1
  • J. E. Hallsworth
    • 1
  1. 1.School of Biological Sciences, MBCQueen’s University BelfastBelfastNorthern Ireland
  2. 2.Department of BioinformaticsPadmashree Dr. D. Y. Patil UniversityCBD BelapurIndia
  3. 3.Department of Biological SciencesUniversity of EssexColchesterUK

Personalised recommendations