, Volume 81, Issue 6, pp 639–650 | Cite as

Aerobic bacterial degradation of polycyclic aromatic hydrocarbons (PAHs) and its kinetic aspects

  • M. A. Baboshin
  • L. A. GolovlevaEmail author


Aerobic bacterial degradation of PAHs is reviewed. Particular attention is paid to its kinetic aspects (rate and specificity). The general concepts of PAH biodegradation in nature and the role of aerobic bacteria in this process are described. The problem of PAH bioavailability and the mechanism of PAH penetration through bacterial cell wall are discussed. The key role of the reaction of PAH hydroxylation in controlling the rate and specificity of PAH biodegradation process is substantiated. The effects of competitive inhibition, intermediate inhibition, cross induction, and cometabolism are considered. The importance of microbial communities for PAH biodegradation in natural ecosystems is shown. The review contains the list of 138 references.


PAH biodegradation bioavailability dioxygenases kinetics specificity inhibition microbial communities 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Yan, J., Wang, L., Fu, P.P., and Yu, H., Photomutagenicity of 16 Polycyclic Aromatic Hydrocarbons from the US EPA Priority Pollutant List, Mutat. Res., 2004, vol. 557, pp. 99–108.PubMedCrossRefGoogle Scholar
  2. 2.
    Srogi, K., Monitoring of Environmental Exposure to Polycyclic Aromatic Hydrocarbons: A Review, Environ. Chem. Lett., 2007, vol. 5, pp. 169.CrossRefGoogle Scholar
  3. 3.
    Shental, R., 1971. Carcinogenic Effect of Polycyclic Aromatic Hydrocarbons and Some Other Compounds, in Politsiklicheskie uglevodorody (Polycyclic Hydrocarbons), Clar, E., Ed., Moscow: Mir, vol. 1, pp. 138–163.Google Scholar
  4. 4.
    Johnsen, A.R. and Karlson, U., Diffuse PAH Contamination of Surface Soils: Environmental Occurrence, Bioavailability, and Microbial Degradation, Appl. Microbiol. Biotechnol., 2007, vol. 76, pp. 533–543.PubMedCrossRefGoogle Scholar
  5. 5.
    Mueller, J.G., Chapman, P.J., and Pritchard, P.H., Creosote Contaminated Sites: Their Potential for Bioremediation, Environ. Sci. Technol., 1989, vol. 23, pp. 1197–1201.CrossRefGoogle Scholar
  6. 6.
    Allard, A.-S. and Neilson, A.H., Bioremediation of Organic Waste Sites: A Critical Review of Microbiological Aspects, Int. Biodeterior. Biodegr., 1997, vol. 39, pp. 253–285.CrossRefGoogle Scholar
  7. 7.
    Birak, P.S. and Miller, C.T., Dense Non-Aqueous Phase Liquids at Former Manufactured Gas Plants: Challenges to Modeling and Remediation, J. Contaminant Hydrol., 2009, vol. 105, pp. 81–98.CrossRefGoogle Scholar
  8. 8.
    Cerniglia, C.E., Biodegradation of Polycyclic Aromatic Hydrocarbons, Biodegradation, 1992, vol. 3, pp. 351–368.CrossRefGoogle Scholar
  9. 9.
    Barker, J.F., Fraser, M., Blaine, F., and Cooke, C., Natural Attenuation of PAHs and Heterocyclic Organics in Groundwater: 10 Years of Experience with a Controlled Field Experiment, 12th Int. Petrol. Environ. Conf., Houston, 2005.Google Scholar
  10. 10.
    Fraser, M., Barker, J.F., Butler, B., Blaine, F., Joseph, S., and Cooke, C., Natural Attenuation of a Plume from an Emplaced Coal Tar Creosote Source over 14 Years, J. Contaminant Hydrol., 2009, vol. 100, pp. 101–115.CrossRefGoogle Scholar
  11. 11.
    Mulligan, C.N. and Yong, R.N., Natural Attenuation of Contaminated Soils, Environ. Int., 2004, vol. 30, pp. 587–601.PubMedCrossRefGoogle Scholar
  12. 12.
    Atagana, H.I., Bioremediation of Creosote-Contaminated Soil in South Africa by Landfarming, J. Appl. Microbiol., 2004, vol. 96, pp. 510–520.PubMedCrossRefGoogle Scholar
  13. 13.
    Antizar-Ladislao, B., Lopez-Real, J., and Beck, A., Bioremediation of Polycyclic Aromatic Hydrocarbon (PAH)-Contaminated Waste Using Composting Approaches, Crit. Rev. Environ. Sci. Technol., 2004, vol. 34, pp. 249–289.CrossRefGoogle Scholar
  14. 14.
    Giordano, A., Stante, L., Pirozzi, F., Cesaro, R., and Bortone, G., Sequencing Batch Reactor Performance Treating PAH Contaminated Lagoon Sediments, J. Hazard. Materials, 2005, vol. 119, pp. 159–166.CrossRefGoogle Scholar
  15. 15.
    Quijano, G., Hernandez, M., Thalasso, F., Mu~noz, R., and Villaverde, S., Two-Phase Partitioning Bioreactors in Environmental Biotechnology, Appl. Microbiol. Biotechnol., 2009, vol. 84, pp. 829–846.PubMedCrossRefGoogle Scholar
  16. 16.
    Kathi, S. and Khan, A.B., Phytoremediation Approaches to PAH Contaminated Soil, Indian J. Sci. Technol., 2011, vol. 4, pp. 56–63.Google Scholar
  17. 17.
    Cerniglia, C.E., Fungal Metabolism of Polycyclic Aromatic Hydrocarbons: Past, Present and Future Applications in Bioremediation, J. Ind. Microbiol. Biotechnol., 1997, vol. 19, pp. 324–333.PubMedCrossRefGoogle Scholar
  18. 18.
    Mihelcic, J.R. and Luthy, R.G., Degradation of Polycyclic Aromatic Hydrocarbon Compounds under Various Redox Conditions in Soil-Water Systems, Appl. Environ. Microbiol., 1988, vol. 54, pp. 1182–1187.PubMedGoogle Scholar
  19. 19.
    Sharak Genthner, B.R., Townsend, G.T., Lantz, S.E., and Mueller, J.G., Persistence of Polycyclic Aromatic Hydrocarbon Components of Creosote under Anaerobic Enrichment Conditions, Arch. Environ. Contaminat. Toxicol., 1997, vol. 32, pp. 99–105.CrossRefGoogle Scholar
  20. 20.
    Eriksson, M., Sodersten, E., Yu, Z., and Dalhammar, G., Degradation of Polycyclic Aromatic Hydrocarbons at Low Temperature under Aerobic and Nitrate-Reducing Conditions in Enrichment Cultures from Northern Soils, Appl. Environ. Microbiol., 2003, vol. 69, pp. 275–284.PubMedCrossRefGoogle Scholar
  21. 21.
    Meckenstock, R.U., Safinowski, M., and Griebler, C., Anaerobic Degradation of Polycyclic Aromatic Hydrocarbons, FEMS Microbiol. Ecol., 2004, vol. 49, pp. 27–36.PubMedCrossRefGoogle Scholar
  22. 22.
    Luthy, R.D., Aiken, G.R., Brusseau, M.L., Cunningham, D.S., Gschwend, P.M., Pignatello, J.J., Reinhard, M., Traina, S.J., Weber, W.J., and Westall, J.C., Sequestration of Hydrophobic Organic Contaminants by Geosorbents, Environ. Sci. Technol., 1997, vol. 31, pp. 3341–3347.CrossRefGoogle Scholar
  23. 23.
    Alexander, M., Aging, Bioavailability, and Overestimation of Risk from Environmental Pollutants, Environ. Sci. Technol., 2000, vol. 34, pp. 4259–4265.CrossRefGoogle Scholar
  24. 24.
    Cornelissen, G., Gustafsson, Ö., Bucheli, T.D., Jonker, M.T.O., Koelmans, A.A., and VanNoort, P.C.M., Extensive Sorption of Organic Compounds to Black Carbon, Coal, and Kerogen in Sediments and Soils: Mechanisms and Consequences for Distribution, Bioaccumulation, and Biodegradation, Environ. Sci. Technol., 2005, vol. 39, pp. 6881–6895.PubMedCrossRefGoogle Scholar
  25. 25.
    Zhang, W.X., Bouwer, E.J., and Ball, W.P., Bioavailability of Hydrophobic Organic Contaminants: Effects and Implications of Sorption-Related Mass Transfer on Bioremediation, Ground Water Monit., 1998, vol. 18, pp. 126–138.CrossRefGoogle Scholar
  26. 26.
    Bouchez, M., Blanchet, D., and Vandecasteele, J.-P., Substrate Availability in Phenanthrene Biodegradation: Transfer Mechanism and Influence on Metabolism, Appl. Microbiol. Biotechnol., 1995, vol. 43, pp. 952–960.PubMedCrossRefGoogle Scholar
  27. 27.
    Volkering, F., Breure, A.M., van Andel, J.G., and Rulkens, W.H., Influence of Nonionic Surfactants on Bioavailability and Biodegradation of Polycyclic Aromatic Hydrocarbons, Appl. Environ. Microbiol., 1995, vol. 61, pp. 1699–1705.PubMedGoogle Scholar
  28. 28.
    Wick, L.Y., Colangelo, T., and Harms, H., Kinetics of Mass Transfer-Limited Bacterial Growth on Solid PAHs, Environ. Sci. Technol., 2001, vol. 35, pp. 354–361.PubMedCrossRefGoogle Scholar
  29. 29.
    Bouchez, M., Blanchet, D., and Vandecasteele, J.-P., An Interfacial Uptake Mechanism for the Degradation of Pyrene by a Rhodococcus Strain, Microbiology (UK), 1997, vol. 143, pp. 1087–1093.CrossRefGoogle Scholar
  30. 30.
    MacLeod, C.T. and Daugulis, A.J., Interfacial Effects in a Two-Phase Partitioning Bioreactor: Degradation of Polycyclic Aromatic Hydrocarbons (PAHs) by a Hydrophobic Mycobacterium, Process. Biochem., 2005, vol. 40, pp. 1799–1805.CrossRefGoogle Scholar
  31. 31.
    Vacca, D.J., Bleam, W.F., and Hickey, W.J., Isolation of Soil Bacteria Adapted to Degrade Humic Acid-Sorbed Phenanthrene, Appl. Environ. Microbiol., 2005, vol. 71, pp. 3797–3805.PubMedCrossRefGoogle Scholar
  32. 32.
    Xia, X., Li, Y., Zhou, Z., and Feng, C., Bioavailability of Adsorbed Phenanthrene by Black Carbon and Multi-Walled Carbon Nanotubes to Agrobacterium, Chemosphere, 2010, vol. 78, pp. 1329–1336.PubMedCrossRefGoogle Scholar
  33. 33.
    Stringfellow, W.T. and Aitken, M.D., Comparative Physiology of Phenanthrene Degradation by Two Dissimilar Pseudomonads Isolated from a Creosote Contaminated Soil, Can. J. Microbiol., 1994, vol. 40, pp. 432–438.PubMedCrossRefGoogle Scholar
  34. 34.
    Guha, S. and Jaffé, P.R., Biodegradation Kinetics of Phenanthrene Partitioned into the Micellar Phase of Nonionic Surfactants, Environ. Sci. Technol., 1996, vol. 30, pp. 605–611.CrossRefGoogle Scholar
  35. 35.
    Semple, K.T., Doick, K.J., Jones, K.C., Burauel, P., Craven, A., and Harms, H., Defining Bioavailability and Bioaccessibility of Contaminated Soil and Sediment Is Complicated, Environ. Sci. Technol., 2004, vol. 38, pp. 228–231.CrossRefGoogle Scholar
  36. 36.
    Bosma, R.M.P., Middeldorp, P.J.M., Schraa, G., and Zehnder, A.J.B., Mass Transfer Limitation of Biotransformation: Quantifying Bioavailability, Environ. Sci. Technol., 1997, vol. 31, pp. 248–252.CrossRefGoogle Scholar
  37. 37.
    Volkering, F., Breure, A.M., Sterkenburg, A., and van Andel, J.G., Microbial Degradation of Polycyclic Aromatic Hydrocarbons: Effect of Substrate Availability on Bacterial Growth Kinetics, Appl. Microbiol. Biotechnol., 1992, vol. 36, pp. 548–552.CrossRefGoogle Scholar
  38. 38.
    Yamane, T. and Shimizu, S., Fed-Batch Techniques in Microbial Processes, Adv. Biochem. Eng./Biotechnol., 1984, vol. 30, pp. 147–194.CrossRefGoogle Scholar
  39. 39.
    Panikov, N.S., Microbial Growth Kinetics, London: Chapman & Hall, 1995.Google Scholar
  40. 40.
    Johnsen, A.R., Wick, L.Y., and Harms, H., Principles of Microbial PAH Degradation in Soil, Environ. Pollut., 2005, vol. 133, pp. 71–84.PubMedCrossRefGoogle Scholar
  41. 41.
    Reichenberg, F. and Mayer, P., Two Complementary Sides of Bioavailability: Accessibility and Chemical Activity of Organic Contaminants in Sediments and Soils, Environ. Toxicol. Chem., 2006, vol. 25, pp. 1239–1245.PubMedCrossRefGoogle Scholar
  42. 42.
    Déziel, E., Comeau, Y., and Villemur, R., Two-Liquid-Phase Bioreactors for Enhanced Degradation of Hydrophobic/Toxic Compounds, Biodegradation, 1999, vol. 10, pp. 219–233.PubMedCrossRefGoogle Scholar
  43. 43.
    Wick, L.Y., Ruiz de Munain, A., Springael, D., and Harms, H., Responses of Mycobacterium sp. LB501T to the Low Bioavailability of Solid Anthracene, Appl. Microbiol. Biotechnol., 2002, vol. 58, pp. 378–385.PubMedCrossRefGoogle Scholar
  44. 44.
    Wick, L.Y., Pelz, O., Bernasconi, S.M., Andersen, N., and Harms, H., Influence of the Growth Substrate on Ester-Linked Phospho- and Glycolipid Fatty Acids of Mycobacterium sp. LB501T, Environ. Microbiol., 2003, vol. 5, pp. 672–680.PubMedCrossRefGoogle Scholar
  45. 45.
    Grimm, A.C. and Harwood, C.S., Chemotaxis of Pseudomonas sp. to the Polyaromatic Hydrocarbon, Naphthalene, Appl. Environ. Microbiol., 1997, vol. 63, pp. 4111–4115.PubMedGoogle Scholar
  46. 46.
    Christofi, N. and Ivshina, I.B., Microbial Surfactants and Their Use in Field Studies of Soil Remediation, J. Appl. Microbiol., 2002, pp. 915–929.Google Scholar
  47. 47.
    Banat, I.M., Franzetti, A., Gandolfi, I., Bestetti, G., Martinotti, M.G., Fracchia, L., Smyth, T.J., and Marchant, R., Microbial Biosurfactants Production, Applications and Future Potential, Appl. Microbiol. Biotechnol., 2010, vol. 87, pp. 427–444.PubMedCrossRefGoogle Scholar
  48. 48.
    Makkar, R.S. and Rockne, K.J., Comparison of Synthetic Surfactants and Biosurfactants in Enhancing Biodegradation of Polycyclic Aromatic Hydrocarbons, Environ. Toxicol. Chem., 2003, vol. 22, pp. 2280–2292.PubMedCrossRefGoogle Scholar
  49. 49.
    Whitman, B.E., Lueking, D.R., and Mihelcic, J.R., Naphthalene Uptake by a Pseudomonas fluorescens Isolate, Can. J. Microbiol., 1998, vol. 44, pp. 1086–1093.PubMedGoogle Scholar
  50. 50.
    Miyata, N., Iwahori, K., Foght, J.M., and Gray, M.R., Saturable, Energy-Dependent Uptake of Phenanthrene in Aqueous Phase by Mycobacterium sp. Strain RJGII-135, Appl. Environ. Microbiol., 2004, vol. 70, pp. 363–369.PubMedCrossRefGoogle Scholar
  51. 51.
    Bugg, T., Foght, J.M., Pickard, M.A., and Gray, M.R., Uptake and Active Efflux of Polycyclic Aromatic Hydrocarbons by Pseudomonas fluorescens LP6a, Appl. Environ. Microbiol., 2000, vol. 66, pp. 5387–5392.PubMedCrossRefGoogle Scholar
  52. 52.
    Hearn, E.M., Dennis, J.J., Gray, M.R., and Foght, J.M., Identification and Characterization of the emhABC Efflux System for Polycyclic Aromatic Hydrocarbons in Pseudomonas fluorescens cLP6a, J. Bacteriol., 2003, vol. 185, pp. 6233–6240.PubMedCrossRefGoogle Scholar
  53. 53.
    Adebusuyi, A.A. and Foght, J.M., An Alternative Physiological Role for the EmhABC Efflux Pump in Pseudomonas fluorescens cLP6a, BMC Microbiol., 2011, vol. 11, p. 252.Google Scholar
  54. 54.
    Ferraro, D.J., Gakhar, L., and Ramaswamy, S., Rieske Business: Structure-Function of Rieske Non-Heme Oxygenases, Biochem. Biophys. Res. Commun., 2005, vol. 338, pp. 175–190.PubMedCrossRefGoogle Scholar
  55. 55.
    Chadhain, S.M.N., Norman, R.S., Pesce, K.V., Kukor, J.J., and Zylstra, G.J., Microbial Dioxygenase Gene Population Shifts during Polycyclic Aromatic Hydrocarbon Biodegradation, Appl. Environ. Microbiol., 2006, vol. 72, pp. 4078–4087.CrossRefGoogle Scholar
  56. 56.
    Moser, R. and Stahl, U., Insights into the Genetic Diversity of Initial Dioxygenases from PAH-Degrading Bacteria, Appl. Microbiol. Biotechnol., 2001, vol. 609–618.Google Scholar
  57. 57.
    Zhou, H.W., Guo, C.L., Wong, Y.S., and Tam, N.F.Y., Genetic Diversity of Dioxygenase Genes in Polycyclic Aromatic Hydrocarbon-Degrading Bacteria Isolated from Mangrove Sediments, FEMS Microbiol. Lett., 2006, vol. 262, pp. 148–157.PubMedCrossRefGoogle Scholar
  58. 58.
    Iwai, S., Johnson, T.A., Chai, B., Hashsham, S.A., and Tiedje, J.M., Comparison of the Specificities and Efficacies of Primers for Aromatic Dioxygenase Gene Analysis of Environmental Samples, Appl. Environ. Microbiol., 2011, vol. 77, pp. 3551–3557.PubMedCrossRefGoogle Scholar
  59. 59.
    Na, K.S., Kuroda, A., Takiguchi, N., Ikeda, T., Ohtake, H., and Kato, J., Isolation and Characterization of Benzene-Tolerant Rhodococcus opacus Strains, J. Biosci. Bioeng., 2005, vol. 99, pp. 378–382.PubMedCrossRefGoogle Scholar
  60. 60.
    Eaton, R.W. and Timmis, K.N., Characterization of a Plasmid-Specified Pathway for Catabolism of Isopropylbenzene in Pseudomonas putida RE204, J. Bacteriol., 1986, vol. 168, pp. 123–131.PubMedGoogle Scholar
  61. 61.
    Dong, X., Fushinobu, S., Fukuda, E., Terada, T., Nakamura, S., Shimizu, K., Nojiri, H., Omori, T., Shoun, H., and Wakagi, T., Crystal Structure of the Terminal Oxygenase Component of Cumene Dioxygenase from Pseudomonas fluorescens IP01, J. Bacteriol., 2005, vol. 187, pp. 2483–2490.PubMedCrossRefGoogle Scholar
  62. 62.
    Beil, S., Happe, B., Timmis, K.N., and Pieper, D.H., Genetic and Biochemical Characterization of the Broad Spectrum Chlorobenzene Dioxygenase from Burkholderia sp. Strain PS12-Dechlorination of 1,2,4,5-Tetrachlorobenzene, Eur. J. Biochem., 1997, vol. 247, pp. 190–199.PubMedCrossRefGoogle Scholar
  63. 63.
    Jiang, X.W., Liu, H., Xu, Y., Wang, S.J., Leak, D.J., and Zhou, N.Y., Genetic and Biochemical Analyses of Chlorobenzene Degradation Gene Clusters in Pandoraea sp. Strain MCB032, Arch. Microbiol., 2009, vol. 191, pp. 485–492.PubMedCrossRefGoogle Scholar
  64. 64.
    Kulkarni, M. and Chaudhari, A., Microbial Remediation of Nitro-Aromatic Compounds: An Overview, J. Environ. Management, 2007, vol. 85, pp. 496–512.CrossRefGoogle Scholar
  65. 65.
    Ang, E.L., Obbard, J.P., and Zhao, H., Directed Evolution of Aniline Dioxygenase for Enhanced Bioremediation of Aromatic Amines, Appl. Microbiol. Biotechnol., 2009, vol. 81, pp. 1063–1070.PubMedCrossRefGoogle Scholar
  66. 66.
    Furukawa, K., Suenaga, H., and Goto, M., Biphenyl Dioxygenases: Functional Versatilities and Directed Evolution, J. Bacteriol., 2004, vol. 186, pp. 5189–5196.PubMedCrossRefGoogle Scholar
  67. 67.
    Pieper, D.H. and Seeger, M., Bacterial Metabolism of Polychlorinated Biphenyls, J. Mol. Microbiol. Biotechnol., 2008, vol. 15, pp. 121–138.PubMedCrossRefGoogle Scholar
  68. 68.
    Bundy, B.M., Campbell, A.L., and Neidle, E.L., Similarities between the antABC-Encoded Anthranilate Dioxygenase and the benABC-Encoded Benzoate Dioxygenase of Acinetobacter sp. Strain ADP1, J. Bacteriol., 1998, vol. 180, pp. 4466–4474.PubMedGoogle Scholar
  69. 69.
    Eaton, R.W., Plasmid-Encoded Phthalate Catabolic Pathway in Arthrobacter keyseri 12B, J. Bacteriol., 2001, vol. 183, pp. 3689–3703.PubMedCrossRefGoogle Scholar
  70. 70.
    Bressler, D.C. and Fedorak, P.M., Bacterial Metabolism of Fluorene, Dibenzofuran, Dibenzothiophene, and Carbazole, Can. J. Microbiol., 2000, vol. 46, pp. 397–409.PubMedCrossRefGoogle Scholar
  71. 71.
    Gibson, D.T. and Parales, R.E., Aromatic Hydrocarbon Dioxygenases in Environmental Biotechnology, Curr. Opin. Biotechnol., 2000, vol. 11, pp. 236–243.PubMedCrossRefGoogle Scholar
  72. 72.
    Nam, J.W., Nojiri, H., Yoshida, T., Habe, H., Yamane, H., and Omori, T., New Classification System for Oxygenase Components Involved in RingHydroxylating Oxygenations, Boisci. Biotechnol. Biochem., 2001, vol. 65, pp. 254–263.CrossRefGoogle Scholar
  73. 73.
    Pérez-Pantoja, D., González, B., and Pieper, D.H., Aerobic Degradation of Aromatic Hydrocarbons, in Handbook of Hydrocarbon and Lipid Microbiology, Timmis, K.N., Ed., Berlin: Springer, 2010, pp. 800–837.Google Scholar
  74. 74.
    Kweon, O., Kim, S.J., Baek, S., Chae, J.C., Adjei, M.D., Baek, D.H., Kim, Y.C., and Cerniglia, C.E., A New Classification System for Bacterial Rieske Non-Heme Iron Aromatic Ring-Hydroxylating Oxygenases, BMC Biochem., 2008, vol. 9, p. 11.PubMedCrossRefGoogle Scholar
  75. 75.
    Notredame, C., Higgins, D.G., and Heringa, J., T-Coffee: A Novel Method for Fast and Accurate Multiple Sequence Alignment, J. Mol. Biol., 2000, vol. 205–217.Google Scholar
  76. 76.
    Van de Peer, Y. and De Wachter, R., Construction of Evolutionary Distance Trees with TREECON, Comput. Applic. Biosci., 1997, vol. 13, pp. 227–230.Google Scholar
  77. 77.
    Suen, W.-C., Haigler, B.E., and Spain, J.C., 2,4-Dinitrotoluene Dioxygenase from Burkholderia sp. Strain DNT: Similarity to Naphthalene Dioxygenase, J. Bacteriol., 1996, vol. 178, pp. 4926–4934.PubMedGoogle Scholar
  78. 78.
    Lessner, D.J., Johnson, G.R., Parales, R.E., Spain, J.C., and Gibson, D.T., Molecular Characterization and Substrate Specificity of Nitrobenzene Dioxygenase from Comamonas sp. Strain JS765, Appl. Environ. Microbiol., 2002, vol. 68, pp. 634–641.PubMedCrossRefGoogle Scholar
  79. 79.
    Kimura, N., Kitagawa, W., Mori, T., Nakashima, N., Tamura, T., and Kamagata, Y., Genetic and Biochemical Characterization of the Dioxygenase Involved in Lateral Dioxygenation of Dibenzofuran from Rhodococcus opacus Strain SAO101, Appl. Microbiol. Biotechnol., 2006, vol. 73, pp. 474–484.PubMedCrossRefGoogle Scholar
  80. 80.
    Kasai, Y., Shindo, K., Harayama, S., and Misawa, N., Molecular Characterization and Substrate Preference of a Polycyclic Aromatic Hydrocarbon Dioxygenase from Cycloclasticus sp. Strain A5, Appl. Environ. Microbiol., 2003, vol. 69, pp. 6688–6697.PubMedCrossRefGoogle Scholar
  81. 81.
    Pagnout, C., Frache, G., Poupin, P., Maunit, B., Muller, J.F., and Ferard, J.F., Isolation and Characterization of a Gene Cluster Involved in PAH Degradation in Mycobacterium sp. Strain SNP11: Expression in Mycobacterium smegmatis mc2155, Res. Microbiol., 2007, vol. 158, pp. 175–186.PubMedCrossRefGoogle Scholar
  82. 82.
    Schuler, L., Jouanneau, Y., Chadhain, S.M.N., Meyer, C., Pouli, M., Zylstra, G.J., Hols, P., and Agathos, S.N., Characterization of a Ring-Hydroxylating Dioxygenase from Phenanthrene-Degrading Sphingomonas sp. Strain LH128 Able to Oxidize Benz[a]anthracene, Appl. Microbiol. Biotechnol., 2009, vol. 83, pp. 465–475.PubMedCrossRefGoogle Scholar
  83. 83.
    Chadhain, S.M.N., Moritz, E.M., Kim, E., and Zylstra, G.J., Identifcation, Cloning, and Characterization of a Multicomponent Biphenyl Dioxygenase from Sphingobium yanoikuyae B1, J. Ind. Microbiol. Biotechnol., 2007, vol. 34, pp. 605–613.PubMedCrossRefGoogle Scholar
  84. 84.
    Jouanneau, Y., Meyer, C., Jakoncic, J., Stojanoff, V., and Gaillard, J., Characterization of a Naphthalene Dioxygenase Endowed with an Exceptionally Broad Substrate Specificity toward Polycyclic Aromatic Hydrocarbons, Biochemistry, 2006, vol. 45, pp. 12380–12391.PubMedCrossRefGoogle Scholar
  85. 85.
    Kauppi, B., Lee, K., Carredano, E., Parales, R.E., Gibson, D.T., Eklund, H., and Ramaswamy, S., Structure of an Aromatic-Ring-Hydroxylating Dioxygenase-Naphthalene 1,2-Dioxygenase, Structure, 1998, vol. 6, pp. 571–586.PubMedCrossRefGoogle Scholar
  86. 86.
    Gakhar, L., Malik, Z.A., Allen, C.C., Lipscomb, D.A., Larkin, M.J., and Ramaswamy, S., Structure and Increased Thermostability of Rhodococcus sp. Naphthalene 1,2-Dioxygenase, J. Bacteriol., 2005, vol. 187, pp. 7222–7231.PubMedCrossRefGoogle Scholar
  87. 87.
    Ferraro, D.J., Brown, E.N., Yu, C.-L., Parales, R.E., Gibson, D.T., and Ramaswamy, S., Structural Investigations of the Ferredoxin and Terminal Oxygenase Components of the Biphenyl 2,3-Dioxygenase from Sphingobium yanoikuyae B1, BMC Structural Biol., 2007, vol. 7, p. 10.CrossRefGoogle Scholar
  88. 88.
    Jakoncic, J., Jouanneau, Y., Meyer, C., and Stojanoff, V., The Catalytic Pocket of the Ring-Hydroxylating Dioxygenase from Sphingomonas CHY-1, Biochem. Biophys. Res. Commun., 2007, vol. 352, pp. 861–866.PubMedCrossRefGoogle Scholar
  89. 89.
    Kweon, O., Kim, S.-J., Freeman, J.P., Song, J., Baek, S., and Cerniglia, C.E., Substrate Specificity and Structural Characteristics of the Novel Rieske Nonheme Iron Aromatic Ring-Hydroxylating Oxygenases NidAB and NidA3B3 from Mycobacterium vanbaalenii PYR-1, mBio, 2010, vol. 1. doi: 10.1128/mBio.00135-10Google Scholar
  90. 90.
    Resnick, S.M., Lee, K., and Gibson, D.T., Diverse Reactions Catalyzed by Naphthalene Dioxygenase from Pseudomonas sp. Strain NCIB 9816, J. Ind. Microbiol., 1996, vol. 17, pp. 438–457.CrossRefGoogle Scholar
  91. 91.
    Pinyakong, O., Habe, H., Kouzuma, A., Nojiri, H., Yamane, H., and Omori, T., Isolation and Characterization of Genes Encoding Polycyclic Aromatic Hydrocarbon Dioxygenase from Acenaphthene and Acenaphthylene Degrading Sphingomonas sp. Strain A4, FEMS Microbiol. Lett., 2004, vol. 238, pp. 297–305.PubMedGoogle Scholar
  92. 92.
    Krivobok, S., Kuony, S., Meyer, C., Louwagie, M., Willison, J.C., and Jouanneau, Y., Identification of Pyrene-Induced Proteins in Mycobacterium sp. Strain 6PY1: Evidence for Two Ring-Hydroxylating Dioxygenases, J. Bacteriol., 2003, vol. 185, pp. 3828–3841.PubMedCrossRefGoogle Scholar
  93. 93.
    Ferraro, D.J., Okerlund, A.L., Mowers, J.C., and Ramaswamy, S., Structural Basis for Regioselectivity and Stereoselectivity of Product Formation by Naphthalene 1,2-Dioxygenase, J. Bacteriol., 2006, vol. 188, pp. 6986–6994.PubMedCrossRefGoogle Scholar
  94. 94.
    Kim, S.-J., Kweon, O., Freeman, J.P., Jones, R.C., Adjei, M.D., Jhoo, J.-W., Edmondson, R.D., and Cerniglia, C.E., 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., 2006, vol. 72, pp. 1045–1054.PubMedCrossRefGoogle Scholar
  95. 95.
    Boyd, D.R. and Bugg, T.D.H., Arene cis-Dihydrodiol Formation: From Biology to Application, Org. Biomol. Chem., 2006, vol. 4, pp. 181–192.PubMedCrossRefGoogle Scholar
  96. 96.
    Kacser, H. and Burns, J.A., The Control of Flux, Symp. Soc. Exp. Biol., 1973, vol. 27, pp. 65–104.PubMedGoogle Scholar
  97. 97.
    Westerhoff, H.V. and van Dam, K., Thermodynamics and Control of Biological Free-Energy Transduction, Amsterdam: Elsevier, 1987.Google Scholar
  98. 98.
    Cornish-Bowden, A., Fundamentals of Enzyme Kinetics, 3rd ed., London: Portland, 2004.Google Scholar
  99. 99.
    Dimitriou-Christidis, P., Autenrieth, R.L., McDonald, T.J., and Desai, A.M., Measurement of Biodegradability Parameters for Single Unsubstituted and Methylated Polycyclic Aromatic Hydrocarbons in Liquid Bacterial Suspensions, Biotechnol. Bioeng., 2007, vol. 97, pp. 922–932.PubMedCrossRefGoogle Scholar
  100. 100.
    Baboshin, M.A. and Golovleva, L.A., Multisubstrate Kinetics of PAH Mixture Biodegradation: Analysis in the Double-Logarithmic Plot, Biodegradation, 2011, vol. 22, pp. 13–23.PubMedCrossRefGoogle Scholar
  101. 101.
    Knightes, C.D. and Peters, C.A., Aqueous Phase Biodegradation Kinetics of 10 PAH Compounds, Environ. Eng. Sci., 2003, vol. 20, pp. 207–218.CrossRefGoogle Scholar
  102. 102.
    Stringfellow, W.T. and Aitken, M.D., Competitive Metabolism of Naphthalene, Methylnaphthalene and Fluorene by Phenanthrene-Degrading Pseudomonads, Appl. Environ. Microbiol., 1995, vol. 61, pp. 357–362.PubMedGoogle Scholar
  103. 103.
    Guha, S., Peters, C.A., and Jaffé, P.R., Multisubstrate Biodegradation Kinetics of Naphthalene, Phenanthrene, and Pyrene Mixtures, Biotechnol. Bioeng., 1999, vol. 65, pp. 491–499.PubMedCrossRefGoogle Scholar
  104. 104.
    Lotfabad, S.K. and Gray, M.R., Kinetics of Biodegradation Mixtures of Polycyclic Aromatic Hydrocarbons, Appl. Microbiol. Biotechnol., 2002, vol. 60, pp. 361–366.PubMedCrossRefGoogle Scholar
  105. 105.
    Knightes, C.D. and Peters, C.A., Multisubstrate Biodegradation Kinetics for Binary and Complex Mixtures of Polycyclic Aromatic Hydrocarbons, Environ. Toxicol. Chem., 2006, vol. 25, pp. 1746–1756.PubMedCrossRefGoogle Scholar
  106. 106.
    Dimitriou-Christidis, P. and Autenrieth, R.L., Kinetics of Biodegradation of Binary and Ternary Mixtures of PAHs, Biotechnol. Bioeng., 2007, vol. 97, pp. 788–800.PubMedCrossRefGoogle Scholar
  107. 107.
    Desai, A.M., Autenrieth, R.L., Dimitriou-Christidis, P., and McDonald, T.J., Biodegradation Kinetics of Select Polycyclic Aromatic Hydrocarbon (PAH) Mixtures by Sphingomonas paucimobilis EPA505, Biodegradation, 2008, vol. 19, pp. 223–233.PubMedCrossRefGoogle Scholar
  108. 108.
    Peng, R.-H., Xiong, A.-S., Xue, Y., Fu, X.-Y., Gao, F., Zhao, W., Tian, Y.-S., and Yao, Q.-H., Microbial Biodegradation of Polyaromatic Hydrocarbons, FEMS Microbiol. Rev., 2008, vol. 32, pp. 927–955.PubMedCrossRefGoogle Scholar
  109. 109.
    Seo, J.-S., Keum, Y.-S., and Li, Q.X., Bacterial Degradation of Aromatic Compounds, Int. J. Environ. Res. Public Health, 2009, vol. 6, pp. 278–309.PubMedCrossRefGoogle Scholar
  110. 110.
    Kanaly, R.A. and Harayama, S., Advances in the Field of High-Molecular-Weight Polycyclic Aromatic Hydrocarbon Biodegradation by Bacteria, Microb. Biotechnol., 2010, vol. 3, pp. 136–164.PubMedCrossRefGoogle Scholar
  111. 111.
    VanBriesen, J.M. and Rittmann, B.E., Mathematical Description of Microbiological Reactions Involving Intermediates, Biotechnol. Bioeng., 2000, vol. 67, pp. 35–52.PubMedCrossRefGoogle Scholar
  112. 112.
    Baboshin, M.A. and Golovleva, L.A., Characterization of Hydrophobic Organic Contaminant Biodegradation by COD Analysis, Int. Biodeterior. Biodegr., 2011, vol. 65, pp. 883–889.CrossRefGoogle Scholar
  113. 113.
    Bouchez, M., Blanchet, D., and Vandecasteele, J.-P., The Microbiological Fate of Polycyclic Aromatic Hydrocarbons: Carbon and Oxygen Balances for Bacterial Degradation of Model Compounds, Appl. Microbiol. Biotechnol., 1996, vol. 45, pp. 556–561.PubMedCrossRefGoogle Scholar
  114. 114.
    Annweiler, E., Richnow, H.H., Antranikian, G., Hebenbrock, S., Garms, C., Franke, S., Franke, W., and Michaelis, W., Naphthalene Degradation and Incorporation of Naphthalene-Derived Carbon into Biomass by the Thermophile Bacillus thermoleovorans, Appl. Environ. Microbiol., 2000, vol. 66, pp. 518–523.PubMedCrossRefGoogle Scholar
  115. 115.
    Kazunga, C. and Aitken, M.D., Products of Incomplete Metabolism of Pyrene by Polycyclic Aromatic Hydrocarbon-Degrading Bacteria, Appl. Environ. Microbiol., 2000, vol. 66, pp. 1917–1922.PubMedCrossRefGoogle Scholar
  116. 116.
    Kazunga, C., Aitken, M.D., Gold, A., and Sangaiah, R., Fluoranthene-2,3- and -1,5-Diones Are Novel Products from the Bacterial Transformation of Fluoranthene, Environ. Sci. Technol., 2001, vol. 35, pp. 917–922.PubMedCrossRefGoogle Scholar
  117. 117.
    Lundstedt, S., White, P.A., Lemieux, C.L., Lynes, K.D., Lambert, I.B., Öberg, L., Haglund, P., and Tysklind, M., Sources, Fate, and Toxic Hazards of Oxygenated Polycyclic Aromatic Hydrocarbons (PAHs) at PAH-Contaminated Sites, AMBIO, 2007, vol. 36, pp. 475–485.PubMedCrossRefGoogle Scholar
  118. 118.
    Kang, H., Hwang, S.Y., Kim, Y.M., Kim, E., Kim, Y.-S., Kim, S.-K., Kim, S.W., Cerniglia, C.E., Shuttleworth, K.L., and Zylstra, G.J., Degradation of Phenanthrene and Naphthalene by a Burkholderia Species Strain, Can. J. Microbiol., 2003, vol. 49, pp. 139–144.PubMedCrossRefGoogle Scholar
  119. 119.
    Baboshin, M.A., Akimov, V.N., Baskunov, B.P., Born, T.L., Khan, S.U., and Golovleva, L.A., Conversion of Polycyclic Aromatic Hydrocarbons by Sphingomonas sp. VKM B-2434, Biodegradation, 2008, vol. 19, pp. 567–576.PubMedCrossRefGoogle Scholar
  120. 120.
    Casellas, M., Grifoll, M., Sebate, J., and Solanas, A.M., Isolation and Characterization of a Fluorenone-Degrading Bacterial Strain and Its Role in Synergistic Degradation of Fluorene by a Consortium, Can. J. Microbiol., 1998, vol. 44, pp. 734–742.Google Scholar
  121. 121.
    Baboshin, M.A. and Golovleva, L.A., Increase of 1-Hydroxy-2-Naphthoic Acid Concentration as a Cause of Temporary Cessation of Growth for Arthrobacter sp. K3: Kinetic Analysis, Microbiology, 2009, vol. 78, pp. 180–186.CrossRefGoogle Scholar
  122. 122.
    Baboshin, M.A. and Golovleva, L.A., The Strategy of Strain Selection for a Mixed Culture Performing Rapid Conversion of a Mixture of Polyaromatic Compounds, Microbiology, 2010, vol. 79, pp. 73–82.CrossRefGoogle Scholar
  123. 123.
    Molina, M., Araujo, R., and Hodson, R.E., Cross-Induction of Pyrene and Phenanthrene in a Mycobacterium sp. Isolated from Polycyclic Aromatic Hydrocarbon Contaminated River Sediments, Can. J. Microbiol., 1999, vol. 45, pp. 520–529.PubMedGoogle Scholar
  124. 124.
    Bouchez, M., Blanchet, D., and Vandecasteele, V.-P., Degradation of Polycyclic Aromatic Hydrocarbons by Pure Strains and by Defined Strain Associations: Inhibition Phenomena and Cometabolism, Appl. Microbiol. Biotechnol., 1995, vol. 43, pp. 156–164.PubMedCrossRefGoogle Scholar
  125. 125.
    Juhasz, A.L. and Naidu, R., Bioremediation of High Molecular Weight Polycyclic Aromatic Hydrocarbons: A Review of Microbial Degradation of Benzo[a]pyrene, Int. Biodeterior. Biodegr., 2000, vol. 45, pp. 57–88.CrossRefGoogle Scholar
  126. 126.
    Boonchan, S., Britz, M.L., and Stanley, G.A., Degradation and Mineralization of High-Molecular-Weight Polycyclic Aromatic Hydrocarbons by Defined Fungal Bacterial Cocultures, Appl. Environ. Microbiol., 2000, vol. 66, pp. 1007–1019.PubMedCrossRefGoogle Scholar
  127. 127.
    Kanaly, R.A., Bartha, R., Watanabe, K., and Harayama, S., Rapid Mineralization of Benzo[a]pyrene by a Microbial Consortium Growing on Diesel Fuel, Appl. Environ. Microbiol., 2000, vol. 66, pp. 4205–4211.PubMedCrossRefGoogle Scholar
  128. 128.
    Bouchez, M., Blanchet, D., Bardin, V., Haeseler, F., and Vandecasteele, J.-P., Efficiency of Defined Strains and of Soil Consortia in the Biodegradation of Polycyclic Aromatic Hydrocarbon (PAH) Mixtures, Biodegradation, 1999, vol. 10, pp. 429–435.PubMedCrossRefGoogle Scholar
  129. 129.
    Odum, E.P., Basic Ecology Philadelphia: Saunders College, 1983.Google Scholar
  130. 130.
    Röling, W.F.M., van Breukelen, B.M., Bruggeman, F.J., and Westerhoff, H.V., Ecological Control Analysis: Being(s) in Control of Mass Flux and Metabolite Concentrations in Anaerobic Degradation Processes, Environ. Microbiol., 2007, vol. 9, pp. 500–511.PubMedCrossRefGoogle Scholar
  131. 131.
    Rastogi, G. and Sani, R.K., Molecular Techniques to Assess Microbial Community Structure, Function, and Dynamics in the Environment, in Microbes and Microbial Technology: Agricultural and Environmental Applications, Ahmad, I., Ahmad, F., and Pichtel, J., Eds., Springer, 2011, pp. 29–57.Google Scholar
  132. 132.
    Jeon, C.O., Park, W., Padmanabhan, P., DeRito, C., Snape, J.R., and Madsen, E.L., Discovery of a Bacterium, with Distinctive Dioxygenase, that Is Responsible for in situ Biodegradation in Contaminated Sediment, Proc. Natl. Acad. Sci. USA, 2003, vol. 100, pp. 13591–13596.PubMedCrossRefGoogle Scholar
  133. 133.
    Yu, C.P. and Chu, K.H., A Quantitative Assay for Linking Microbial Community Function and Structure of a Naphthalene-Degrading Microbial Consortium, Environ. Sci. Technol., 2005, vol. 39, pp. 9611–9619.PubMedCrossRefGoogle Scholar
  134. 134.
    Singleton, D.R., Powell, S.N., Sangaiah, R., Gold, A., Ball, L.M., and Aitken, M.D., Stable-Isotope Probing of Bacteria Capable of Degrading Salicylate, Naphthalene, or Phenanthrene in a Bioreactor Treating Contaminated Soil, Appl. Environ. Microbiol., 2005, vol. 71, pp. 1202–1209.PubMedCrossRefGoogle Scholar
  135. 135.
    Singleton, D.R., Sangaiah, R., Gold, A., Ball, L.M., and Aitken, M.D., Identification and Quantification of Uncultivated Proteobacteria Associated with Pyrene Degradation in a Bioreactor Treating PAH Contaminated Soil, Environ. Microbiol., 2006, vol. 8, pp. 1736–1745.PubMedCrossRefGoogle Scholar
  136. 136.
    Jones, M.D., Crandell, D.W., Singleton, D.R., and Aitken, M.D., Stable-Isotope Probing of the Polycyclic Aromatic Hydrocarbon-Degrading Bacterial Guild in a Contaminated Soil, Environ. Microbiol., 2011, vol. 13, pp. 2623–2632.PubMedCrossRefGoogle Scholar
  137. 137.
    Zhang, S., Wan, R., Wang, Q., and Xie, S., Identification of Anthracene Degraders in Leachate-Contaminated Aquifer Using Stable Isotope Probing, Int. Biodeterior. Biodegr., 2001, vol. 65, pp. 1224–1228.CrossRefGoogle Scholar
  138. 138.
    Singleton, D.R., Ramirez, L.G., and Aitken, M.D., Characterization of a Polycyclic Aromatic Hydrocarbon Degradation Gene Cluster in a Phenanthrene-Degrading Acidovorax Strain, Appl. Environ. Microbiol., 2009, vol. 75, pp. 2613–2620.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2012

Authors and Affiliations

  1. 1.Skryabin Institute of Biochemistry and Physiology of MicroorganismsRussian Academy of SciencesPushchino, Moscow oblastRussia

Personalised recommendations