Skip to main content

Surface Properties and Cellular Energetics of Bacteria in Response to the Presence of Hydrocarbons

  • Living reference work entry
  • First Online:
Cellular Ecophysiology of Microbe

Abstract

Many toxic hydrocarbons that are present as environmental pollutants are potential substrates for bacteria; other, very hydrophobic hydrocarbons exhibit extremely low water solubility and are poorly bioavailable. The development of specific adaptive mechanisms to the toxicity as well as the low bioavailability of these substrates allows many bacteria to cope with such challenges. Strategies of bacteria to increase the accessibility of these compounds are modifications of their cell surfaces or the release of biosurfactants. Both “strategies” aim at an increased accessibility of the compounds, either by the reduction of surface tension or by allowing a direct hydrophobic-hydrophobic interaction between cell surface and the substrates. The toxicity of hydrocarbons is mainly caused by their permeabilizing effect on the cytoplasmic membranes leading also to a loss of ATP and a decrease in the proton gradient. Bacteria are able to modify their cellular energetics in order to adapt to the presence of toxic hydrocarbons by activating their electron transport phosphorylation systems allowing homeostasis of ATP level and energy charge in the presence of the toxic conditions, however, at the price of a reduced growth yield.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Institutional subscriptions

References

  • Arias-Barrau E, Sandoval A, Olivera ER, Luengo JM, Naharro G (2005) A two-component hydroxylase involved in the assimilation of 3-hydroxyphenyl acetate in Pseudomonas putida. J Biol Chem 280:26435

    Article  CAS  PubMed  Google Scholar 

  • Atkinson DE, Walton GM (1967) Adenosine triphosphate conservation in metabolic regulation. Rat liver citrate cleavage enzyme. J Biol Chem 342:3239–3241

    Google Scholar 

  • Baldi F et al (1999) Adhesion of Acinetobacter venetianus to diesel fuel droplets studied with in situ electrochemical and molecular probes. Appl Environ Microbiol 65:2041–2048

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baldi F et al (2003) Envelope glycosylation determined by lectins in microscopy sections of Acinetobacter venetianus induced by diesel fuel. Res Microbiol 154:417–424

    Article  CAS  PubMed  Google Scholar 

  • Baumgarten T, Heipieper HJ (2016) Outer membrane vesicle secretion: from envelope stress to biofilm formation. In: de Bruijn FJ (ed) Stress and environmental control of gene expression in bacteria. Wiley-Blackwell, New York, pp 1322–1327

    Chapter  Google Scholar 

  • Baumgarten T et al (2012a) Membrane vesicle formation as a multiple-stress response mechanism enhances Pseudomonas putida DOT-T1E cell surface hydrophobicity and biofilm formation. Appl Environ Microbiol 78:6217–6224. doi:10.1128/aem.01525-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baumgarten T et al (2012b) Alkanols and chlorophenols cause different physiological adaptive responses on the level of cell surface properties and membrane vesicle formation in Pseudomonas putida DOT-T1E. Appl Microbiol Biotechnol 93:837–845. doi:10.1007/s00253-011-3442-9

    Article  CAS  PubMed  Google Scholar 

  • Chapman AG, Fall L, Atkinson DE (1971) Adenylate energy charge in Escherichia coli during growth and starvation. J Bacteriol 108:1072–1086

    CAS  PubMed  PubMed Central  Google Scholar 

  • de Bont JAM (1998) Solvent-tolerant bacteria in biocatalysis. Trends Biotechnol 16:493–499

    Article  Google Scholar 

  • de Carvalho CCCR, Wick LY, Heipieper HJ (2009) Cell wall adaptations of planktonic and biofilm Rhodococcus erythropolis cells to growth on C5 to C16 n-alkane hydrocarbons. Appl Microbiol Biotechnol 82:311–320

    Article  CAS  PubMed  Google Scholar 

  • de Carvalho CCCR, Fischer MA, Kirsten S, Wurz B, Wick LY, Heipieper HJ (2016) Adaptive response of Rhodococcus opacus PWD4 to salt and phenolic stress on the level of mycolic acids. AMB Express 6:8. doi:10.1186/s13568-016-0241-9

    Article  Google Scholar 

  • Dorobantu LS, Bhattacharjee S, Foght JM, Gray MR (2008) Atomic force microscopy measurement of heterogeneity in bacterial surface hydrophobicity. Langmuir 24:4944–4951

    Article  CAS  PubMed  Google Scholar 

  • Heipieper HJ, Keweloh H, Rehm HJ (1991) Influence of phenols on growth and membrane permeability of free and immobilized Escherichia coli. Appl Environ Microbiol 57:1213–1217

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heipieper HJ, Diefenbach R, Keweloh H (1992) Conversion of cis-unsaturated fatty acids to trans, a possible mechanism for the protection of phenol-degrading Pseudomonas putida P8 from substrate toxicity. Appl Environ Microbiol 58:1847–1852

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heipieper HJ, Weber FJ, Sikkema J, Keweloh H, de Bont JAM (1994) Mechanisms behind resistance of whole cells to toxic organic solvents. Trends Biotechnol 12:409–415

    Article  CAS  Google Scholar 

  • Heipieper HJ, Neumann G, Cornelissen S, Meinhardt F (2007) Solvent-tolerant bacteria for biotransformations in two-phase fermentation systems. Appl Microbiol Biotechnol 74:961–973

    Article  CAS  PubMed  Google Scholar 

  • Hori K, Watanabe H, Ishii S, Tanji Y, Unno H (2008) Monolayer adsorption of a “bald” mutant of the highly adhesive and hydrophobic bacterium Acinetobacter sp strain tol 5 to a hydrocarbon surface. Appl Environ Microbiol 74:2511–2517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Isken S, Derks A, Wolffs PFG, de Bont JAM (1999) Effect of organic solvents on the yield of solvent-tolerant Pseudomonas putida S12. Appl Environ Microbiol 65:2631–2635

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kadurugamuwa JL, Beveridge TJ (1995) Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J Bacteriol 177:3998–4008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kadurugamuwa JL, Lam JS, Beveridge TJ (1993) Interaction of gentamicin with the A band and B band lipopolysaccharides of Pseudomonas aeruginosa and its possible lethal effect. Antimicrob Agents Chemother 37:715–721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang ZW, Yeung A, Foght JM, Gray MR (2008) Mechanical properties of hexadecane-water interfaces with adsorbed hydrophobic bacteria. Colloids Surf B: Biointerfaces 62:273–279

    Article  CAS  PubMed  Google Scholar 

  • Kayser A, Weber J, Hecht V, Rinas U (2005) Metabolic flux analysis of Escherichia coli in glucose-limited continuous culture. I. Growth-rate-dependent metabolic efficiency at steady state. Microbiology 151:693–706

    Article  CAS  PubMed  Google Scholar 

  • Kelly NM, MacDonald MH, Martin N, Nicas T, Hancock REW (1990) Comparison of the outer membrane protein and lipopolysaccharide profiles of mucoid and nonmucoid Pseudomonas aeruginosa. J Clin Microbiol 28:2017–2021

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kulp A, Kuehn MJ (2010) Biological functions and biogenesis of secreted bacterial outer membrane vesicles. In: Gotteseman S, Harwood CS (eds) Annual review of microbiology. Annual Reviews, Palo Alto, pp 163–184

    Google Scholar 

  • Lambert PA, Hammond SM (1973) Potassium fluxes, first indication of membrane damage in micro-organisms. Biochem Biophys Res Commun 54:796–799

    Article  CAS  PubMed  Google Scholar 

  • Lang S, Philp JC (1998) Surface-active lipids in rhodococci. Anton Leeuw Int J Gen Mol Microbiol 74:59–70

    Article  CAS  Google Scholar 

  • Loffhagen N, Babel W (1985) pH-linked control of energy charge in Acetobacter methanolicus sp. MB 70. J Basic Microbiol 25:575–580

    Article  CAS  Google Scholar 

  • Lundin A, Hasenson M, Persson J, Pousette A (1986) Estimation of biomass in growing cell lines by adenosine triphosphate assay. Methods Enzymol 133:27–44

    Article  CAS  PubMed  Google Scholar 

  • Makin SA, Beveridge TJ (1996a) The influence of A-band and B-band lipopolysaccharide on the surface characteristics and adhesion of Pseudomonas aeruginosa to surfaces. Microbiology 142:299–307

    Article  CAS  PubMed  Google Scholar 

  • Makin SA, Beveridge TJ (1996b) Pseudomonas aeruginosa PAO1 ceases to express serotype-specific lipopolysaccharide at 45°C. J Bacteriol 178:3350–3352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mashburn-Warren LM, Whiteley M (2006) Special delivery: vesicle trafficking in prokaryotes. Mol Microbiol 61:839–846

    Article  CAS  PubMed  Google Scholar 

  • Misic C, Giani M, Povero P, Polimene L, Fabiano M (2005) Relationships between organic carbon and microbial components in a Tyrrhenian area (Isola del Giglio) affected by mucilages. Sci Total Environ 353:350–359

    Article  CAS  PubMed  Google Scholar 

  • Navon-Venezia S et al (1995) Alasan, a new bioemulsifier from Acinetobacter radioresistens. Appl Environ Microbiol 61:3240–3244

    CAS  PubMed  PubMed Central  Google Scholar 

  • Neumann G et al (2006) Energetics and surface properties of Pseudomonas putida DOT-T1E in a two-phase fermentation system with 1-decanol as second phase. Appl Environ Microbiol 72:4232–4238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Norman RS, Frontera-Suau R, Morris PJ (2002) Variability in Pseudomonas aeruginosa lipopolysaccharide expression during crude oil degradation. Appl Environ Microbiol 68:5096–5103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osterreicher-Ravid D, Ron EZ, Rosenberg E (2000) Horizontal transfer of an exopolymer complex from one bacterial species to another. Environ Microbiol 2:366–372

    Article  CAS  PubMed  Google Scholar 

  • Pines O, Gutnick D (1986) Role for emulsan in growth of Acinetobacter calcoaceticus RAG-1 on crude oil. Appl Environ Microbiol 51:661–663

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pinkart HC, Wolfram JW, Rogers R, White DC (1996) Cell envelope changes in solvent-tolerant and solvent-sensitive Pseudomonas putida strains following exposure to o-xylene. Appl Environ Microbiol 62:1129–1132

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ron EZ, Rosenberg E (2002) Biosurfactants and oil bioremediation. Curr Opin Biotechnol 13:249–252

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg M (2006) Microbial adhesion to hydrocarbons: twenty-five years of doing MATH. FEMS Microbiol Lett 262:129–134

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg E, Ron EZ (1997) Bioemulsans: microbial polymeric emulsifiers. Curr Opin Biotechnol 8:313–316

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg E, Ron EZ (1999) High- and low-molecular-mass microbial surfactants. Appl Microbiol Biotechnol 52:154–162

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg M, Rosenberg E (1981) Role of adherence in growth of Acinetobacter calcoaceticus RAG-1 on hexadecane. J Bacteriol 148:51–57

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sabra W, Lunsdorf H, Zeng AP (2003) Alterations in the formation of lipopolysaccharide and membrane vesicles on the surface of Pseudomonas aeruginosa PAO1 under oxygen stress conditions. Microbiology 149:2789–2795

    Article  CAS  PubMed  Google Scholar 

  • Schwechheimer C, Kuehn MJ (2015) Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions. Nat Rev Microbiol 13:605–619. doi:10.1038/nrmicro3525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Segura A et al (2004) Enzymatic activation of the cis-trans isomerase and transcriptional regulation of efflux pumps in solvent tolerance in Pseudomonas putida. In: Ramos JL (ed) The pseudomonads. Kluwer Press, Dordrecht, pp 479–508

    Chapter  Google Scholar 

  • Segura A et al (2005) Proteomic analysis reveals the participation of energy- and stress-related proteins in the response of Pseudomonas putida DOT-T1E to toluene. J Bacteriol 187:5937–5945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tashiro Y, Ichikawa S, Nakajima-Kambe T, Uchiyama H, Nomura N (2010a) Pseudomonas quinolone signal affects membrane vesicle production in not only Gram-negative but also Gram-positive bacteria. Microbes Environ 25:120–125. doi:10.1264/jsme2.ME09182

    Article  PubMed  Google Scholar 

  • Tashiro Y et al (2010b) Variation of physiochemical properties and cell association activity of membrane vesicles with growth phase in Pseudomonas aeruginosa. Appl Environ Microbiol 76:3732–3739. doi:10.1128/aem.02794-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tashiro Y, Uchiyama H, Nomura N (2012) Multifunctional membrane vesicles in Pseudomonas aeruginosa. Environ Microbiol 14:1349–1362. doi:10.1111/j.1462-2920.2011.02632.x

    Article  CAS  PubMed  Google Scholar 

  • Toren A, Orr E, Paitan Y, Ron EZ, Rosenberg E (2002) The active component of the bioemulsifier alasan from Acinetobacter radioresistens KA53 is an OmpA-like protein. J Bacteriol 184:165–170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tran QH, Unden G (1998) Changes in the proton potential and the cellular energetics of Escherichia coli during growth by aerobic and anaerobic respiration or by fermentation. Eur J Biochem 251:538

    Article  CAS  PubMed  Google Scholar 

  • Van Loosdrecht MCM, Lyklema J, Norde W, Schraa G, Zehnder AJB (1987a) Electrophoretic mobility and hydrophobicity as a measure to predict the initial steps of bacterial adhesion. Appl Environ Microbiol 53:1898–1901

    CAS  PubMed  PubMed Central  Google Scholar 

  • Van Loosdrecht MCM, Lyklema J, Norde W, Schraa G, Zehnder AJB (1987b) The role of bacterial cell wall hydrophobicity in adhesion. Appl Environ Microbiol 53:1893–1897

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vaneechoutte M et al (1999) Oil-degrading Acinetobacter strain RAG-1 and strains described as ‘Acinetobacter venetianus sp nov.’ belong to the same genomic species. Res Microbiol 150:69–73

    Article  CAS  PubMed  Google Scholar 

  • Volkers RJM, de Jong AL, Hulst AG, van Baar BLM, de Bont JAM, Wery J (2006) Chemostat-based proteomic analysis of toluene-affected Pseudomonas putida S12. Environ Microbiol 8:1674–1679

    Article  CAS  PubMed  Google Scholar 

  • Walzer G, Rosenberg E, Ron EZ (2006) The Acinetobacter outer membrane protein A (OmpA) is a secreted emulsifier. Environ Microbiol 8:1026–1032

    Article  CAS  PubMed  Google Scholar 

  • Wick LY, de Munain AR, Springael D, Harms H (2002a) Responses of Mycobacterium sp LB501T to the low bioavailability of solid anthracene. Appl Microbiol Biotechnol 58:378–385

    Article  CAS  PubMed  Google Scholar 

  • Wick LY, Wattiau P, Harms H (2002b) Influence of the growth substrate on the mycolic acid profiles of mycobacteria. Environ Microbiol 4:612–616

    Article  CAS  PubMed  Google Scholar 

  • Wick LY, Pasche N, Bernasconi SM, Pelz O, Harms H (2003) Characterization of multiple-substrate utilization by anthracene-degrading Mycobacterium frederiksbergense LB501T. Appl Environ Microbiol 69:6133–6142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hermann J. Heipieper .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this entry

Cite this entry

Heipieper, H.J., Pepi, M., Baumgarten, T., Eberlein, C. (2017). Surface Properties and Cellular Energetics of Bacteria in Response to the Presence of Hydrocarbons. In: Krell, T. (eds) Cellular Ecophysiology of Microbe. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-20796-4_50-1

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-20796-4_50-1

  • Received:

  • Accepted:

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-20796-4

  • Online ISBN: 978-3-319-20796-4

  • eBook Packages: Springer Reference Biomedicine and Life SciencesReference Module Biomedical and Life Sciences

Publish with us

Policies and ethics