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Water-Hydrophobic Compound Interactions with the Microbial Cell

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Handbook of Hydrocarbon and Lipid Microbiology

Abstract:

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.

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Notes

  1. 1.

    Some of these interactions do not result in metabolic inhibition, for example those between the relatively non-polar enzyme and substrate, naphthalene dehydrogenase and naphthalene, (Kulakov et al., 2006) that give rise to a physiologically valuable response.

  2. 2.

    This said, a more rapid response may occur at a phenotypic level; for example the cis-trans unsaturated fatty-acid isomerase of Pseudomonas putida. This enzyme is expressed constitutively at all stages of the growth cycle but appears only to be active only when the cell is challenged by a stressor, such as toluene (Bernal et al., 2007; Junker and Ramos, 1999).

References

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Arakawa T, Timasheff SN (1985) The stabilization of proteins by osmolytes. Biophys J 47: 411–414.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Brown, AD (1990) Microbial Water Stress Physiology. Chichester, UK: John Wiley and Sons.

    Google Scholar 

  • Chandler D (2005) Interfaces and the driving force of hydrophobic assembly. Nature 437: 640–647.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Dill KA (1990) Dominant forces in protein folding. Biochemistry 29: 7133–7155.

    Article  PubMed  CAS  Google Scholar 

  • Dill KA, Flory PJ (1980) Interphases of chain molecules: monolayers and lipid bilayer membranes. PNAS 77: 3115–3119.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Eisenberg D, Kauzmann W (1969) The Structure and Properties of Water. London: Oxford University Press.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Fersht A (1985) Enzyme Structure and Mechanism, 2nd edn. New York: WH Freeman.

    Google Scholar 

  • Finney JL (2004) What’s so special about water? Philos Trans R Soc Lond B 359: 1145–1165.

    Article  CAS  Google Scholar 

  • Gill SJ, Wadsö I (1976) An equation of state describing hydrophobic interactions. Proc Natl Acad Sci USA 73: 2955–2958.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • Hallsworth, JE (1998) Ethanol-induced water stress in yeast. J Ferment Bioeng 85: 125–137.

    Article  CAS  Google Scholar 

  • Hallsworth JE, Heim S, Timmis KN (2003) Chaotropic solutes cause water stress in Pseudomonas putida. Environ Microbiol 5: 1270–1280.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Head IM, Jones DM, Roling WFM (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4: 173–182.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Höfinger S, Zerbetto F (2005) Simple models for hydrophobic hydration. Chem Soc Rev 34: 1012–1020.

    Article  PubMed  Google Scholar 

  • Inoue A, Horikoshi K (1991) Estimation of solvent-tolerance of bacteria by the solvent parameter log P. J Ferment Bioeng 71: 194–196.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kim IS, Foght JM, Gray MR (2002) Selective transport and accumulation of alkanes by Rhodococcus erythropolis S+14He. Biotechnol Bioeng 80: 650–659.

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi H, Uematsu K, Hirayama H, Horihoshi K (2000) Novel toluene elimination system in a toluene-tolerant microorganism. J Bacteriol 182: 6451–6455.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Lomize AL, Pogozheva ID, Mosberg HI (2004) Quantification of helix-helix binding affinities in micelles and lipid bilayers. Protein Sci 13: 2600–2612.

    Article  PubMed  CAS  Google Scholar 

  • Lünsdorf H, Erb RW, Abraham WR, Timmis KN (2000) “Clay hutches”: a novel interaction between bacteria and clay minerals. Environ Microbiol 2: 161–168.

    Article  PubMed  Google Scholar 

  • Marqusee JA, Dill KA (1986) Solute partitioning into chain molecule interphases: monolayers, bilayer membranes, and micelles. J Chem Phys 85: 434–444.

    Article  CAS  Google Scholar 

  • Marrink SJ, Berendsen HJC (1994) Simulation of water transport through a lipid membrane. J Phys Chem 98: 4155–4168.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Norman KE, Nymeyer H (2006) Indole localization in lipid membranes revealed by molecular simulation. Biophys J 91: 2049–2054.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Peters R, Peters J, Tews KH, Bähr W (1974) A microfluorimetric study of translational diffusion in erythrocyte membranes Biochim Biophys Acta 367: 282–294.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Schrödinger E (1944) What is Life? The Physical Aspect of the Living Cell. Cambridge, MA: Cambridge University Press.

    Google Scholar 

  • Sikkema J, De Bont JAM, Poolman B (1994) Interactions of cyclic hydrocarbons with biological membranes. J Biol Chem 269: 8022–8028.

    PubMed  CAS  Google Scholar 

  • Sikkema J, De Bont JAM, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59: 201–222.

    PubMed  CAS  Google Scholar 

  • Strevett KA, Chen G (2003) Microbial surface thermodynamics and applications. Res Microbiol 154: 329–335.

    Article  PubMed  CAS  Google Scholar 

  • Tanford C (1973) The Hydrophobic Effect: Formation of Micelles and Biological Membranes. New York: Wiley.

    Google Scholar 

  • Tanford C (1978) The hydrophobic effect and the organization of living matter. Science 200: 1012–1018.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Timmis KN (2002) Pseudomonas putida: a cosmopolitan par excellence. Environ Microbiol 4: 779–781.

    Article  PubMed  Google Scholar 

  • APJ, Trinci JE (eds.) Ryley (1984) Mode of Action of Antifungal Agents. Cambridge, MA: Cambridge University Press.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Washabaugh MW, Collins KD (1986) The systematic characterization by aqueous column chromatography of solutes which affect protein structure. J Biol Chem 261: 12477–12485.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Zhang J, Lazaridis T (2006) Calculating the free energy of association of transmembrane helices. Biophys J 91: 1710–1723.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Zielkiewicz J (2008) Two-particle entropy and structural ordering in liquid water. J Phys Chem B 112: 7810–7815.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

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).

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McCammick, E.M., Gomase, V.S., McGenity, T.J., Timson, D.J., Hallsworth, J.E. (2010). Water-Hydrophobic Compound Interactions with the Microbial Cell. In: Timmis, K.N. (eds) Handbook of Hydrocarbon and Lipid Microbiology. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-77587-4_99

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