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.
Similar content being viewed by others
References
Bateman JN, Speer BL, Feduik L, Hartline RA (1986) Naphthalene association and uptake in Pseudomonas putida. J Bacteriol 166:155–161
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917
Boggs JM (1984) Membrane fluidity. In: Kates M, Mansons LA (ed) Biomembranes vol. 12. Plenum, New York, pp 1–53
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
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
Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368
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
de Bont JAM (1998) Solvent-tolerant bacteria in biocatalysis. Trends Biotech 16:493–499
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
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
Habe H, Omori T (2003) Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 67:225–243
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
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
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
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
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
Kanaly RA, Harayama S (2000) Biodegradation of high-molecular-weight PAHs by bacteria. J Bacteriol 182:2059–2067
Keough KMW, Davis PJ (1984) Membrane fluidity. In: Kates M, Mansons LA (ed) Biomembranes, vol. 12. Plenum, New York, pp 55–97
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
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
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
Lowry OH, Rosenbrough NH, Farr AL, Randall RJ (1951) Protein measurement with Folin-phenol reagent. J Biol Chem 193:265–275
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
Morrison WR, Smith LM (1964) Preparation of fatty acids methyl esters and dimethylacetals from lipids with boronfluoride-methanol. J Lip Res 5:600–608
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
Mueller JG, Chapman PJ, Pritchard PH (1989) Creosote-contaminated sites. Environ Sci Technol 23:1197–1201
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
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
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
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
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
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
Sikkema J, de Bont JAM, Poolman B (1994) Interactions of cyclic hydrocarbons with biological membranes. J Biol Chem 269:8022–8028
Sikkema J, de Bont JAM, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222
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
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
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
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
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
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
Van Hamme JD, Singh A, Ward OP (2003) Recent advances in petroleum microbiology. Microbiol Mol Biol Rev 67:503–549
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
Whitman BE, Lueking DR, Mihelcic JR (1998) Naphthalene uptake by a Pseudomonas fluorescens isolate. Can J Microbiol 44:1086–1093
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
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
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
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).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-007-1036-3