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Biodegradation and surfactant-mediated biodegradation of diesel fuel by 218 microbial consortia are not correlated to cell surface hydrophobicity

  • Applied Microbial and Cell Physiology
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Abstract

In this study, we elucidated the role of cell surface hydrophobicity (microbial adhesion to hydrocarbons method, MATH) and the effect of anionic rhamnolipids and nonionic Triton X-100 surfactants on biodegradation of diesel fuel employing 218 microbial consortia isolated from petroleum-contaminated soils. Applied enrichment procedure with floating diesel fuel as a sole carbon source in liquid cultures resulted in consortia of varying biodegradation potential and diametrically different cell surface properties, suggesting that cell surface hydrophobicity is a conserved parameter. Surprisingly, no correlations between cell surface hydrophobicity and biodegradation of diesel fuel were found. Nevertheless, both surfactants altered cell surface hydrophobicity of the consortia in similar manner: increased for the hydrophilic and decreased for the hydrophobic cultures. In addition to this, the surfactants exhibited similar influence on diesel fuel biodegradation: Increase was observed for initially slow-degrading cultures and the opposite for fast degraders. This indicates that in the surfactant-mediated biodegradation, effectiveness of surfactants depends on the specification of microorganisms and not on the type of surfactant. In contrary to what was previously reported for pure strains, cell surface hydrophobicity, as determined by MATH, is not a good descriptor of biodegrading potential for mixed cultures.

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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

    CAS  PubMed  Google Scholar 

  • Abraham WR, Nogales B, Golyshin PN, Pieper DH, Timmis KN (2002) Polychlorinated biphenyl-degrading microbial communities in soils and sediments. Curr Opin Microbiol 5:246–253

    Article  CAS  PubMed  Google Scholar 

  • Baldi F, Ivošević N, Minacci A, Pepi M, Fani R, Svetličić V, Žutić V (1999) Adhesion of Acinetobacter venetianus to diesel fuel droplet studied with in situ electrochemical and molecular probes. Appl Environ Microbiol 65:2041–2048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bastiaens L, Springael D, Wattiau P, Harms H, deWachter R, Verachtert H, Diels L (2000) Isolation of adherent polycyclic aromatic hydrocarbon (PAH)-degrading bacteria using PAH-sorbing carriers. Appl Environ Microbiol 66:1834–1843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouchez-Naïtali M, Rakatozafy H, Marchal R, Leveau JY, Vandecasteele JP (1999) Diversity of bacterial strains degrading hexadecane in relation to the mode of substrate uptake. J Appl Microbiol 86:421–428

    Article  PubMed  Google Scholar 

  • Breugelmans P, D'Huys P-J, De Mot R, Springael D (2007) Characterization of novel linuron-mineralizing bacterial consortia enriched from long-term linuron-treated agricultural soils. FEMS Microbiol Ecol 62:374–385

    Article  CAS  PubMed  Google Scholar 

  • Cavalca L, Rao MA, Bernasconi S, Kolombo M, Andreoni V, Gianfreda L (2008) Biodegradation of phenanthrene and analysis of degrading cultures in the presence of a model organo-mineral matrix and of a simulated NAPL phase. Biodegradation 19:1–13

    Article  CAS  PubMed  Google Scholar 

  • Chen P, Pickard MA, Gray MR (2000) Surfactant inhibition of bacterial growth on solid anthracene. Biodegradation 11:341–347

    Article  CAS  PubMed  Google Scholar 

  • Chrzanowski Ł, Bielicka-Daszkiewicz K, Owsianiak M, Aurich A, Kaczorek E, Olszanowski A (2008) Phenol and n-alkanes (C12 and C16) utilization: influence on yeast cell surface hydrophobicity. World J Microb Biot 24:1943–1949

    Article  CAS  Google Scholar 

  • Chrzanowski Ł, Stasiewicz M, Owsianiak M, Szulc A, Piotrowska-Cyplik A, Olejnik-Schmidt A, Wyrwas B (2009a) Biodegradation of diesel fuel by a microbial consortium in the presence of 1-alkoxymethyl-2-methyl-5-hydroxypyridinium chloride homologues. Biodegradation . doi:https://doi.org/10.1007/s10532-009-9253-3

    Article  CAS  PubMed  Google Scholar 

  • Chrzanowski Ł, Owsianiak M, Wyrwas B, Aurich A, Szulc A, Olszanowski A (2009b) Adsorption of sodium dodecylbenzenesulphonate (SDBS) on Candida maltosa EH 15 strain: influence on cell surface hydrophobicity and n-alkanes biodegradation. Water Air Soil Pollut 196:345–353

    Article  CAS  Google Scholar 

  • Chrzanowski Ł, Wick LY, Meulenkamp R, Kaestner M, Heipieper HJ (2009c) Rhamnolipid biosurfactants decrease the toxicity of chlorinated phenols to Pseudomonas putida DOT-T1E. Lett Appl Microbiol 48:756–762

    CAS  PubMed  Google Scholar 

  • Churchill PF, Dudley RJ, Churchill SA (1995) Surfactant-enhanced bioremediation. Waste Manage 15:371–377

    Article  CAS  Google Scholar 

  • Daffonchio D, Thaveesri J, Verstraete W (1995) Contact angle measurement and cell hydrophobicity of granular sludge from upflow anaerobic sludge bed reactors. Appl Environ Microbiol 61:3676–3680

    Article  CAS  PubMed  PubMed Central  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 

  • Endo S, Schmidt T (2006) Prediction of partitioning between complex organic mixtures and water: application of polyparameter linear free energy relationships. Environ Sci Technol 40:536–545

    Article  CAS  PubMed  Google Scholar 

  • Friedrich M, Grosser RJ, Kern EA, Inskeep WP, Ward DM (2000) Effect of model sorptive phases on phenanthrene biodegradation: molecular analysis of enrichments and isolates suggests selection based on bioavailability. Appl Environ Microbiol 66:2703–2710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghazali FM, Rahman RNZA, Salleh AB, Basri M (2004) Biodegradation of hydrocarbons in soil by microbial consortium. Int Biodeterior Biodegrad 54:61–67

    Article  CAS  Google Scholar 

  • Geertsema-Doornbusch GI, van der Mei HC, Busscher HJ (1993) Microbial cell surface hydrophobicity: the involvement of electrostatic interactions in microbial adhesion to hydrocarbons (MATH). J Microbiol Methods 28:61–68

    Article  Google Scholar 

  • Goulter RM, Gentle IR, Dykes GA (2009) Issues in determining factors influencing bacterial attachment: a review using the attachment of Escherichia coli to abiotic surfaces as an example. Lett Appl Microbiol . doi:https://doi.org/10.1111/j.1472-765X.2009.02591.x

    Article  CAS  PubMed  Google Scholar 

  • Grosser RJ, Friedrich M, Kern EA, Inskeep WP, Ward DM (2000) Effect of model sorptive phases on phenanthrene biodegradation: different enrichment conditions influence bioavailability and selection of phenanthrene-degrading isolates. Appl Environ Microbiol 66:2695–2702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • ISO 9377-2:2000 (2000) Water quality—determination of hydrocarbon oil index—part 2: method using solvent extraction and gas chromatography. ISO, Geneva

    Google Scholar 

  • Ito H, Hosokawa R, Morikawa M, Okuyama H (2008) A turbine oil-degrading bacterial consortium from soils of oil fields and its characteristics. Int Biodeterior Biodegrad 61:223–232

    Article  CAS  Google Scholar 

  • Jacques RJS, Okeke BC, Bento FM, Teixeira AS, Peralba MCR, Camargo FAO (2008) Microbial consortium bioaugmentation of a polycyclic aromatic hydrocarbons contaminated soil. Bioresour Technol 99:2637–2643

    Article  CAS  PubMed  Google Scholar 

  • Johnsen AR, Karlson U (2004) Evaluation of bacterial strategies to promote the bioavailability of polycyclic aromatic hydrocarbons. Appl Microbiol Biotechnol 63:452–459

    Article  CAS  PubMed  Google Scholar 

  • Kaczorek E, Chrzanowski Ł, Pijanowska A, Olszanowski A (2008) Yeast and bacteria cell hydrophobicity and hydrocarbon biodegradation in the presence of natural surfactants: rhamnolipides and saponins. Bioresour Technol 99:4285–4291

    Article  CAS  PubMed  Google Scholar 

  • Neu TR (1996) Significance of bacterial surface-active compounds in interaction of bacteria with interfaces. Microbiol Rev 60:151–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Obuekwe CO, Al-Jadi ZK, Al-Saleh E (2007a) Sequential hydrophobic partitioning of cells of Pesudomonas aeruginosa gives rise to variants of increasing cell-surface hydrophobicity. FEMS Microbiol Lett 270:214–219

    Article  CAS  PubMed  Google Scholar 

  • Obuekwe CO, Al-Jadi ZK, Al-Saleh E (2007b) Insight into heterogeneity in cell-surface hydrophobicity and ability to degrade hydrocarbons among cells of two hydrocarbon-degrading bacterial populations. Can J Microbiol 53:252–260

    Article  CAS  PubMed  Google Scholar 

  • Obuekwe CO, Al-Jadi ZK, Al-Saleh E (2008) Comparative hydrocarbon utilization by hydrophobic and hydrophilic variants of Pseudomonas aeruginosa. J Appl Microbiol 105:1876–1887

    Article  CAS  PubMed  Google Scholar 

  • Obuekwe CO, Al-Jadi ZK, Al-Saleh ES (2009) Hydrocarbon degradation in relation to cell-surface hydrophobicity among bacterial hydrocarbon degraders from petroleum-contaminated Kuwait desert environment. Int Biodeterior Biodegrad 63:273–279

    Article  CAS  Google Scholar 

  • Olivera NL, Nievas ML, Lozada M, del Prado G, Dionisi HM, Siñeriz F (2009) Isolation and characterization of biosurfactant-producing Alcanivorax strains: hydrocarbon accession strategies and alkane hydroxylase gene analysis. Res Microbiol 160:19–26

    Article  CAS  PubMed  Google Scholar 

  • Ortega-Calvo J-J, Alexander M (1994) Roles of bacterial attachment and spontaneous partitioning in the biodegradation of naphthalene initially present in nonaqueous-phase liquids. Appl Environ Microbiol 60:2643–2646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Owsianiak M, Chrzanowski Ł, Szulc A, Staniewski J, Olszanowski A, Olejnik-Schmidt A, Heipieper HJ (2009) Biodegradation of diesel/biodiesel blends by a consortium of hydrocarbon degraders: effect of the type of blend and the addition of biosurfactants. Bioresour Technol 100:1497–1500

    Article  CAS  PubMed  Google Scholar 

  • Paria S (2008) Surfactant-enhanced remediation of organic contaminated soil and water. Adv Colloid Interface Sci 138:24–58

    Article  CAS  PubMed  Google Scholar 

  • Pelz O, Tesar M, Wittach R-M, Moore ERB, Timmis KN, Abraham W-R (1999) Towards elucidation of microbial community metabolic pathways: unravelling the network of carbon sharing in a pollutant-degrading bacterial consortium by immunocapture and isotopic ratio mass spectrometry. Environ Microbiol 1:167–174

    Article  CAS  PubMed  Google Scholar 

  • Pembrey RS, Marshall KC, Schneider RP (1999) Cell surface analysis techniques: what do cell preparation protocols do to cell surface properties? Appl Environ Microbiol 65:2877–2894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pepi M, Minacci A, Di Cello F, Baldi F, Fani R (2003) Long-term analysis of diesel fuel consumption in a co-culture of Acinetobacter venetianus, Pseudomonas putida and Alcaligenes faecalis. Antonie Van Leeuwenhoek 83:3–9

    Article  CAS  PubMed  Google Scholar 

  • Pompilio A, Piccolomini R, Picciani C, D’Antonio D, Savini V, Di Bonaventura G (2008) Factors associated with adherence to and biofilm formation on polystyrene by Stenotrophomonas maltophilia: the role of cell surface hydrophobicity and motility. FEMS Microbiol Lett 287:41–47

    Article  CAS  PubMed  Google Scholar 

  • Potter TL, Simmons KE (1998) Composition of petroleum mixtures. In: Total petroleum hydrocarbon criteria working group series, vol 2. Amherst Scientific, Amherst, MA

  • Ron EZ, Rosenberg E (2001) Natural roles of biosurfactants. Environ Microbiol 3:229–236

    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 M, Gutnick D, Rosenberg E (1980) Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol Lett 9:29–33

    Article  CAS  Google Scholar 

  • Rosenberg M, Gutnick D, Rosenberg E (1983) Adherence of bacteria to hydrocarbons. In: Zajic JE, Cooper DG, Jack TR, Kosaric N (eds) Microbial enhanced oil recovery. Pen Well, Tulsa, OK, pp 114–123

    Google Scholar 

  • Sjögren M, Li H, Rannug U, Westerholm R (1995) A multivariate statistical analysis of chemical composition and physical characteristics of ten diesel fuels. Fuel 74:983–989

    Article  Google Scholar 

  • Stelmack PL, Gray MR, Pickard MA (1999) Bacterial adhesion to soil contaminants in the presence of surfactants. Appl Environ Microbiol 65:163–168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sutherland IW (2002) Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147:3–9

    Article  Google Scholar 

  • Thomassin-Lacroix EJM, Eriksson M, Reimer KJ, Mohn WW (2002) Biostimulation and bioaugmentation for on-site treatment of weathered diesel fuel in Arctic soil. Appl Microbiol Biotechnol 59:551–556

    Article  CAS  PubMed  Google Scholar 

  • Trigo A, Valencia A, Cases I (2009) Systemic approaches to biodegradation. FEMS Microbiol Rev 33:98–108

    Article  CAS  PubMed  Google Scholar 

  • Watkinson R, Morgan P (1990) Physiology of aliphatic hydrocarbon-degrading microorganisms. Biodegradation 1:79–92

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Van Hamme JD, Ward OP (2001) Physical and metabolic interactions of Pseudomonas sp. strain JA5–B45 and Rhodococcus sp. strain F9–D79 during growth on crude oil and effect of a chemical surfactant on them. Appl Environ Microbiol 67:4874–4879

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Viñas M, Grifoll M, Sabaté J, Solanas AM (2002) Biodegradation of a crude oil by three microbial consortia of different origins and metabolic capabilities. J Ind Microbiol Biotechnol 28:252–260

    Article  PubMed  Google Scholar 

  • Volkering F, Breure AM, Rulkens (1998) Microbiological aspects of surfactant use for biological soil remediation. Biodegradation 8:401–417

    Article  CAS  Google Scholar 

  • Zhang Y, Miller RM (1994) Effect of a Pseudomonas rhamnolipid biosurfactant on cell hydrophobicity and biodegradation of octadecane. Appl Environ Microbiol 60:2101–2106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong H, Zeng GM, Yuan XZ, Fu HY, Huang GH, Ren FY (2007) Adsorption of dirhamnolipid on four microorganisms and the effect on cell surface hydrophobicity. Appl Microbiol Biotechnol 77:447–455

    Article  CAS  PubMed  Google Scholar 

  • Zhong H, Zeng GM, Liu JX, Xu XM, Yuan XZ, Fu HY, Huang GH, Liu ZF, Ding Y (2008) Adsorption of monorhamnolipid and dirhamnolipid on two Pseudomonas aeruginosa strains and the effect on cell surface hydrophobicity. Appl Microbiol Biotechnol 79:671–677

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Isolation, identification of microorganisms, and hydrophobicity studies were performed in the framework of the Grant No. N N305 035434 Polish Ministry of Science and Higher Education, years 2008–2010. We are thankful to Arnaud Dechesne for the comments on an earlier version of the manuscript.

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Correspondence to Łukasz Chrzanowski.

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Owsianiak, M., Szulc, A., Chrzanowski, Ł. et al. Biodegradation and surfactant-mediated biodegradation of diesel fuel by 218 microbial consortia are not correlated to cell surface hydrophobicity. Appl Microbiol Biotechnol 84, 545–553 (2009). https://doi.org/10.1007/s00253-009-2040-6

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  • DOI: https://doi.org/10.1007/s00253-009-2040-6

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