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Taxonomic identification, phenanthrene uptake activity, and membrane lipid alterations of the PAH degrading Arthrobacter sp. strain Sphe3

  • Applied Microbial and Cell Physiology
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Abstract

This report describes phenanthrene uptake as well as the effect of phenanthrene on the membrane phospholipid and fatty acid composition in a newly isolated bacterial strain, Sphe3, that we taxonomically identified as Arthrobacter sp. Strain Sphe3 is able to utilize phenanthrene as a carbon source at high rates and appears to internalize phenanthrene with two mechanisms: a passive diffusion when cells are grown on glucose, and an inducible active transport system when cells are grown on phenanthrene as a sole carbon source. Active transport followed Michaelis-Menten kinetics, and it was amenable to inhibition by 2,4-dinitrophenol and sodium azide. Evidence provided here indicates that apart from inducing an active PAH uptake, the presence of phenanthrene elicits significant changes in membrane fluidity.

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References

  • Bateman JN, Speer BL, Feduik L, Hartline RA (1986) Naphthalene association and uptake in Pseudomonas putida. J Bacteriol 166:155–161

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    CAS  PubMed  Google Scholar 

  • Boggs JM (1984) Membrane fluidity. In: Kates M, Mansons LA (ed) Biomembranes vol. 12. Plenum, New York, pp 1–53

    Google Scholar 

  • Brown GR, Sutcliffe IC, Bendell D, Cummings SP (2000) The modification of the membrane of Oceanomonas baumannii T when subjected to both osmotic and organic solvent stress. FEMS Microbiol Lett 189:149–154

    CAS  PubMed  Google Scholar 

  • Bugg T, Foght JM, Pickard MA, Gray MR (2000) Uptake and active efflux of polycyclic aromatic hydrocarbons by a Pseudomonas fluorescens LP6a. Appl Environ Microbiol 66:5387–5392

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368

    CAS  Google Scholar 

  • Crocker FH, Fredrickson JK, White DC, Ringelberg DB, Balkwill DL (2000) Phylogenetic and physiological diversity of Arthrobacter strains isolated from unconsolidated subsurface sediments. Microbiology 146:1295–1310

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Fang J, Barcelona MJ, Alvarez PJJ (2000) Phospholipid compositional changes of five pseudomonad archetypes grown with and without toluene. Appl Microbiol Biotechnol 54:382–389

    CAS  PubMed  Google Scholar 

  • Grifoll M, Casellas M, Bayona JM, Solanas AM (1992) Isolation and characterization of a fluorene-degrading bacterium: identification of ring oxidation and ring fission products. Appl Environ Microbiol 58:2910–2917

    CAS  PubMed  PubMed Central  Google Scholar 

  • Habe H, Omori T (2003) Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 67:225–243

    CAS  PubMed  Google Scholar 

  • Hearn EM, Dennis JJ, Gray MR, Foght JM (2003) Identification and characterization of the emhABC efflux system for polycyclic aromatic hydrocarbons in Pseudomonas fluorescens cLP6a. J Bacteriol 185:6233–6240

    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, Meinhardt F, Segura A (2003) The cis-trans isomerase of unsaturated fatty acids in Pseudomonas and Vibrio: biochemistry, molecular biology and physiological function of a unique stress adaptive mechanism. FEMS Microbiol Lett 229:1–7

    CAS  PubMed  Google Scholar 

  • Ingram LO (1977) Changes in lipid composition of Escherichia coli resulting from growth with organic solvents and food additives. Appl Environ Microbiol 33:1233–1236

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jonhson JL (1994) Similarity analysis of DNAs. In: Gerhardt P, Murray RGE, Willis A, Krieg NR (ed) Methods for general and molecular bacteriology. ASM, Washington DC, pp 665–666

    Google Scholar 

  • Kanaly RA, Harayama S (2000) Biodegradation of high-molecular-weight PAHs by bacteria. J Bacteriol 182:2059–2067

    CAS  PubMed  PubMed Central  Google Scholar 

  • Keough KMW, Davis PJ (1984) Membrane fluidity. In: Kates M, Mansons LA (ed) Biomembranes, vol. 12. Plenum, New York, pp 55–97

    Google Scholar 

  • Kiyohara H, Kazutaka N, Yana K (1982) Rapid screen for bacteria degrading water-insoluble, solid hydrocarbons on agar plates. Appl Environ Microbiol 43:454–457

    CAS  PubMed  PubMed Central  Google Scholar 

  • Koukou AI, Tsoukatos D, Drainas C (1990) Effect of ethanol on the phospholipid and fatty acid content of Schizosaccharomyces pombe membranes. J Gen Microbiol 136:1271–1277

    CAS  PubMed  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    CAS  PubMed  Google Scholar 

  • Lowry OH, Rosenbrough NH, Farr AL, Randall RJ (1951) Protein measurement with Folin-phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Miyata N, Iwahori K, Foght JM, Gray MR (2004) saturable energy-depended uptake of phenanthrene in aqueous phase by Mycobacterium sp. strain RJGII-135. Appl Environ Microbiol 70:363–369

    CAS  PubMed  PubMed Central  Google Scholar 

  • Morrison WR, Smith LM (1964) Preparation of fatty acids methyl esters and dimethylacetals from lipids with boronfluoride-methanol. J Lip Res 5:600–608

    CAS  Google Scholar 

  • Mrozik A, Labuzek S, Piotrowska-Seget Z (2005) Changes in fatty acid composition in Pseudomonas putida and Pseudomonas stutzeri during naphthalene degradation. Microbiol Res 160:149–157

    CAS  PubMed  Google Scholar 

  • Mueller JG, Chapman PJ, Pritchard PH (1989) Creosote-contaminated sites. Environ Sci Technol 23:1197–1201

    CAS  Google Scholar 

  • Neumann G, Kabelitz N, Zehnsdorf A, Miltner A, Lippold H, Meyer D, Schmid A, Heipieper HJ (2005) Prediction of the adaptability of Pseudomonas putida DOT-T1E to a second phase of a solvent for economically sound two-phase biotransformations. Appl Environ Microbiol 71:6606–6612

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nielsen LE, Kavady DR, Rajagopal S, Drijber R, Nickerson KW (2005) Survey of extreme solvent tolerance in gram-positive cocci: membrane fatty acid changes in Staphylococcus haemolyticus grown in toluene. Appl Environ Microbiol 71:5171–5176

    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 

  • Samanta SK, Chakraborti AK, Jain RK (1999) Degradation of phenanthrene by different bacteria: evidence for novel transformation sequences involving the formation of 1-naphthol. Appl Microbiol Biotechnol 53:98–107

    CAS  PubMed  Google Scholar 

  • Segura A, Duque E, Mosqueda G, Ramos JL, Junker F (1999) Multiple responses of Gram-negative bacteria to organic solvents. Environ Microbiol 1:191–198

    CAS  PubMed  Google Scholar 

  • Seo JS, Keum YS, Hu Y, Lee SE, Li QX (2006) Phenanthrene degradation in Arthrobacter sp. Pl-1: Initial 1,2-, 3,4- and 9,10-dioxygenation, and meta- and ortho-cleavages of naphthalene-1,2-diol after its formation from naphthalene-1,2-dicarboxylic acid and hydroxyl naphthoic acids. Chemosphere 65:2388–2394

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smibert MR, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Willis A, Krieg NR (eds) Methods for general and molecular bacteriology. ASM, Washington DC, pp 607–654

    Google Scholar 

  • Stackenbrandt E, Liesack W (1993) Nucleic acid classification. In: Goodfellow M, O’ Connell AG (eds) Handbook of new bacterial systematics. Academic, London, pp 181–183

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tsitko IV, Zaitsev GM, Lobanok AG, Salkinoja-Salonen MS (1999) Effect of aromatic compounds on cellular fatty acid composition of Rhodococcus opacus. Appl Environ Microbiol 65:853–855

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ultee A, Kets EPW, Alberda M, Hoekstra FA, Smid EJ (2000) Adaptation of the food-borne pathogen Bacillus cereus to carvacrol. Arch Microbiol 174:233–238

    CAS  PubMed  Google Scholar 

  • Unell M, Kabelitz N, Jansson JK, Heipieper HJ (2007) Adaptation of the psychrotroph Arthrobacter chlorophenolicus A6 to growth temperature and the presence of phenols by changes in the anteiso/iso ratio of branched fatty acids. FEMS Microbiol Lett 266:138–143

    CAS  PubMed  Google Scholar 

  • Van Hamme JD, Singh A, Ward OP (2003) Recent advances in petroleum microbiology. Microbiol Mol Biol Rev 67:503–549

    PubMed  PubMed Central  Google Scholar 

  • Weber FJ, de Bont JAM (1996) Adaptation mechanisms of microorganisms to the toxic effects of organic solvents on membranes. Biochim Biophys Acta 1286:225–245

    CAS  PubMed  Google Scholar 

  • Whitman BE, Lueking DR, Mihelcic JR (1998) Naphthalene uptake by a Pseudomonas fluorescens isolate. Can J Microbiol 44:1086–1093

    CAS  PubMed  Google Scholar 

  • Wick LY, Pelz O, Bernasconi SM, Andersen N, Harms H (2003) Influence of the growth substrate on ester-linked phospho- and glycolipid fatty acids on PAH-degrading Mycobacterium sp. LB501T. Environ Microbiol 5:672–680

    CAS  PubMed  Google Scholar 

  • Willecke K, Pardee AB (1971) Fatty Acid-requiring Mutant of Bacillus subtilis Defective in Branched Chain α-Keto Acid Dehydrogenase. J Biol Chem 246:5264–5272

    CAS  PubMed  Google Scholar 

  • Zhang H, Kallimanis A, Koukkou AI, Drainas C (2004) Isolation and characterization of novel bacteria degrading polycyclic aromatic hydrocarbons from polluted Greek soils. Appl Microbiol Biotechnol 65:124–131

    CAS  PubMed  Google Scholar 

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Acknowledgements

This work was cofunded by the European Union in the framework of the program “Pythagoras II” of the “Operational Program for Education and Initial Vocational Training” of the Third Community Support Framework of the Hellenic Ministry of Education, funded by 25% from national sources and by 75% from the European Social Fund (ESF). Part of this work concerning the isolation and identification of strain Sphe3 was funded by the Greek Secretariat for Research and Technology (Programme PENED 1999).

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  1. Sector of Organic Chemistry and Biochemistry, Department of Chemistry, University of Ioannina, 45110, Ioannina, Greece

    Aristeidis Kallimanis, Constantin Drainas & Anna Irini Koukkou

  2. Laboratory of Biological Chemistry, Medical School, University of Ioannina, 45110, Ioannina, Greece

    Stathis Frillingos

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  1. Aristeidis Kallimanis
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  2. Stathis Frillingos
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  3. Constantin Drainas
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  4. Anna Irini Koukkou
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Correspondence to Anna Irini Koukkou.

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Kallimanis, A., Frillingos, S., Drainas, C. et al. Taxonomic identification, phenanthrene uptake activity, and membrane lipid alterations of the PAH degrading Arthrobacter sp. strain Sphe3. Appl Microbiol Biotechnol 76, 709–717 (2007). https://doi.org/10.1007/s00253-007-1036-3

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  • DOI: https://doi.org/10.1007/s00253-007-1036-3

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