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Bacterial metabolism of polycyclic aromatic hydrocarbons: strategies for bioremediation

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Abstract

Polycyclic aromatic hydrocarbons (PAHs) are compounds of intense public concern due to their persistence in the environment and potentially deleterious effects on human, environmental and ecological health. The clean up of such contaminants using invasive technologies has proven to be expensive and more importantly often damaging to the natural resource properties of the soil, sediment or aquifer. Bioremediation, which exploits the metabolic potential of microbes for the clean-up of recalcitrant xenobiotic compounds, has come up as a promising alternative. Several approaches such as improvement in PAH solubilization and entry into the cell, pathway and enzyme engineering and control of enzyme expression etc. are in development but far from complete. Successful application of the microorganisms for the bioremediation of PAH-contaminated sites therefore requires a deeper understanding of the physiology, biochemistry and molecular genetics of potential catabolic pathways. In this review, we briefly summarize important strategies adopted for PAH bioremediation and discuss the potential for their improvement.

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References

  1. Kästner M (2000) Degradation of aromatic and polyaromatic compounds. In H.-J. Rehm and G. Reed (eds) Biotechnology, Vol. 11b, Wiley-VCH, Weinheim, Germany. 211–239

    Chapter  Google Scholar 

  2. Blumer M (1976) Polycyclic aromatic compounds in nature. Sci American 234:35–45

    CAS  Google Scholar 

  3. Ramdahl T (1985) PAH emissions from combustion of biomass. In A. Bjørseth and T. Ramdahl (eds) Handbook of Polycyclic Aromatic Hydrocarbons, Macel Dekker, N.Y., 61–85

    Google Scholar 

  4. Saraswathy A and Hallberg R (2002) Degradation of pyrene by indigenous fungi from a former gasworks site. FEMS Microbiol Lett 210:227–232

    Article  PubMed  CAS  Google Scholar 

  5. Stefen KT (2003) Degradation of recalcitrant biopolymers and polycyclic aromatic hydrocarbons by litter-decomposing basidiomycetous fungi. Academic Dissertation in Microbiology, University of Helsinki Finland

  6. Brandt HCA and Watson WP (2003) Monitoring human occupational and environmental exposures to polycyclic aromatic compounds. Ann Occup Hyg 47:349–378

    Article  PubMed  CAS  Google Scholar 

  7. Hammond EC, Selikof IJ, Lawther PL and Seidman H (1976) Inhalation of benz[a]pyrene and cancer in man. Ann NY Acad Sci 271:116–124

    Article  PubMed  CAS  Google Scholar 

  8. Grimmer G (1979) Selected methods of analysis. In Environmental carcinogens, Vol. 3, IARC Scientific Publications No. 29, p. 31. Lyon: IARC

    Google Scholar 

  9. IPCS (1998) Selected non-heterocyclic polycyclic aromatic hydrocarbons. Environmental Health Criteria 202. International Programme on Chemical Safety, World Health Organization, Geneva

    Google Scholar 

  10. Liu K (2001) Polycyclic aromatic hydrocarbon (PAH) emissions from a coal fired pilot FBC system. J Hazard Mater 84:175–188

    Article  PubMed  CAS  Google Scholar 

  11. Mastrangela G (1997) Polycyclic aromatic hydrocarbons and cancer in man. Environ Health Perspect 104:1166–1170

    Article  Google Scholar 

  12. Sram RJ (1999) Adverse reproductive outcomes from exposure to environmental mutagens. Mutat Res 428:203–215

    PubMed  CAS  Google Scholar 

  13. Wilson SC and Jones KC (1993) Bioremediation of soil contaminated with polynucleararomatic hydrocarbons (PAHs): a review. Environ Poll 81:229–249

    Article  CAS  Google Scholar 

  14. Cerniglia CE and Heitkamp MA (1989) Microbial degradation of polycyclic aromatic hydrocarbons (PAH) in the aquatic environment. In U. Varanasi (ed) Metabolismof Polycyclic Aromatic Hydrocarbons in the Aquatic Environment, CRC Press, Inc., BocaRaton, Florida. 41–68

    Google Scholar 

  15. Goldman R (2001) Smoking increases carcinogenic polycyclic aromatic hydrocarbons in human lung tissue. Cancer Res 61:6367–6371

    PubMed  CAS  Google Scholar 

  16. Kaiser J (1997) Endocrine disrupters: Synergy paper questioned at toxicology meeting. Science 275:1879–1880

    Article  PubMed  CAS  Google Scholar 

  17. Pothuluri JV and Cerniglia CE (1994) Microbial metabolism of polycyclic aromatic hydrocarbons. In: G.R. Chaudhry, Editor, Biological degradation and Bioremediation of Toxic Chemicals, Chapman and Hall, 92–124

  18. Howard PH, Boethling RS, Jarvis WF, Meylan WM and Michalenko EM (1991) Handbook of Environmental Degradation Rates. Printup, H.T. (ed). Lewis Publishers, Chelsea, MI

    Google Scholar 

  19. Bamforth SM and Singleton I (2005) Bioremediation of polycyclic aromatic hydrocarbons: current knowledge and future directions. J Chemical Technol Biotechnol 80:723–736

    Article  CAS  Google Scholar 

  20. Ulric W (2000) Contaminated soil areas, different countries and contaminants, monitoring of contaminants. In: Rehm, H.J., Reed, G., Pühler, A., Stadler, P. (2 [nd] Eds.), Biotechnology Vol. 11b: environmental Processes II, Wiley-VCH, Weihheim, FRG, pp. 5–42

    Google Scholar 

  21. Mueller JG, Lantz SE, Ross D, Colvin RJ, Middaugh DP and Pritchard PH (1993) Strategy using bioreactors and specially selected micro-organisms for bioremediation of groundwater contaminated with creosote and pentachlorophenol. Environ Sci Technol 27:691–698

    Article  CAS  Google Scholar 

  22. Cerniglia CE (1993) Biodegradation of polycyclic aromatic hydrocarbons. Curr Opn Biotechnol 4:331–338

    Article  CAS  Google Scholar 

  23. Samanta SK, Singh OV and Jain RK (2002) Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends Biotechnol 20:243–248

    Article  PubMed  CAS  Google Scholar 

  24. Patel TR and ainsley EA (1980) Napthelene metabolism by Pseudomonads: Purification and properties of 1,2-dihydroxynaphthalene oxygenase. J Bateriol 143:668–673

    CAS  Google Scholar 

  25. Samanta SK, Rani M and Jain RK (1998) Segregational and structural instability of a recombinant plasmid carrying genes for naphthalene degradation. Lett Appl Microbiol 26:265–269

    Article  PubMed  CAS  Google Scholar 

  26. Johnsen AR, Lukas Yand Hauke H (2005) Principles of microbial PAH-degradation in soil. Environ Poll 1:71–84

    Article  CAS  Google Scholar 

  27. Smith MR (1990) The biodegradation of aromatic hydrocarbons by bacteria. Biodegradation 1:191–206

    Article  PubMed  CAS  Google Scholar 

  28. Watanabe K (2001) Microrganisms relevant to bioremediation. Curr Opin Biotechnol 12:237–241

    Article  PubMed  CAS  Google Scholar 

  29. Bakermans C, Hohnstock-Ashe AM, Padmanabhan S, Padmanabhan P and Madsen EL (2002) Geochemical and physiological evidence for mixed aerobic and anaerobic field biodegradation of coal tar waste by subsurface microbial communities. Microbial Ecol 44:107–117

    Article  CAS  Google Scholar 

  30. Bewley RJF and Webb G (2001) In situ bioremediation of groundwater contaminated with phenols, BTEX and PAHs using nitrate as electron acceptor. Land Contam Reclam 9:335–347

    Google Scholar 

  31. Meckenstock RU, Annweiler E, Michaelis W, Richnow HH and Schink B (2000) Anaerobic naphthalene degradation by a sulphate reducing enrichment culture. Appl Environ Microbiol 66:2743–2747

    Article  PubMed  CAS  Google Scholar 

  32. Genthner BRS, Townsend GT, Lantz SE and Mueller JG (1997) Persistence of polycyclic aromatic hydrocarbon components of creosote under anaerobic enrichment conditions. Arch Environ Contam Toxicol 32:99–105

    Article  Google Scholar 

  33. Coates JD, Anderson RT and Lovley DR (1996) Oxidation of polycyclic aromatic hydrocarbons under sulfate-reducing conditions. Appl Environ Microbiol 62:1099–1101

    PubMed  CAS  Google Scholar 

  34. Ohkouchi N, Kawamura K and Kawahata H (1999) Distributions of three to seven-ring polynuclear aromatic hydrocarbons on the deep sea floor in the central pacific. Environ Sci Technol 33:3086–3090

    Article  CAS  Google Scholar 

  35. Zhang X, Sullivan ER and Young LY (2000) Evidence for aromatic ring reduction in the biodegradation pathway of carboxylated naphthalene by a sulphate-reducing consortium. Biodegradation 11:117–124

    Article  PubMed  CAS  Google Scholar 

  36. Ambrosoli R, Petruzzelli L, Minati JL and Marsan FA (2005) Anaerobic PAH degradation in soil by a mixed bacterial consortium under denitrifying conditions. Chemosphere 60:1231–1236

    Article  PubMed  CAS  Google Scholar 

  37. Quantin C, Joner EJ, Portal JM and Berthelin J (2005) PAH dissipation in a contaminated river sediment under oxic and anoxic conditions. Environ Poll 134:315–322

    Article  CAS  Google Scholar 

  38. Xu-Xiang Z, Shu-Pei C, Cheng-Jun Z and Shi-Lei S (2006) Microbial PAH degradation in soil: degradation pathways and contributing factors. Pedosphere 16:555–565

    Article  Google Scholar 

  39. Kim S-Ja, Kweon O, Freeman JP Jones RC, Adjei MD, Jhoo J-W, Edmondson RD and Cerniglia CE (2006) Molecular cloning and expression of genes encoding a novel dioxygenase involved in low-and high-molecular-weight polycyclic aromatic hydrocarbon degradation in Mycobacterium vanbaalenii PYR-1. Appl Environ Microbiol 72:1045–1054

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  41. Bosch R, Garcia-Valdés E and Moore ERB (1999) Genetic characterization and evolutionary implications of a chromosomally encoded naphthalene-degradation upper pathway from Pseudomonas stutzeri AN10. Gene 236:149–157

    Article  PubMed  CAS  Google Scholar 

  42. Sanseverino J, Applegate BM, King JM and Sayler GS (1993) Plasmid-mediated mineralization of naphthalene, phenanthrene, and anthracene. Appl Environ Microbiol 59:1931–1937

    PubMed  CAS  Google Scholar 

  43. Takizawa N, Iida T, Sawada T, Yamauchi K, Wang Y-W, Fukuda M and Kiyohara H (1999) Nucleotide sequences and characterization of genes encoding naphthalene upper pathway of Pseudomonas aeruginosa PaK1 and Pseudomonas putida OUS82. J Biosci Bioeng 87:723–731

    Article  Google Scholar 

  44. Habe H and Omori T (2003) Genetics of polycyclic aromatic hydrocarbon degradation by diverse aerobic baceria. Biosci Biotechnol Biochem 67:225–243

    Article  PubMed  CAS  Google Scholar 

  45. Juhasz AL (2000) Microbial degradation and detoxification of high molecular weight polycyclic aromatic hydrocarbons by Stenotrophomonas maltophilia strain VUN 10003. Lett Appl Microbiol 30:396–401

    Article  PubMed  CAS  Google Scholar 

  46. Kanaly RA and Harayama S (2000) Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria. J Bacteriol 182:2059–2067

    Article  PubMed  CAS  Google Scholar 

  47. Watanabe K (2001) Microorganisms relevant to bioremediation. Curr Opin Biotechnol 12:237–241

    Article  PubMed  CAS  Google Scholar 

  48. Hatfull GF and Jacobs WR (2000) Molecular genetics of Mycobacteria. ASM Press, Washington, DC

    Google Scholar 

  49. Khan AA, Wang R-F, Cao W-W, Doerge DR, Wennerstrom D and Cerniglia CE (2001) Molecular cloning, nucleotide sequence, and expression of genes encoding a polycyclic aromatic ring dioxygenase from Mycobacterium sp. strain PYR-1. Appl Environ Microbiol 67:3577–3585

    Article  PubMed  CAS  Google Scholar 

  50. Krivobok S, Kuony S, Meyer C, Louwagie M, Willison JC and Jouanneau Y (2003) Identification of pyrene-induced proteins in Mycobacterium sp. strain 6PY1: evidence for two ring-hydroxylating dioxygenases. J Bacteriol 185:3828–3841

    Article  PubMed  CAS  Google Scholar 

  51. Sho M, Hamel C and Greer CW (2004) Two distinct gene clusters encode pyrene degradation in Mycobacterium sp. strain S65. FEMS Microbiol Ecol 48:209–220

    Article  CAS  PubMed  Google Scholar 

  52. Brezna B, Khan AA and Cerniglia CE (2003) Molecular characterization of dioxygenases from polycyclic aromatic hydrocarbon-degrading Mycobacterium sp. FEMS Microbiol Lett 223:177–183

    Article  PubMed  CAS  Google Scholar 

  53. Hall K, Miller CD, Sorensen DL, Anderson AJ and Sims RC (2005) Development of a catabolically significant genetic probe for polycyclic aromatic hydrocarbon-degrading Mycobacteria in soil. Biodegradation 16:475–484

    Article  PubMed  CAS  Google Scholar 

  54. Cruden DL, Gibson DT and Zylstra GJ (1993) Sequences of genes encoding naphthalene dioxygenase in Pseudomonas putida strains G7 and NCIB 9816-4. Gene 127:31–37

    Article  PubMed  Google Scholar 

  55. Brezna B, Khan AA and Cerniglia CE (2004) Molecular characterization of a phenanthrene degradation pathway in Mycobacterium vanbaalenii PYR-1. Biochem Biophys Res Commun 322:133–146

    Article  CAS  Google Scholar 

  56. Pagnout C, Frache G, Poupin P, Maunit B, Muller J-F and Férard J-F (2007) Isolation and characterization of a gene cluster involved in PAH degradation in Mycobacterium sp. strain SNP11: Expression in Mycobacterium smegmatis mc 2155. Res Microbiol 158:175–186

    Article  PubMed  CAS  Google Scholar 

  57. Brezna B, Kweon O, Stingley RL, Freeman JP, Polek B, Jones, RC, Khan AA and Cerniglia CE (2006) Molecular characterization of cytochrome P450 genes in the polycyclic aromatic hydrocarbon degrading Mycobacterium vanbaalenii PYR-1. Appl Microbiol Biotechnol 71:522–532

    Article  PubMed  CAS  Google Scholar 

  58. Liang Y, Gardner DR, Miller CD, Chen D, Anderson AJ, Weimer, BC and Sims RC (2006) Study of biochemical pathways and enzymes involved in pyrene degradation by Mycobacterium sp. strain KMS. Appl Environ Microbiol 72:7821–7828

    Article  PubMed  CAS  Google Scholar 

  59. Kim S-J, Kweon O, Jones Richard C, Freeman JP, Edmondson RD and Cerniglia CE (2007) Complete and integrated pyrene degradation pathway in Mycobacterium vanbaalenii PYR-1 based on systems biology. J Bacteriol 189: 464–472

    Article  PubMed  CAS  Google Scholar 

  60. Juhasz AL and Naidu R (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. Int Biodeterior Biodegradation 45:57–88

    Article  CAS  Google Scholar 

  61. Kastner M and Mahro B (1996) Microbial degradation of polycyclic aromatic hydrocarbons in soils affected by the organic matrix of compost. Appl Microbiol Biotechnol 44:668–675

    Article  PubMed  CAS  Google Scholar 

  62. Pandey G and Jain RK (2002) Bacterial chemotaxis toward environmental pollutants: role in bioremediation. Appl Environ Microbiol 68:5789–5795

    Article  PubMed  CAS  Google Scholar 

  63. Herrenkohl MJ, Lunz JD, Sheets RG and Wakeman JS (2001) Environmental impacts of PAH and oil release as a NAPL or as contaminated pore water from the construction of a 90-cm in situ isolation cap. Environ Sci Technol 35:4927–4932

    Article  PubMed  CAS  Google Scholar 

  64. Schluep M, Imboden DM, Galli R and Zeyer J (2001) Mechanisms affecting the dissolution of nonaqueous phase liquids into the aqueous phase in slow stirring batch system. Environ Toxicol Chem 20:459–466

    Article  PubMed  CAS  Google Scholar 

  65. Wick, LY, Colangelo T and Harms H (2001). Kinetics of mass transfer-limited bacterial growth on solid PAHs. Environ Sci Technol 35:354–361

    Article  PubMed  CAS  Google Scholar 

  66. Volkering F, Breure AM, Andel JGV and Rulkens WH (1995) Influence of nonionic surfactants on bioavailability and biodegradation of polycyclic aromatic hydrocarbons. Appl Environ Microbiol 61:1699–1705

    PubMed  CAS  Google Scholar 

  67. Grimberg SJ (1996) Quantifying the biodegradation of phenanthrene by Pseudomonas stutzeri P16 in the presence of a nonionic surfactant. Appl Environ Microbiol 62:2387–2392

    PubMed  CAS  Google Scholar 

  68. Willumsen PA (2001) Degradation of phenanthrene-analogue azaarenes by Mycobacterium gilvum strain LB307T under aerobic conditions. Appl Microbiol Biotechnol 56:539–544

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  70. Rosenberg E, Barkay T, Navon-Venezia S and Ron EZ (1999) Role of Acinetobacter bioemulsans in petroleum degradation. In Novel Approaches for Bioremediation of Organic Pollution. Edited by Fass R. New York: Kluwer Academic/Plenum Publishers; 171–180

    Google Scholar 

  71. Barkay T, Navon-Venezia S, Ron E and Rosenberg E (1999) Enhancement of solubilization and biodegradation of polyaromatic hydrocarbons by the bioemulsifier alasan. Appl Environ Microbiol 65:2697–2702

    PubMed  CAS  Google Scholar 

  72. Aronstein BN and Alexander M (1992) Surfactants at low concentrations stimulate biodegradation of sorbed hydrocarbons in samples of aquifer sands and soil slurries. Environ Toxicol Chem 11:1227–1233

    Article  CAS  Google Scholar 

  73. Aronstein BN and Alexander M (1993) Effect of a non-ionic surfactant added to the soil surface on the biodegradation of aromatic hydrocarbons within the soil. Appl Environ Microbiol 39:386–390

    CAS  Google Scholar 

  74. Bury SJ and Miller CA (1993) Effect of micellar solubilization on biodegradation rates of hydrocarbons. Environ Sci Technol 27:104–110

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  76. Tiehm A (1994) Degradation of polycyclic aromatic hydrocarbons in the presence of synthetic surfactants. Appl Environ Microbiol 60:258–263

    PubMed  CAS  Google Scholar 

  77. Straube WL, Nestler CC, Hansen LD, Ringleberg D, Pritchard PJ and Jones-Meehan J (2003) Remediation of polyaromatic hydrocarbons (PAHs) through landfarming with biostimulation and bioaugmentation. Acta Biotechnologica 2:179–196

    Article  Google Scholar 

  78. Mulligan and Gibbs (1993) Factors influencing the economics of biosurfactants In: N. Kosaric, Editors, Biosurfactants, Production, Properties, Applications, Marcel Dekker, New York, pp. 329–371

    Google Scholar 

  79. Deschênes L, Lafrance P, Villeneuve J-P and Samson R (1995) The effect of an anionic surfactant on the mobilization and biodegradation of PAHs in a creosote-contaminated soil. Hydrol Sci J 40:471–484

    Article  Google Scholar 

  80. Grimberg SJ and Aitken MD (1995) Biodegradation kinetics of phenanthrene solubilized in surfactant micelles, p. 59–66. In R. E. Hinchee, F. J. Brockman, and C. M. Vogel (ed.), Microbial processes for bioremediation. Battelle Press, Columbus, Ohio

    Google Scholar 

  81. Laha S and Luthy RG (1992) Effects of nonionic surfactants on the solubilization and mineralization of phenanthrene in soil-water systems. Biotechnol Bioeng 40:1367–1380

    Article  PubMed  CAS  Google Scholar 

  82. Bruheim P (1997) Bacterial degradation of emulsified crude oil and the effect of various surfactants. Can J Microbiol 43:17–22

    PubMed  CAS  Google Scholar 

  83. Bruheim P (1998) Chemically emulsified crude oil as substrate for bacterial oxidation: differences in species response. Can J Microbiol 44:195–199

    Article  PubMed  CAS  Google Scholar 

  84. García-Junco ME, de Olmedo and Ortega-Calvo JJ (2001) Bioavailability of solid and non-aqueous phase liquid (NAPL)-dissolved phenanthrene to the biosurfactant-producing bacterium Pseudomonas aeruginosa 19SJ. Environ Microbiol 3:561–569

    Article  PubMed  Google Scholar 

  85. Guerin WF and Boyd SA (1992) Differential bioavailability of soil-sorbed naphthalene to two bacterial species. Appl Environ Microbiol 58:1142–1152

    PubMed  CAS  Google Scholar 

  86. Tang, WC, White JC and Alexander M (1998) Utilization of sorbed compounds by microorganisms specifically isolated for that purpose. Appl Microbiol Biotechnol 49:117–121

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  89. Tongpim S and Pickard MA (1996) Growth of Rhodococcus S1 on anthracene. Can J Microbiol 42:289–294

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  92. Dean-Ross D, Moody J and Cerniglia CE (2002) Utilization of mixtures of polycyclic aromatic hydrocarbons by bacteria isolated from contaminated sediment. FEMS Microbiol Ecol 41:1–7

    Article  CAS  PubMed  Google Scholar 

  93. McLellan SL, Warshawsky D and Shann JR (2002) The effect of polycyclic aromatic hydrocarbons on the degradation of benzo[aa]pyrene by Mycobacterium sp. strain RJGII-135. Environ Toxicol Chem 21:253–259

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  96. Kahng HY, Byrne AM, Olsen RH and Kukor JJ (2000) Characterization and role of tbuXtbuX in utilization of toluene by Ralstonia PKO1. J Bacteriol 182:1232–1242

    Article  PubMed  CAS  Google Scholar 

  97. Kasai Y, Inoue J and Harayama S (2001) The TOL plasmid pWW0 xylNxylN gene product from Pseudomonas putida is involved in mm-xylene uptake. J Bacteriol 183:6662–6666

    Article  PubMed  CAS  Google Scholar 

  98. Beal R and Betts (2000) Role of rhamnolipid biosurfactants in the uptake and mineralization of hexadecane in Pseudomonas aeruginosa. J Appl Microbiol 89:158–168

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  100. Noordman WH and Janssen DB (2002) Rhamnolipid stimulates uptake of hydrophobic compounds by Pseudomonas aeruginosa. Appl Environ Microbiol 68:4502–4508

    Article  PubMed  CAS  Google Scholar 

  101. Noda KI, Watanabe K and Maruhashi K (2003) Isolation of the Pseudomonas aeruginosa gene affecting uptake of dibenzothiophene in nn-tetradecane. J Biosci Bioeng 95:504–511

    PubMed  CAS  Google Scholar 

  102. Black PN and DiRusso CC (1994) Molecular and biochemical analyses of fatty acid transport, metabolism, and gene regulation in Escherichia coli. Biochim Biophys Acta 1210:123–145

    PubMed  CAS  Google Scholar 

  103. Hirsch D, Stahl A and Lodish HF (1998) A family of fatty acid transporters conserved from Mycobacterium to man. Proc Natl Acad Sci USA 95:8625–8629

    Article  PubMed  CAS  Google Scholar 

  104. Diaz E and Prieto MA (2000) Bacterial promoters triggering biodegradation of aromatic pollutants. Curr Opin Biotechnol 11:467–475

    Article  PubMed  CAS  Google Scholar 

  105. Cases and V de Lorenzo (1998) Expression systems and physiological control of promoter activity in bacteria. Curr Opin Microbiol 1:303–310

    Article  PubMed  CAS  Google Scholar 

  106. Platt A, Shingler V, Taylor SC and Williams PA (1995) The 4-hydroxy-2-oxovalerate aldolase and acetaldehyde dehydrogenase (acylating) encodedby the nahM and nahO genes of the naphthalene catabolic plasmid pWW60-22 provide further evidence of conservation of meta-cleavage pathway gene sequences. Microbiology 141:2223–2233

    PubMed  Google Scholar 

  107. Simon MJ, Osslund TD, Saunders R, Ensley BD, Suggs S, Harcourt, W-C, Cruden SL, Gibson DT and Zylstra GJ (1993) Sequence of genes encoding naphthalene dioxygenase in Pseudomonas putida strains G7 and NCIB 9816-4. Gene 127:31–37

    Article  PubMed  CAS  Google Scholar 

  108. Yen K-M and Serdar CM (1988) Genetics of naphthalene catabolism in Pseudomonads. CRC Crit Rev Microbiol 15:247–268

    Article  CAS  Google Scholar 

  109. QLau PCK, Wang Y, Patel A, Labbe D, Bergeron H, Brousseau R, Konishi Y and Rawlings (1997) A bacterial basic region leucine zipper histidine kinase regulating toluene degradation. Proc Natl Acad Sci 95:1453–1458

    Article  Google Scholar 

  110. Goldstein RM, Mallory LM and Alexander M (1985) Reasons for possible failure of inoculation to enhance biodegradation. Curr Opin Biotechnol 50:977–983

    CAS  Google Scholar 

  111. Bouchez M, Blanchet D and Vandecasteele V-P (1995) Degradation of polycyclic aromatic hydrocarbons by pure strains and by defined strain associations: inhibition phenomena and cometabolism. Appl Microbiol Biotechnol 43:156–164

    Article  PubMed  CAS  Google Scholar 

  112. Wagner-Döbler I (2003) Pilot plant for bioremediation of mercury-containing industrial wastewater. Appl Microbiol Biotechnol 62:124–133

    Article  PubMed  CAS  Google Scholar 

  113. Providenti MA, Lee H and Trevors JT (1993) Selected factors limiting the microbial degradation of recalcitrant compounds. J Ind Microbiol 12:379–395

    Article  CAS  Google Scholar 

  114. Molina M, Araujo R and Hodson RE (1999) Cross-induction of pyrene and phenanthrene in a Mycobacterium sp. isolated from polycyclic aromatic hydrocarbon contaminated river sediments. Can J Microbiol 45:520–529

    Article  PubMed  CAS  Google Scholar 

  115. Mohan S, Takuro K, Takeru O, Robert K and Yoshihisa S (2006) Bioremediation technologies for treatment of PAH-contaminated soil and strategies to enhance process efficiency. Rev Environ Sci Biotechnol 5:347–374

    Article  CAS  Google Scholar 

  116. Demane che S, Meyer C, Micoud J, Louwagie M, Willison JC and Jouanneaul Y (2004) Identification and functional analysis of two aromatic-ring-hydroxylating dioxygenases from a Sphingomonas strain that degrades various polycyclic aromatic hydrocarbons. Appl Environ Microbiol 70:6714–6725

    Article  CAS  Google Scholar 

  117. Gilbert ES and Crowley DE (1997) Plant compounds that induce polychlorinated biphenyl biodegradation by Arthrobacter sp. strain B1B. Appl Environ Microbiol 63:1933–1938

    PubMed  CAS  Google Scholar 

  118. Ohtsubo Y, Shimura M, Delawary M, Kimbara K, Takagi M, Kudo T, Ohta A, Nagata Y (2003) Novel approach to the improvement of biphenyl and polychlorinated biphenyl degradation activity: promoter implantation by homologous recombination. Appl Environ Microbiol 69:146–153

    Article  PubMed  CAS  Google Scholar 

  119. Batie CJ, LaHaie E and Ballou DP (1987) Purification and characterization of phthalate oxygenase and phthalate oxygenase reductase from Pseudomonas cepacia. J Biol Chem 262:1510–1518

    PubMed  CAS  Google Scholar 

  120. Correll CC, Batie CJ, Ballou DP and Ludwig ML (1992) Phthalate dioxygenase reductase: a modular structure for electron transfer from pyridine nucleotides to [2Fe-2S]. Science 258:1604–1610

    Article  PubMed  CAS  Google Scholar 

  121. Kauppi B, Lee K, Carredano E, Parales RE, Gibson DT, Eklund H and Ramaswamy S (1998) Structure of an aromatic-ring-hydroxylating dioxygenase-naphthalene 1,2-dioxygenase. Structure 6:571–586

    Article  PubMed  CAS  Google Scholar 

  122. Parales RE, Lee K, Resnick SM, Jiang HY, Lessner DJ and Gibson DT (2000) Substrate specificity of naphthalene dioxygenase: effect of specific amino acids at the active site of the enzyme. J BacterioL 182:1641–1649

    Article  PubMed  CAS  Google Scholar 

  123. Furusawa Y, Nagarajan V, Tanokura M, Masai E, Fukuda M and Senda T (2004) Crystal structure of the terminal oxygenase component of biphenyl dioxygenase derived from Rhodococcus sp. strain RHA1. J Mol Biol 342:1041–1052

    Article  PubMed  CAS  Google Scholar 

  124. Jouanneau Y, Meyer C, Jakoncic J, Stojanoff V and Gaillard J (2006) Characterization of a naphthalene dioxygenase endowed with an exceptionally broad substrate specificity toward polycyclic aromatic hydrocarbons. Biochemistry 45:12380–12391

    Article  PubMed  CAS  Google Scholar 

  125. Hammel KE, Kalyanaraman B and Kirk TK (1986) Oxidation of polycyclic aromatic-hydrocarbons and dibenzo P-dioxins by phanerochaete-chrysosporium ligninase. J Biol Chem 261:6948–6952

    Google Scholar 

  126. Ang EL, Zhao H and Obbard JP (2005) Recent advances in the bioremediation of persistent organic pollutants via biomolecular engineering. Enz Microbial Technol 37:487–496

    Article  CAS  Google Scholar 

  127. Bulter T, Alcalde T, Sieber V, Meinhold P, Schlachtbauer C and Arnold FH (2003) Functional expression of a fungal laccase in Saccharomyces cerevisiae by directed evolution. Appl Environ Microbiol 69:987–995

    Article  PubMed  CAS  Google Scholar 

  128. Alcalde M, Ferrer M, Plou FJ and Ballesteros A (2006) Environmental biocatalysis: from remediation with enzymes to novel green processes. Trends Biotechnol 24:281–287

    Article  PubMed  CAS  Google Scholar 

  129. Harford-Cross CF, Carmichael AB, Allan AK, England PA, Rouch DA and Wong LL (2000) Protein engineering of cytochrome P450(cam) (CYP101) for the oxidation of polycyclic aromatic hydrocarbons. Prot Eng 13:121–128

    Article  CAS  Google Scholar 

  130. Carmichael AB and Wong LL (2001) Protein engineering of Bacillus megaterium CYP102-the oxidation of polycyclic aromatic hydrocarbons. Eur J Biochem 268:3117–3125

    Article  PubMed  CAS  Google Scholar 

  131. Li QS, Ogawa J, Schmid RD and Shimizu S (2001) Engineering cytochrome P450BM-3 for oxidation of polycyclic aromatic hydrocarbons. Appl Environ Microbiol 67:5735–5739

    Article  PubMed  CAS  Google Scholar 

  132. Joo ZL, Lin and Arnold FH (1999) Laboratory evolution of peroxide-mediated cytochrome P450 hydroxylation. Nature 399:670–673

    Article  PubMed  CAS  Google Scholar 

  133. Salazar O, Cirino PC and Arnold FH (2003) Thermostabilization of a cytochrome p450 peroxygenase. Chembiochem 4:891–893

    Article  PubMed  CAS  Google Scholar 

  134. Belotte D, Curien JB, Maclean RC and Bell G (2003) An experimental test of local adaptation in soil bacteria. Evolution 57:27–36

    PubMed  Google Scholar 

  135. Law AM and Aitken MD (2003) Bacterial chemotaxis to naphthalene desorbing from a nonaqueous liquid. Appl Environ Microbiol 69:5968–5973

    Article  PubMed  CAS  Google Scholar 

  136. Bhushan B (2000) Chemotaxis and biodegradation of 3-methyl-4-nitrophenol by Ralstonia sp. SJ98. Biochem Biophy Res Commun 275:129–133

    Article  CAS  Google Scholar 

  137. Bhushan B (2000) Chemotaxis and biodegradation of 3-methyl-4-nitrophenol by Ralstonia sp. SJ98. Biochem Biophy Res Commun 275:129–133

    Article  CAS  Google Scholar 

  138. Gentry TJ, Rensing C and Pepper IL (2004) New approaches for bioaugmentation as a remediation technology. Cri Rev Environ Sci Technol 34:447–494

    Article  CAS  Google Scholar 

  139. Kuiper I, Lagendijk EL, Bloemberg, GV and Lugtenberg BJJ (2004) Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant Microbe Interact 17:6–15

    Article  PubMed  CAS  Google Scholar 

  140. Wu CH, Wood TK, Mulchandani A and Chen W (2006) Engineering plant-microbe symbiosis for rhizoremediation of heavy metals. Appl Environ Microbiol 72:1129–1134

    Article  PubMed  CAS  Google Scholar 

  141. Barac T, Taghavi S, Borremans B, Provoost A, Oeyen L and Colpaert JV (2004) Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nat Biotechnol 22:583–588

    Article  PubMed  CAS  Google Scholar 

  142. Villacieros M, Whelan C, Mackova M, Molgaard J, Sánchez-Contreras M and Lloret J (2005) Polychlorinated biphenyl rhizoremediation by Pseudomonas fluorescens F113 derivatives, using a Sinorhizobium meliloti nod system to drive bph gene expression. Appl Environ Microbiol 71:2687–2694

    Article  PubMed  CAS  Google Scholar 

  143. Kuiper I, Kravchenko LV, Bloemberg GV and Lugtenberg BJJ (2002) Pseudomonas putida strain PCL1444, selected for efficient root colonization and naphthalene degradation, effectively utilizes root exudate components. Mol Plant Microbe Interact 15:734–741

    Article  PubMed  CAS  Google Scholar 

  144. Monti MR, Smania AM, Fabro G, Alvarez ME and Argaraña CE (2005) Engineering Pseudomonas fluorescens for biodegradation of 2,4-dinitrotoluene. Appl Environ Microbiol 71:8864–8872

    Article  PubMed  CAS  Google Scholar 

  145. Crowley DE, Brennerova MV, Irwin C, Brenner V and Focht DD (1996) Rhizosphere effects on biodegradation of 2,5-dichlorobenzoate by a bioluminescent strain of root-colonizing Pseudomonas fluorescens. FEMS Microbiol Ecol 20:79–89

    Article  CAS  Google Scholar 

  146. Kuiper I, Bloemberg GV and Lugtenberg BJ (2001) Selection of a plant-bacterium pair as a novel tool for rhizostimulation of polycyclic aromatic hydrocarbon-degrading bacteria. Mol Plant Microbe Interact 14:1197–1205

    Article  PubMed  CAS  Google Scholar 

  147. Liu L, Jiang C-Y, Liu X-Y, Wu J-F, Ha J-G and Liu S-J (2007) Plant-microbe association for rhizoremediation of chloronitroaromatic pollutants with Comamonas sp. strain CNB-1. Environ Microbiol 9:465–473

    Article  PubMed  CAS  Google Scholar 

  148. Child R, Miller C, Liang Y, Narasimham G, Chatterton J, Harrison P, Sims R, Britt D and Anderson A (2007) Polycyclic aromatic hydrocarbon-degrading Mycobacterium isolates: their association with plant roots. Appl Microbiol Biotechnol 75:655–663

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Rakesh K. Jain.

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Chauhan, A., Fazlurrahman, Oakeshott, J.G. et al. Bacterial metabolism of polycyclic aromatic hydrocarbons: strategies for bioremediation. Indian J Microbiol 48, 95–113 (2008). https://doi.org/10.1007/s12088-008-0010-9

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