Advertisement

Degradation of Polycyclic Aromatic Hydrocarbons by Fungi

  • C. E. Cerniglia
  • J. B. Sutherland

Abstract:

Many fungi metabolize polycyclic aromatic hydrocarbons with enzymes that include lignin peroxidase, manganese peroxidase, laccase, cytochrome P450, and epoxide hydrolase. The products include trans-dihydrodiols, phenols, quinones, dihydrodiol epoxides, and tetraols, which may be conjugated to form glucuronides, glucosides, xylosides, and sulfates. The fungal metabolites generally are less toxic than the parent hydrocarbons. Cultures of fungi that degrade polycyclic aromatic hydrocarbons may be useful for bioremediation of contaminated soils, sediments, and waters.

Keywords

Pleurotus Ostreatus Trametes Versicolor High Molecular Weight PAHs Ligninolytic Fungus Irpex Lacteus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Diana Mathews and Sherry Terry for secretarial assistance. The views presented in this article do not necessarily reflect those of the Food and Drug Administration.

References

  1. Andersson BE, Henrysson T (1996) Accumulation and degradation of dead-end metabolites during treatment of soil contaminated with polycyclic aromatic hydrocarbons with five strains of white-rot fungi. Appl Microbiol Biotechnol 46: 647–652.Google Scholar
  2. Andersson BE, Lundstedt S, Tornberg K, Schnürer Y, Öberg LG, Mattiasson B (2003) Incomplete degradation of polycyclic aromatic hydrocarbons in soil inoculated with wood-rotting fungi and their effect on the indigenous soil bacteria. Environ Toxicol Chem 22: 1238–1243.PubMedGoogle Scholar
  3. Anh DH, Ullrich R, Benndorf D, Svatoś A, Muck A, Hofrichter M (2007) The coprophilous mushroom Coprinus radians secretes a haloperoxidase that catalyzes aromatic peroxygenation. Appl Environ Microbiol 73: 5477–5485.PubMedGoogle Scholar
  4. Anyakora C (ed.) (2007) Environmental Impact of Polynuclear Aromatic Hydrocarbons. Kerala: Research Signpost.Google Scholar
  5. Atlas RM, Cerniglia CE (1995) Bioremediation of petroleum pollutants: diversity and environmental aspects of hydrocarbon biodegradation. BioScience 45: 332–339.Google Scholar
  6. Baborová P, Möder M, Baldrian P, Cajthamlová K, Cajthaml T (2006) Purification of a new manganese peroxidase of the white-rot fungus Irpex lacteus, and degradation of polycyclic aromatic hydrocarbons by the enzyme. Res Microbiol 157: 248–253.PubMedGoogle Scholar
  7. Baldrian P, in der Wiesche C, Gabriel J, Nerud F, Zadražil F (2000) Influence of cadmium and mercury on activities of ligninolytic enzymes and degradation of polycyclic aromatic hydrocarbons by Pleurotus ostreatus in soil. Appl Environ Microbiol 66: 2471–2478.PubMedGoogle Scholar
  8. Barclay CD, Farquhar GF, Legge RL (1995) Biodegradation and sorption of polyaromatic hydrocarbons by Phanerochaete chrysosporium. Appl Microbiol Biotechnol 42: 958–963.PubMedGoogle Scholar
  9. Bezalel L, Hadar Y, Cerniglia CE (1996a) Mineralization of polycyclic aromatic hydrocarbons by the white rot fungus Pleurotus ostreatus. Appl Environ Microbiol 62: 292–295.PubMedGoogle Scholar
  10. Bezalel L, Hadar Y, Cerniglia CE (1997) Enzymatic mechanisms involved in phenanthrene degradation by the white rot fungus Pleurotus ostreatus. Appl Environ Microbiol 63: 2495–2501.PubMedGoogle Scholar
  11. Bezalel L, Hadar Y, Fu PP, Freeman JP, Cerniglia CE (1996b) Metabolism of phenanthrene by the white rot fungus Pleurotus ostreatus. Appl Environ Microbiol 62: 2547–2553.PubMedGoogle Scholar
  12. Bezalel L, Hadar Y, Fu PP, Freeman JP, Cerniglia CE (1996c) Initial oxidation products in the metabolism of pyrene, anthracene, fluorene, and dibenzothiophene by the white rot fungus Pleurotus ostreatus. Appl Environ Microbiol 62: 2554–2559.PubMedGoogle Scholar
  13. Bhatt M, Cajthaml T, Šašek V (2002) Mycoremediation of PAH-contaminated soil. Folia Microbiol 47: 255–258.Google Scholar
  14. Bogan BW, Lamar RT (1996) Polycyclic aromatic hydrocarbon-degrading capabilities of Phanerochaete laevis HHB-1625 and its extracellular ligninolytic enzymes. Appl Environ Microbiol 62: 1597–1603.PubMedGoogle Scholar
  15. Bogan BW, Lamar RT, Burgos WD, Tien M (1999) Extent of humification of anthracene, fluoranthene, and benzo[a]pyrene by Pleurotus ostreatus during growth in PAH-contaminated soils. Lett Appl Microbiol 28: 250–254.Google Scholar
  16. Bogan BW, Lamar RT, Hammel KE (1996) Fluorene oxidation in vivo by Phanerochaete chrysosporium and in vitro during manganese peroxidase-dependent lipid peroxidation. Appl Environ Microbiol 62: 1788–1792.PubMedGoogle Scholar
  17. Böhmer S, Messner K, Srebotnik E (1998) Oxidation of phenanthrene by a fungal laccase in the presence of 1-hydroxybenzotriazole and unsaturated lipids. Biochem Biophys Res Commun 244: 233–238.PubMedGoogle Scholar
  18. Boonchan S, Britz ML, Stanley GA (2000) Degradation and mineralization of high-molecular-weight polycyclic aromatic hydrocarbons by defined fungal-bacterial cocultures. Appl Environ Microbiol 66: 1007–1019.PubMedGoogle Scholar
  19. Braun-Lüllemann A, Hüttermann A, Majcherczyk A (1999) Screening of ectomycorrhizal fungi for degradation of polycyclic aromatic hydrocarbons. Appl Microbiol Biotechnol 53: 127–132.Google Scholar
  20. Bressler DC, Fedorak PM, Pickard MA (2000) Oxidation of carbazole, N-ethylcarbazole, fluorene, and dibenzothiophene by the laccase of Coriolopsis gallica. Biotechnol Lett 22: 1119–1125.Google Scholar
  21. Bumpus JA (1989) Biodegradation of polycyclic aromatic hydrocarbons by Phanerochaete chrysosporium. Appl Environ Microbiol 55: 154–158.PubMedGoogle Scholar
  22. Bumpus JA, Tien M, Wright D, Aust SD (1985) Oxidation of persistent environmental pollutants by a white rot fungus. Science 228: 1434–1436.PubMedGoogle Scholar
  23. Cajthaml T, Erbanová P, Šašek V, Moeder M (2006) Breakdown products on metabolic pathway of degradation of benz[a]anthracene by a ligninolytic fungus. Chemosphere 64: 560–564.PubMedGoogle Scholar
  24. Cajthaml T, Möder M, Kačer P, Šašek V, Popp P (2002) Study of fungal degradation products of polycyclic aromatic hydrocarbons using gas chromatography with ion trap mass spectrometry detection. J Chromatogr A 974: 213–222.PubMedGoogle Scholar
  25. Cambria MT, Minniti Z, Librando V, Cambria A (2008) Degradation of polycyclic aromatic hydrocarbons by Rigidoporus lignosus and its laccase in the presence of redox mediators. Appl Biochem Biotechnol 149: 1–8.PubMedGoogle Scholar
  26. Canet R, Birnstingl JG, Malcolm DG, Lopez-Real JM, Beck AJ (2001) Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by native microflora and combinations of white-rot fungi in a coal-tar contaminated soil. Biores Technol 76: 113–117.Google Scholar
  27. Canet R, Lopez-Real JM, Beck AJ (1999) Overview of polycyclic aromatic hydrocarbon biodegradation by white-rot fungi. Land Contam Reclam 7: 191–197.Google Scholar
  28. Capotorti G, Cesti P, Lombardi A, Guglielmetti G (2005) Formation of sulfate conjugates metabolites in the degradation of phenanthrene, anthracene, pyrene and benzo[a]pyrene by the ascomycete Aspergillus terreus. Polycycl Aromat Compd 25: 197–213.Google Scholar
  29. Capotorti G, Digianvincenzo P, Cesti P, Bernardi A, Guglielmetti G (2004) Pyrene and benzo[a]pyrene metabolism by an Aspergillus terreus strain isolated from a polycylic aromatic hydrocarbons polluted soil. Biodegradation 15: 79–85.PubMedGoogle Scholar
  30. Casillas RP, Crow SA, Heinze TM, Deck J, Cerniglia CE (1996) Initial oxidative and subsequent conjugative metabolites produced during the metabolism of phenanthrene by fungi. J Ind Microbiol 16: 205–215.PubMedGoogle Scholar
  31. Cerniglia CE (1982) Initial reactions in the oxidation of anthracene by Cunninghamella elegans. J Gen Microbiol 128: 2055–2061.Google Scholar
  32. Cerniglia CE (1993) Biodegradation of polycyclic aromatic hydrocarbons. Curr Opin Biotechnol 4: 331–338.Google Scholar
  33. Cerniglia CE (1997) Fungal metabolism of polycyclic aromatic hydrocarbons: past, present and future applications in bioremediation. J Ind Microbiol Biotechnol 19: 324–333.PubMedGoogle Scholar
  34. Cerniglia CE, Dodge RH, Gibson DT (1980) Studies on the fungal oxidation of polycyclic aromatic hydrocarbons. Bot Mar 23: 121–124.Google Scholar
  35. Cerniglia CE, Freeman JP, Mitchum RK (1982) Glucuronide and sulfate conjugation in the fungal metabolism of aromatic hydrocarbons. Appl Environ Microbiol 43: 1070–1075.PubMedGoogle Scholar
  36. Cerniglia CE, Gibson DT (1977) Metabolism of naphthalene by Cunninghamella elegans. Appl Environ Microbiol 34: 363–370.PubMedGoogle Scholar
  37. Cerniglia CE, Gibson DT (1979) Oxidation of benzo[a]pyrene by the filamentous fungus Cunninghamella elegans. J Biol Chem 254: 12174–12180.PubMedGoogle Scholar
  38. Cerniglia CE, Gibson DT, Dodge RH (1994) Metabolism of benz[a]anthracene by the filamentous fungus Cunninghamella elegans. Appl Environ Microbiol 60: 3931–3938.PubMedGoogle Scholar
  39. Cerniglia CE, Hebert RL, Szaniszlo PJ, Gibson DT (1978) Fungal transformation of naphthalene. Arch Microbiol 117: 135–143.PubMedGoogle Scholar
  40. Cerniglia CE, Kelly DW, Freeman JP, Miller DW (1986) Microbial metabolism of pyrene. Chem-Biol Interact 57: 203–216.PubMedGoogle Scholar
  41. Cerniglia CE, Sutherland JB (2001) Bioremediation of polycyclic aromatic hydrocarbons by ligninolytic and non-ligninolytic fungi. In Fungi in Bioremediation. GM Gadd (ed.). Cambridge, UK: Cambridge University Press, pp. 136–187.Google Scholar
  42. Cerniglia CE, Sutherland JB (2006) Relative roles of bacteria and fungi in polycyclic aromatic hydrocarbon biodegradation and bioremediation of contaminated soils. In Fungi in Biogeochemical Cycles. GM Gadd (ed.). Cambridge, UK: Cambridge University Press, pp. 182–211.Google Scholar
  43. Cerniglia CE, Yang SK (1984) Stereoselective metabolism of anthracene and phenanthrene by the fungus Cunninghamella elegans. Appl Environ Microbiol 47: 119–124.PubMedGoogle Scholar
  44. Chang BV, Shiung LC, Yuan SY (2002) Anaerobic biodegradation of polycyclic aromatic hydrocarbon in soil. Chemosphere 48: 717–724.PubMedGoogle Scholar
  45. Chulalaksananukul S, Gadd GM, Sangvanich P, Sihanonth P, Piapukiew J, Vangnai AS (2006) Biodegradation of benzo[a]pyrene by a newly isolated Fusarium sp. FEMS Microbiol Lett 262: 99–106.PubMedGoogle Scholar
  46. Clemente AR, Anazawa TA, Durrant LR (2001) Biodegradation of polycyclic aromatic hydrocarbons by soil fungi. Braz J Microbiol 32: 255–261.Google Scholar
  47. Collins PJ, Dobson ADW (1996) Oxidation of fluorene and phenanthrene by Mn(II) dependent peroxidase activity in whole cultures of Trametes (Coriolus) versicolor. Biotechnol Lett 18: 801–804.Google Scholar
  48. Collins PJ, Kotterman MJJ, Field JA, Dobson ADW (1996) Oxidation of anthracene and benzo[a]pyrene by laccases from Trametes versicolor. Appl Environ Microbiol 62: 4563–4567.PubMedGoogle Scholar
  49. Colombo JC, Cabello M, Arambarri AM (1996) Biodegradation of aliphatic and aromatic hydrocarbons by natural soil microflora and pure cultures of imperfect and lignolitic fungi. Environ Pollut 94: 355–362.PubMedGoogle Scholar
  50. Corgié SC, Fons F, Beguiristain T, Leyval C (2006) Biodegradation of phenanthrene, spatial distribution of bacterial populations and dioxygenase expression in the mycorrhizosphere of Lolium perenne inoculated with Glomus mosseae. Mycorrhiza 16: 207–212.PubMedGoogle Scholar
  51. Daisy BH, Strobel GA, Castillo U, Ezra D, Sears J, Weaver DK, Runyon JB (2002) Naphthalene, an insect repellent, is produced by Muscodor vitigenus, a novel endophytic fungus. Microbiology 148: 3737–3741.PubMedGoogle Scholar
  52. da Silva M, Cerniglia CE, Pothuluri JV, Canhos VP, Esposito E (2003) Screening filamentous fungi isolated from estuarine sediments for the ability to oxidize polycyclic aromatic hydrocarbons. World J Microbiol Biotechnol 19: 399–405.Google Scholar
  53. Datta D, Samanta TB (1988) Effect of inducers on metabolism of benzo[a]pyrene in vivo and in vitro: analysis by high pressure liquid chromatography. Biochem Biophys Res Commun 155: 493–502.PubMedGoogle Scholar
  54. Davis MW, Glaser JA, Evans JW, Lamar RT (1993) Field evaluation of the lignin-degrading fungus Phanerochaete sordida to treat creosote-contaminated soil. Environ Sci Technol 27: 2572–2576.Google Scholar
  55. Doddapaneni H, Subramanian V, Yadav JS (2005) Physiological regulation, xenobiotic induction, and heterologous expression of P450 monooxygenase gene pc-3 (CYP63A3), a new member of the CYP63 gene cluster in the white-rot fungus Phanerochaete chrysosporium. Curr Microbiol 50: 292–298.PubMedGoogle Scholar
  56. Doddapaneni H, Yadav JS (2004) Differential regulation and xenobiotic induction of tandem P450 monooxygenase genes pc-1 (CYP63A1) and pc-2 (CYP63A2) in the white-rot fungus Phanerochaete chrysosporium. Appl Microbiol Biotechnol 65: 559–565.PubMedGoogle Scholar
  57. Eggen T (1999) Application of fungal substrate from commercial mushroom production–Pleurotus ostreatus–for bioremediation of creosote contaminated soil. Int Biodeterior Biodegrad 44: 117–126.Google Scholar
  58. Eggen T, Majcherczyk A (1998) Removal of polycyclic aromatic hydrocarbons (PAH) in contaminated soil by white rot fungus Pleurotus ostreatus. Int Biodeterior Biodegrad 41: 111–117.Google Scholar
  59. Eggen T, Sveum P (1999) Decontamination of aged creosote polluted soil: the influence of temperature, white rot fungus Pleurotus ostreatus, and pre-treatment. Int Biodeterior Biodegrad 43: 125–133.Google Scholar
  60. Eibes G, Moreira MT, Feijoo G, Daugulis AJ, Lema JM (2007) Operation of a two-phase partitioning bioreactor for the oxidation of anthracene by the enzyme manganese peroxidase. Chemosphere 66: 1744–1751.PubMedGoogle Scholar
  61. Engler KH, Kelly SL, Coker RD, Evans IH (2000) Toxin-binding properties of cytochrome P450 in Saccharomyces cerevisiae and Kluyveromyces marxianus. Biotechnol Lett 22: 3–8.Google Scholar
  62. Faber BW, Schonewille ABJA, van Gorcom RFM, Duine JA (2001) Constitutive and inducible hydroxylase activities involved in the degradation of naphthalene by Cunninghamella elegans. Appl Microbiol Biotechnol 55: 486–491.PubMedGoogle Scholar
  63. Ferris JP, Fasco MJ, Stylianopoulou FL, Jerina DM, Daly JW, Jeffrey AM (1973) Monooxygenase activity in Cunninghamella bainieri: evidence for a fungal system similar to liver microsomes. Arch Biochem Biophys 156: 97–103.PubMedGoogle Scholar
  64. Field JA, Boelsma F, Baten H, Rulkens WH (1995) Oxidation of anthracene in water/solvent mixtures by the white-rot fungus, Bjerkandera sp. strain BOS55. Appl Microbiol Biotechnol 44: 234–240.Google Scholar
  65. Finlayson-Pitts BJ, Pitts JN (1997) Tropospheric air pollution: Ozone, airborne toxics, polycyclic aromatic hydrocarbons, and particles. Science 276: 1045–1052.PubMedGoogle Scholar
  66. Garon D, Krivobok S, Seigle-Murandi F (2000) Fungal degradation of fluorene. Chemosphere 40: 91–97.PubMedGoogle Scholar
  67. Garon D, Krivobok S, Wouessidjewe D, Seigle-Murandi F (2002) Influence of surfactants on solubilization and fungal degradation of fluorene. Chemosphere 47: 303–309.PubMedGoogle Scholar
  68. Garon D, Sage L, Seigle-Murandi F (2004) Effects of fungal bioaugmentation and cyclodextrin amendment on fluorene degradation in soil slurry. Biodegradation 15: 1–8.PubMedGoogle Scholar
  69. Gauthier E, Déziel E, Villemur R, Juteau P, Lépine F, Beaudet R (2003) Initial characterization of new bacteria degrading high-molecular weight polycyclic aromatic hydrocarbons isolated from a 2-year enrichment in a two-liquid-phase culture system. J Appl Microbiol 94: 301–311.PubMedGoogle Scholar
  70. Giraud F, Guiraud P, Kadri M, Blake G, Steiman R (2001) Biodegradation of anthracene and fluoranthene by fungi isolated from an experimental constructed wetland for wastewater treatment. Water Res 35: 4126–4136.PubMedGoogle Scholar
  71. Gómez J, Rodríguez Solar D, Pazos M, Ángeles Sanromán M (2006) Applicability of Coriolopsis rigida for biodegradation of polycyclic aromatic hydrocarbons. Biotechnol Lett 28: 1013–1017.PubMedGoogle Scholar
  72. Gramss G, Kirsche B, Voigt K-D, Günther T, Fritsche W (1999a) Conversion rates of five polycyclic aromatic hydrocarbons in liquid cultures of fifty-eight fungi and the concomitant production of oxidative enzymes. Mycol Res 103: 1009–1018.Google Scholar
  73. Gramss G, Voigt KD, Kirsche B (1999b) Degradation of polycyclic aromatic hydrocarbons with three to seven aromatic rings by higher fungi in sterile and unsterile soils. Biodegradation 10: 51–62.PubMedGoogle Scholar
  74. Grotenhuis T, Field J, Wasseveld R, Rulkens W (1998) Biodegradation of polyaromatic hydrocarbons (PAH) in polluted soil by the white-rot fungus Bjerkandera. J Chem Technol Biotechnol 71: 359–360.Google Scholar
  75. Guiraud P, Bonnet JL, Boumendjel A, Kadri-Dakir M, Dusser M, Bohatier J, Steiman R (2008) Involvement of Tetrahymena pyriformis and selected fungi in the elimination of anthracene, and toxicity assessment of the biotransformation products. Ecotoxicol Environ Saf 69: 296–305.PubMedGoogle Scholar
  76. Günther T, Sack U, Hofrichter M, Lätz M (1998) Oxidation of PAH and PAH-derivatives by fungal and plant oxidoreductases. J Basic Microbiol 38: 113–122.Google Scholar
  77. Habe H, Omori T (2003) Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 67: 225–243.PubMedGoogle Scholar
  78. Haemmerli SD, Leisola MSA, Sanglard D, Fiechter A (1986) Oxidation of benzo[a]pyrene by extracellular ligninases of Phanerochaete chrysosporium: veratryl alcohol and stability of ligninase. J Biol Chem 261: 6900–6903.PubMedGoogle Scholar
  79. Hallett PD, White NA, Ritz K (2006) Impact of basidiomycete fungi on the wettability of soil contaminated with a hydrophobic polycyclic aromatic hydrocarbon. Biologia 61(Suppl. 19): S334–S338.Google Scholar
  80. Hammel KE (1995) Mechanisms for polycyclic aromatic hydrocarbon degradation by ligninolytic fungi. Environ Health Perspect 103(Suppl. 5): 41–43.PubMedGoogle Scholar
  81. Hammel KE, Gai WZ, Green B, Moen MA (1992) Oxidative degradation of phenanthrene by the ligninolytic fungus Phanerochaete chrysosporium. Appl Environ Microbiol 58: 1832–1838.PubMedGoogle Scholar
  82. Hammel KE, Green B, Gai WZ (1991) Ring fission of anthracene by a eukaryote. Proc Natl Acad Sci USA 88: 10605–10608.PubMedGoogle Scholar
  83. Hammel KE, Kalyanaraman B, Kirk TK (1986) Oxidation of polycyclic aromatic hydrocarbons and dibenzo[p]dioxins by Phanerochaete chrysosporium ligninase. J Biol Chem 261: 16948–16952.PubMedGoogle Scholar
  84. Harayama S (1997) Polycyclic aromatic hydrocarbon bioremediation design. Curr Opin Biotechnol 8: 268–273.PubMedGoogle Scholar
  85. Harvey RG (1997) Polycyclic Aromatic Hydrocarbons. Hoboken, NJ: Wiley.Google Scholar
  86. Hesham AE-L, Wang Z, Zhang Y, Zhang J, Lv W, Yang M (2006) Isolation and identification of a yeast strain capable of degrading four and five ring aromatic hydrocarbons. Ann Microbiol 56: 109–112.Google Scholar
  87. Hestbjerg H, Willumsen PA, Christensen M, Andersen O, Jacobsen CS (2003) Bioaugmentation of tar-contaminated soils under field conditions using Pleurotus ostreatus refuse from commercial mushroom production. Environ Toxicol Chem 22: 692–698.PubMedGoogle Scholar
  88. Hiratsuka N, Oyadomari M, Shinohara H, Tanaka H, Wariishi H (2005) Metabolic mechanisms involved in hydroxylation reactions of diphenyl compounds by the lignin-degrading basidiomycete Phanerochaete chrysosporium. Biochem Eng J 23: 241–246.Google Scholar
  89. in der Wiesche C, Martens R, Zadražil F (1996) Two-step degradation of pyrene by white-rot fungi and soil microorganisms. Appl Microbiol Biotechnol 46: 653–659.PubMedGoogle Scholar
  90. Jiang C, Alexander R, Kagi RI, Murray AP (2000) Origin of perylene in ancient sediments and its geological significance. Org Geochem 31: 1545–1559.Google Scholar
  91. Johannes C, Majcherczyk A (2000) Natural mediators in the oxidation of polycyclic aromatic hydrocarbons by laccase mediator systems. Appl Environ Microbiol 66: 524–528.PubMedGoogle Scholar
  92. Johannes C, Majcherczyk A, Hüttermann A (1996) Degradation of anthracene by laccase of Trametes versicolor in the presence of different mediator compounds. Appl Microbiol Biotechnol 46: 313–317.PubMedGoogle Scholar
  93. Johannes C, Majcherczyk A, Hüttermann A (1998) Oxidation of acenaphthene and acenaphthylene by laccase of Trametes versicolor in a laccase-mediator system. J Biotechnol 61: 151–156.Google Scholar
  94. Juhasz AL, Naidu R (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. Int Biodeterior Biodegrad 45: 57–88.Google Scholar
  95. Kanaly RA, Harayama S (2000) Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria. J Bacteriol 182: 2059–2067.PubMedGoogle Scholar
  96. Kelly SL, Lamb DC, Kelly DE (1997) Sterol 22-desaturase, cytochrome P45061, possesses activity in xenobiotic metabolism. FEBS Lett 412: 233–235.PubMedGoogle Scholar
  97. Kiehlmann E, Pinto L, Moore M (1996) The biotransformation of chrysene to trans-1,2-dihydroxy-1,2-dihydrochrysene by filamentous fungi. Can J Microbiol 42: 604–608.Google Scholar
  98. Kim J-D, Lee C-G (2007) Microbial degradation of polycyclic aromatic hydrocarbons in soil by bacterium-fungus co-cultures. Biotechnol Bioprocess Eng 12: 410–416.Google Scholar
  99. Koivula TT, Salkinoja-Salonen M, Peltola R, Romantschuk M (2004) Pyrene degradation in forest humus microcosms with or without pine and its mycorrhizal fungus. J Environ Qual 33: 45–53.PubMedGoogle Scholar
  100. Kotterman MJJ, Rietberg H-J, Hage A, Field JA (1998) Polycyclic aromatic hydrocarbon oxidation by the white-rot fungus Bjerkandera sp. strain BOS55 in the presence of nonionic surfactants. Biotechnol Bioeng 57: 220–227.PubMedGoogle Scholar
  101. Kotterman MJJ, Wasseveld RA, Field JA (1996) Hydrogen peroxide production as a limiting factor in xenobiotic compound oxidation by nitrogen-sufficient cultures of Bjerkandera sp. strain BOS55 overproducing peroxidases. Appl Environ Microbiol 62: 880–885.PubMedGoogle Scholar
  102. Lahav R, Fareleira P, Nejidat A, Abeliovich A (2002) The identification and characterization of osmotolerant yeast isolates from chemical wastewater evaporation ponds. Microbial Ecol 43: 388–396.Google Scholar
  103. Lambert M, Kremer S, Sterner O, Anke H (1994) Metabolism of pyrene by the basidiomycete Crinipellis stipitaria and identification of pyrenequinones and their hydroxylated precursors in strain JK375. Appl Environ Microbiol 60: 3597–3601.PubMedGoogle Scholar
  104. Lang E, Nerud F, Novotná E, Zadražil F, Martens R (1996) Production of ligninolytic exoenzymes and 14C-pyrene mineralization by Pleurotus sp. in lignocellulose substrate. Folia Microbiol 41: 489–493.Google Scholar
  105. Lange B, Kremer S, Sterner O, Anke H (1994) Pyrene metabolism in Crinipellis stipitaria: identification of trans-4,5-dihydro-4,5-dihydroxypyrene and 1-pyrenylsulfate in strain JK364. Appl Environ Microbiol 60: 3602–3607.PubMedGoogle Scholar
  106. Lange B, Kremer S, Sterner O, Anke H (1996) Metabolism of pyrene by basidiomycetous fungi of the genera Crinipellis, Marasmius, and Marasmiellus. Can J Microbiol 42: 1179–1183.Google Scholar
  107. Lau KL, Tsang YY, Chiu SW (2003) Use of spent mushroom compost to bioremediate PAH-contaminated samples. Chemosphere 52: 1539–1546.PubMedGoogle Scholar
  108. Launen L, Pinto L, Wiebe C, Kiehlmann E, Moore M (1995) The oxidation of pyrene and benzo[a]pyrene by nonbasidiomycete soil fungi. Can J Microbiol 41: 477–488.PubMedGoogle Scholar
  109. Leonardi V, Šašek V, Petruccioli M, D’Annibale A, Erbanová P, Cajthaml T (2007) Bioavailability modification and fungal biodegradation of PAHs in aged industrial soils. Int Biodeterior Biodegrad 60: 165–170.Google Scholar
  110. Leonowicz A, Matuszewska A, Luterek J, Ziegenhagen D, Wojtaś-Wasilewska M, Cho N-S, Hofrichter M, Rogalski J (1999) Biodegradation of lignin by white rot fungi. Fungal Genet Biol 27: 175–185.PubMedGoogle Scholar
  111. Levin L, Viale A, Forchiassin A (2003) Degradation of organic pollutants by the white rot basidiomycete Trametes trogii. Int Biodeter Biodegrad 52: 1–5.Google Scholar
  112. Lisowska K, Długoński J (1999) Removal of anthracene and phenanthrene by filamentous fungi capable of cortexolone 11-hydroxylation. J Basic Microbiol 39: 117–125.PubMedGoogle Scholar
  113. Lisowska K, Długoński J (2003) Concurrent corticosteroid and phenanthrene transformation by filamentous fungus Cunninghamella elegans. J Steroid Biochem Mol Biol 85: 63–69.PubMedGoogle Scholar
  114. Lisowska K, Długoński J, Freeman JP, Cerniglia CE (2006) The effect of the corticosteroid hormone cortexolone on the metabolites produced during phenanthrene biotransformation in Cunninghamella elegans. Chemosphere 64: 1499–1506.PubMedGoogle Scholar
  115. Lisowska K, Pałecz B, Długoński J (2004) Microcalorimetry as a possible tool for phenanthrene toxicity evaluation to eukaryotic cells. Thermochim Acta 411: 181–186.Google Scholar
  116. Liu SL, Luo YM, Cao ZH, Wu LH, Ding KQ, Christie P (2004) Degradation of benzo[a]pyrene in soil with arbuscular mycorrhizal alfalfa. Environ Geochem Health 26: 285–293.PubMedGoogle Scholar
  117. Löser C, Seidel H, Zehnsdorf A, Hoffmann P (2000) Improvement of the bioavailability of hydrocarbons by applying nonionic surfactants during the microbial remediation of a sandy soil. Acta Biotechnol 20: 99–118.Google Scholar
  118. MacGillivray AR, Shiaris MP (1993) Biotransformation of polycyclic aromatic hydrocarbons by yeasts isolated from coastal sediments. Appl Environ Microbiol 59: 1613–1618.PubMedGoogle Scholar
  119. Majcherczyk A, Johannes C (2000) Radical mediated indirect oxidation of a PEG-coupled polycyclic aromatic hydrocarbon (PAH) model compound by fungal laccase. Biochim Biophys Acta 1474: 157–162.PubMedGoogle Scholar
  120. Majcherczyk A, Johannes C, Hüttermann A (1998) Oxidation of polycyclic aromatic hydrocarbons (PAH) by laccase of Trametes versicolor. Enzyme Microb Technol 22: 335–341.Google Scholar
  121. Mamilov AS, Byzov BA, Zvyagintsev DG, Dilly OM (2001) Predation on fungal and bacterial biomass in a soddy-podzolic soil amended with starch, wheat straw and alfalfa meal. Appl Soil Ecol 16: 131–139.Google Scholar
  122. Martens R, Zadražil F (1998) Screening of white-rot fungi for their ability to mineralize polycyclic aromatic hydrocarbons in soil. Folia Microbiol 43: 97–103.Google Scholar
  123. Masaphy S, Lamb DC, Kelly SL (1999) Purification and characterization of a benzo[a]pyrene hydroxylase from Pleurotus pulmonarius. Biochem Biophys Res Commun 266: 326–329.Google Scholar
  124. Masaphy S, Levanon D, Henis Y, Venkateswarlu K, Kelly SL (1996) Evidence for cytochrome P-450 and P-450-mediated benzo[a]pyrene hydroxylation in the white rot fungus Phanerochaete chrysosporium. FEMS Microbiol Lett 135: 51–55.PubMedGoogle Scholar
  125. Mastral AM, Callén MS (2000) A review on polycyclic aromatic hydrocarbon (PAH) emissions from energy generation. Environ Sci Technol 34: 3051–3057.Google Scholar
  126. Mastrangelo G, Fadda E, Marzia V (1996) Polycyclic aromatic hydrocarbons and cancer in man. Environ Health Perspect 104: 1166–1170.PubMedGoogle Scholar
  127. May R, Schröder P, Sandermann H (1997) Ex-situ process for treating PAH-contaminated soil with Phanerochaete chrysosporium. Environ Sci Technol 31: 2626–2633.Google Scholar
  128. Meléndez-Estrada J, Amezcua-Allieri MA, Alvarez PJJ, Rodríguez-Vázquez R (2006) Phenanthrene removal by Penicillium frequentans grown on a solid-state culture: effect of oxygen concentration. Environ Technol 27: 1073–1080.PubMedGoogle Scholar
  129. Miller KP, Ramos KS (2001) Impact of cellular metabolism on the biological effects of benzo[a]pyrene and related hydrocarbons. Drug Metab Rev 33: 1–35.PubMedGoogle Scholar
  130. Moen MA, Hammel KE (1994) Lipid-peroxidation by the manganese peroxidase of Phanerochaete chrysosporium is the basis for phenanthrene oxidation by the intact fungus. Appl Environ Microbiol 60: 1956–1961.PubMedGoogle Scholar
  131. Mollea C, Bosco F, Ruggeri B (2005) Fungal biodegradation of naphthalene: microcosms studies. Chemosphere 60: 636–643.PubMedGoogle Scholar
  132. Mori T, Kitano S, Kondo R (2003) Biodegradation of chloronaphthalenes and polycyclic aromatic hydrocarbons by the white-rot fungus Phlebia lindtneri. Appl Microbiol Biotechnol 61: 380–383.PubMedGoogle Scholar
  133. Mougin C (2002) Bioremediation and phytoremediation of industrial PAH-polluted soils. Polycycl Aromat Compd 22: 1011–1043.Google Scholar
  134. Mougin C, Jolivalt C, Malosse C, Chaplain V, Sigoillot J-C, Asther M (2002) Interference of soil contaminants with laccase activity during the transformation of complex mixtures of polycyclic aromatic hydrocarbons in liquid media. Polycycl Aromat Compd 22: 673–688.Google Scholar
  135. Mueller JG, Cerniglia CE, Pritchard PH (1996) Bioremediation of environments contaminated by polycyclic aromatic hydrocarbons. In Bioremediation: Principles and Applications. RL Crawford and DL Crawford (ed.). Cambridge, UK: Cambridge University Press, pp. 125–194.Google Scholar
  136. Nemergut DR, Wunch KG, Johnson RM, Bennett JW (2000) Benzo[a]pyrene removal by Marasmiellus troyanus in soil microcosms. J Ind Microbiol Biotechnol 25: 116–119.Google Scholar
  137. Novotny Č, Erbanová P, Cajthaml T, Rothschild N, Dosoretz C, Šašek V (2000) Irpex lacteus, a white rot fungus applicable to water and soil bioremediation. Appl Microbiol Biotechnol 54: 850–853.PubMedGoogle Scholar
  138. Novotny Č, Erbanová P, Šašek V, Kubátová A, Cajthaml T, Lang E, Krahl J, Zadražil F (1999) Extracellular oxidative enzyme production and PAH removal in soil by exploratory mycelium of white rot fungi. Biodegradation 10: 159–168.PubMedGoogle Scholar
  139. Obuekwe CO, Hourani G, Radwan SS (2001) High-temperature hydrocarbon biodegradation activities in Kuwaiti desert soil samples. Folia Microbiol 46: 535–539.Google Scholar
  140. Phillips DH (1983) Fifty years of benzo[a]pyrene. Nature 303: 468–472.PubMedGoogle Scholar
  141. Pickard MA, Roman R, Tinoco R, Vázquez-Duhalt R (1999) Polycyclic aromatic hydrocarbon metabolism by white rot fungi and oxidation by Coriolopsis gallica UAMH 8260 laccase. Appl Environ Microbiol 65: 3805–3809.PubMedGoogle Scholar
  142. Pointing SB (2001) Feasibility of bioremediation by white-rot fungi. Appl Microbiol Biotechnol 57: 20–33.PubMedGoogle Scholar
  143. Pothuluri JV, Cerniglia CE (1994) Microbial metabolism of polycyclic aromatic hydrocarbons. In Biological Degradation and Bioremediation of Toxic Chemicals. GR Chaudhry (ed.). Portland, Oregon: Dioscorides Press, pp. 92–124.Google Scholar
  144. Pothuluri JV, Evans FE, Heinze TM, Cerniglia CE (1996) Formation of sulfate and glucoside conjugates of benzo[e]pyrene by Cunninghamella elegans. Appl Microbiol Biotechnol 45: 677–683.Google Scholar
  145. Pothuluri JV, Freeman JP, Evans FE, Cerniglia CE (1990) Fungal transformation of fluoranthene. Appl Environ Microbiol 56: 2974–2983.PubMedGoogle Scholar
  146. Pothuluri JV, Freeman JP, Evans FE, Cerniglia CE (1992) Fungal metabolism of acenaphthene by Cunninghamella elegans. Appl Environ Microbiol 58: 3654–3659.PubMedGoogle Scholar
  147. Pothuluri JV, Freeman JP, Evans FE, Cerniglia CE (1993) Biotransformation of fluorene by the fungus Cunninghamella elegans. Appl Environ Microbiol 59: 1977–1980.PubMedGoogle Scholar
  148. Pothuluri JV, Selby A, Evans FE, Freeman JP, Cerniglia CE (1995) Transformation of chrysene and other polycyclic aromatic hydrocarbon mixtures by the fungus Cunninghamella elegans. Can J Bot 73(Suppl. 1): S1025–S1033.Google Scholar
  149. Pozdnyakova NN, Rodakiewicz-Nowak J, Turkovskaya OV, Haber J (2006a) Oxidative degradation of polyaromatic hydrocarbons and their derivatives catalyzed directly by the yellow laccase from Pleurotus ostreatus D1. J Mol Catal B-Enzym 41: 8–15.Google Scholar
  150. Pozdnyakova NN, Rodakiewicz-Nowak J, Turkovskaya OV, Haber J (2006b) Oxidative degradation of polyaromatic hydrocarbons catalyzed by blue laccase from Pleurotus ostreatus D1 in the presence of synthetic mediators. Enzyme Microb Technol 39: 1242–1249.Google Scholar
  151. Rafin C, Potin O, Veignie E, Lounès-Hadj Sahraoui A, Sancholle M (2000) Degradation of benzo[a]pyrene as sole carbon source by a non white rot fungus, Fusarium solani. Polycycl Aromat Compd 21: 311–329.Google Scholar
  152. Raghukumar C, Shailaja MS, Parameswaran PS, Singh SK (2006) Removal of polycyclic aromatic hydrocarbons from aqueous media by the marine fungus NIOCC # 312: involvement of lignin-degrading enzymes and exopolysaccharides. Indian J Mar Sci 35: 373–379.Google Scholar
  153. Rama R, Mougin C, Boyer FD, Kollmann A, Malosse C, Sigoillot JC (1998) Biotransformation of benzo[a]pyrene in bench scale reactor using laccase of Pycnoporus cinnabarinus. Biotechnol Lett 20: 1101–1104.Google Scholar
  154. Rama R, Sigoillot J-C, Chaplain V, Asther M, Jolivalt C, Mougin C (2001) Inoculation of filamentous fungi in manufactured gas plant site soils and PAH transformation. Polycycl Aromat Compd 18: 397–414.Google Scholar
  155. Rama-Mercier R, Mougin C, Sigoillot J-C, Sohier L, Chaplain V, Asther M (1998) Wet sand cultures to screen filamentous fungi for the biotransformation of polycyclic aromatic hydrocarbons. Biotechnol Tech 12: 725–728.Google Scholar
  156. Ravelet C, Grosset C, Krivobok S, Montuelle B, Alary J (2001a) Pyrene degradation by two fungi in a freshwater sediment and evaluation of fungal biomass by ergosterol content. Appl Microbiol Biotechnol 56: 803–808.PubMedGoogle Scholar
  157. Ravelet C, Grosset C, Montuelle B, Benoit-Guyod JL, Alary J (2001b) Liquid chromatography study of pyrene degradation by two micromycetes in a freshwater sediment. Chemosphere 44: 1541–1546.PubMedGoogle Scholar
  158. Ravelet C, Krivobok S, Sage L, Steiman R (2000) Biodegradation of pyrene by sediment fungi. Chemosphere 40: 557–563.PubMedGoogle Scholar
  159. Reid BJ, Fermor TR, Semple KT (2002) Induction of PAH-catabolism in mushroom compost and its use in the biodegradation of soil-associated phenanthrene. Environ Pollut 118: 65–73.PubMedGoogle Scholar
  160. Rodríguez E, Nuero O, Guillén F, Martínez AT, Martínez MJ (2004) Degradation of phenolic and non-phenolic aromatic pollutants by four Pleurotus species: the role of laccase and versatile peroxidase. Soil Biol Biochem 36: 909–916.Google Scholar
  161. Romero MC, Cazau MC, Giorgieri S, Arambarri AM (1998) Phenanthrene degradation by microorganisms isolated from a contaminated stream. Environ Pollut 101: 355–359.Google Scholar
  162. Romero MC, Salvioli ML, Cazau MC, Arambarri AM (2002) Pyrene degradation by yeasts and filamentous fungi. Environ Pollut 117: 159–163.PubMedGoogle Scholar
  163. Sack U, Günther T (1993) Metabolism of PAH by fungi and correlation with extracellular enzymatic activities. J Basic Microbiol 33: 269–277.PubMedGoogle Scholar
  164. Sack U, Heinze TM, Deck J, Cerniglia CE, Cazau MC, Fritsche W (1997b) Novel metabolites in phenanthrene and pyrene transformation by Aspergillus niger. Appl Environ Microbiol 63: 2906–2909.PubMedGoogle Scholar
  165. Sack U, Heinze TM, Deck J, Cerniglia CE, Martens R, Zadražil F, Fritsche W (1997a) Comparison of phenanthrene and pyrene degradation by different wood-decaying fungi. Appl Environ Microbiol 63: 3919–3925.PubMedGoogle Scholar
  166. Sack U, Hofrichter M, Fritsche W (1997c) Degradation of polycyclic aromatic hydrocarbons by manganese peroxidase of Nematoloma frowardii. FEMS Microbiol Lett 152: 227–234.PubMedGoogle Scholar
  167. Salicis F, Krivobok S, Jack M, Benoit-Guyod J-L (1999) Biodegradation of fluoranthene by soil fungi. Chemosphere 38: 3031–3039.PubMedGoogle Scholar
  168. Santodonato J (1997) Review of the estrogenic and antiestrogenic activity of polycyclic aromatic hydrocarbons: relationship to carcinogenicity. Chemosphere 34: 835–848.PubMedGoogle Scholar
  169. Saraswathy A, Hallberg R (2002) Degradation of pyrene by indigenous fungi from a former gasworks site. FEMS Microbiol Lett 210: 227–232.PubMedGoogle Scholar
  170. Saraswathy A, Hallberg R (2005) Mycelial pellet formation by Penicillium ochrochloron species due to exposure to pyrene. Microbiol Res 160: 375–383.PubMedGoogle Scholar
  171. Schützendübel A, Majcherczyk A, Johannes C, Hüttermann A (1999) Degradation of fluorene, anthracene, phenanthrene, fluoranthene, and pyrene lacks connection to the production of extracellular enzymes by Pleurotus ostreatus and Bjerkandera adusta. Int Biodeterior Biodegrad 43: 93–100.Google Scholar
  172. Shanshal M, Aljuboori MH, Dawood SK, Abdullah HH (2004) Carcinogenic polyaromatic hydrocarbons in smut wheat infected with Tilletia caries. Deut Lebensm-Rundsch 100: 505–506.Google Scholar
  173. Shinya M, Tsuchinaga T, Kitano M, Yamada Y, Ishikawa M (2000) Characterization of heavy metals and polycyclic aromatic hydrocarbons in urban highway runoff. Water Sci Technol 42: 201–208.Google Scholar
  174. Shor LM, Rockne KJ, Taghon GL, Young LY, Kosson DS (2003) Desorption kinetics for field-aged polycyclic aromatic hydrocarbons from sediments. Environ Sci Technol 37: 1535–1544.PubMedGoogle Scholar
  175. Singh H (2006) Mycoremediation: Fungal Bioremediation. Hoboken, NJ: Wiley.Google Scholar
  176. Sokhn J, De Leij FAAM, Hart TD, Lynch JM (2001) Effect of copper on the degradation of phenanthrene by soil micro-organisms. Lett Appl Microbiol 33: 164–168.PubMedGoogle Scholar
  177. Song H-G (1999) Comparison of pyrene biodegradation by white rot fungi. World J Microbiol Biotechnol 15: 669–672.Google Scholar
  178. Steffen KT, Hatakka A, Hofrichter M (2002) Removal and mineralization of polycyclic aromatic hydrocarbons by litter-decomposing basidiomycetous fungi. Appl Microbiol Biotechnol 60: 212–217.PubMedGoogle Scholar
  179. Steffen KT, Hatakka A, Hofrichter M (2003) Degradation of benzo[a]pyrene by the litter-decomposing basidiomycete Stropharia coronilla: Role of manganese peroxidase. Appl Environ Microbiol 69: 3957–3964.PubMedGoogle Scholar
  180. Su D, Li P-J, Frank S, Xiong X-Z (2006) Biodegradation of benzo[a]pyrene in soil by Mucor sp. SF06 and Bacillus sp. SB02 co-immobilized on vermiculite . J Environ Sci (China) 18: 1204–1209.Google Scholar
  181. Sutherland JB (2004) Degradation of hydrocarbons by yeasts and filamentous fungi. In Fungal Biotechnology in Agricultural, Food, and Environmental Applications. DK Arora (ed.). New York: Marcel Dekker, pp. 443–455.Google Scholar
  182. Sutherland JB, Freeman JP, Selby AL, Fu PP, Miller DW, Cerniglia CE (1990) Stereoselective formation of a K-region dihydrodiol from phenanthrene by Streptomyces flavovirens. Arch Microbiol 154: 260–266.PubMedGoogle Scholar
  183. Sutherland JB, Fu PP, Yang SK, Von Tungeln LS, Casillas RP, Crow SA, Cerniglia CE (1993) Enantiomeric composition of the trans-dihydrodiols produced from phenanthrene by fungi. Appl Environ Microbiol 59: 2145–2149.PubMedGoogle Scholar
  184. Sutherland JB, Rafii F, Khan AA, Cerniglia CE (1995) Mechanisms of polycyclic aromatic hydrocarbon degradation. In Microbial Transformation and Degradation of Toxic Organic Chemicals. New York: Wiley-Liss, pp. 269–306.Google Scholar
  185. Sutherland JB, Selby AL, Freeman JP, Evans FE, Cerniglia CE (1991) Metabolism of phenanthrene by Phanerochaete chrysosporium. Appl Environ Microbiol 57: 3310–3316.PubMedGoogle Scholar
  186. Sutherland JB, Selby AL, Freeman JP, Fu PP, Miller DW, Cerniglia CE (1992) Identification of xyloside conjugates formed from anthracene by Rhizoctonia solani. Mycol Res 96: 509–517.Google Scholar
  187. Szewczyk R, Bernat P, Milczarek K, Dlugoński J (2003) Application of microscopic fungi isolated from polluted industrial areas for polycyclic aromatic hydrocarbons and pentachlorophenol reduction. Biodegradation 14: 1–8.PubMedGoogle Scholar
  188. Tabak HH, Lazorchak JM, Lei L, Khodadoust AP, Antia JE, Bagchi R, Suidan MT (2003) Studies on bioremediation of polycyclic aromatic hydrocarbon-contaminated sediments: bioavailability, biodegradability, and toxicity issues. Environ Toxicol Chem 22: 473–482.PubMedGoogle Scholar
  189. Tatarko M, Bumpus JA (1993) Biodegradation of phenanthrene by Phanerochaete chrysosporium: on the role of lignin peroxidase. Lett Appl Microbiol 17: 20–24.Google Scholar
  190. Tekere M, Read JS, Mattiasson B (2005) Polycyclic aromatic hydrocarbon biodegradation in extracellular fluids and static batch cultures of selected sub-tropical white rot fungi. J Biotechnol 115: 367–377.PubMedGoogle Scholar
  191. Terrazas-Siles E, Alvarez T, Guieysse B, Mattiasson B (2005) Isolation and characterization of a white rot fungus Bjerkandera sp. strain capable of oxidizing phenanthrene. Biotechnol Lett 27: 845–851.PubMedGoogle Scholar
  192. Tongpim S, Pickard MA (1999) Cometabolic oxidation of phenanthrene to phenanthrene trans-9,10-dihydrodiol by Mycobacterium strain S1 growing on anthracene in the presence of phenanthrene. Can J Microbiol 45: 369–376.PubMedGoogle Scholar
  193. Tuháčková J, Cajthaml T, Novák K, Novotny Č, Mertelik J, Šašek V (2001) Hydrocarbon deposition and soil microflora as affected by highway traffic. Environ Pollut 113: 255–262.PubMedGoogle Scholar
  194. Ullrich R, Hofrichter M (2005) The haloperoxidase of the agaric fungus Agrocybe aegerita hydroxylates toluene and naphthalene. FEBS Lett 579: 6247–6250.PubMedGoogle Scholar
  195. Valentín L, Feijoo G, Moreira MT, Lema JM (2006) Biodegradation of polycyclic aromatic hydrocarbons in forest and salt marsh soils by white-rot fungi. Int Biodeterior Biodegrad 58: 15–21.Google Scholar
  196. Valentín L, Lu-Chau TA, López C, Feijoo G, Moreira MT, Lema JM (2007) Biodegradation of dibenzothiophene, fluoranthene, pyrene and chrysene in a soil slurry reactor by the white-rot fungus Bjerkandera sp BOS55. Process Biochem 42: 641–648.Google Scholar
  197. Vázquez-Duhalt R, Ayala M, Márquez-Rocha FJ (2001) Biocatalytic chlorination of aromatic hydrocarbons by chloroperoxidase of Caldariomyces fumago. Phytochemistry 58: 929–933.PubMedGoogle Scholar
  198. Veignie E, Rafin C, Woisel P, Lounès-Hadj Sahraoui A, Cazier F (2002) Metabolization of the polycyclic aromatic hydrocarbon benzo[a]pyrene by a non-white rot fungus (Fusarium solani) in a batch reactor. Polycycl Aromat Compd 22: 87–97.Google Scholar
  199. Verdin A, Lounès-Hadj Sahraoui A, Fontaine J, Grandmougin-Ferjani A, Durand R (2006a) Effects of anthracene on development of an arbuscular mycorrhizal fungus and contribution of the symbiotic association to pollutant dissipation. Mycorrhiza 16: 397–405.PubMedGoogle Scholar
  200. Verdin A, Lounès-Hadj Saharoui A, Laruelle F, Grandmougin-Ferjani A, Durand R (2006b) Effect of the high polycyclic aromatic hydrocarbon, benzo[a]pyrene, on the lipid content of Fusarium solani. Mycol Res 110: 479–484.PubMedGoogle Scholar
  201. Verdin A, Lounès-Hadj Sahraoui A, Newsam R, Robinson G, Durand R (2005) Polycyclic aromatic hydrocarbons storage by Fusarium solani in intracellular lipid vesicles. Environ Pollut 133: 283–291.PubMedGoogle Scholar
  202. Villemain D, Guiraud P, Bordjiba O, Steiman R (2006) Biotransformation of anthracene and fluoranthene by Absidia fusca Linnemann. Electron J Biotechnol 9: 107–116.Google Scholar
  203. Vyas BRM, Bakowski S, Šašek V, Matucha M (1994) Degradation of anthracene by selected white rot fungi. FEMS Microbiol Ecol 14: 65–70.Google Scholar
  204. Wang R-F, Cao W-W, Khan AA, Cerniglia CE (2000) Cloning, sequencing, and expression in Escherichia coli of a cytochrome P450 gene from Cunninghamella elegans. FEMS Microbiol Lett 188: 55–61.PubMedGoogle Scholar
  205. Wang X, Gong Z, Li P, Zhang L (2007) Degradation of pyrene in soils by free and immobilized yeasts, Candida tropicalis. Bull Environ Contam Toxicol 78: 522–526.PubMedGoogle Scholar
  206. Wang X, Li P, Gong Z, Li B, Ju J, He X, Tai P (2001) Degradation of phenanthrene and pyrene in contaminated soil by immobilized Zoogloea sp. and Fusarium sp. Chin J Appl Ecol 12: 636–638 (in Chinese).Google Scholar
  207. Warshawsky D (1999) Polycyclic aromatic hydrocarbons in carcinogenesis. Environ Health Perspect 107: 317–319.PubMedGoogle Scholar
  208. Wilcke W (2000) Polycyclic aromatic hydrocarbons (PAHs) in soil. J Plant Nutr Soil Sci 163: 229–248.Google Scholar
  209. Wolter M, Zadražil F, Martens R, Bahadir M (1997) Degradation of eight highly condensed polycyclic aromatic hydrocarbons by Pleurotus sp. Florida in solid wheat straw substrate. Appl Microbiol Biotechnol 48: 398–404.Google Scholar
  210. Wu Y, Luo Y, Zou D, Ni J, Liu W, Teng Y, Li Z (2008) Bioremediation of polycyclic aromatic hydrocarbons contaminated soil with Monilinia sp.: degradation and microbial community analysis. Biodegradation 19: 247–257.PubMedGoogle Scholar
  211. Wunch KG, Alworth WL, Bennett JW (1999) Mineralization of benzo[a]pyrene by Marasmiellus troyanus, a mushroom isolated from a toxic waste site. Microbiol Res 154: 75–79.PubMedGoogle Scholar
  212. Wunch KG, Feibelman T, Bennett JW (1997) Screening for fungi capable of removing benzo[a]pyrene in culture. Appl Microbiol Biotechnol 47: 620–624.Google Scholar
  213. Wunder T, Kremer S, Sterner O, Anke H (1994) Metabolism of the polycyclic aromatic hydrocarbon pyrene by Aspergillus niger SK 9317. Appl Microbiol Biotechnol 42: 636–641.PubMedGoogle Scholar
  214. Yogambal RK, Karegoudar TB (1997) Metabolism of polycyclic aromatic hydrocarbons by Aspergillus niger. Indian J Exp Biol 35: 1021–1023.PubMedGoogle Scholar
  215. Yu H (2002) Environmental carcinogenic polycyclic aromatic hydrocarbons: photochemistry and phototoxicity. J Environ Sci Health C 20: 149–183.Google Scholar
  216. Zang S-Y, Li P-J, Yu X-C, Shi K, Zhang H, Chen J (2007) Degradation of metabolites of benzo[a]pyrene by coupling Penicillium chrysogenum with KMnO4. J Environ Sci (China) 19: 238–243.Google Scholar
  217. Zhang DL, Yang YF, Leakey JEA, Cerniglia CE (1996) Phase I and phase II enzymes produced by Cunninghamella elegans for the metabolism of xenobiotics. FEMS Microbiol Lett 138: 221–226.PubMedGoogle Scholar
  218. Zheng Z, Obbard JP (2000) Removal of polycyclic aromatic hydrocarbons from soil using surfactant and the white rot fungus Phanerochaete chrysosporium. J Chem Technol Biotechnol 75: 1183–1189.Google Scholar
  219. Zheng Z, Obbard JP (2001) Effect of non-ionic surfactants on elimination of polycyclic aromatic hydrocarbons (PAHs) in soil-slurry by Phanerochaete chrysosporium. J Chem Technol Biotechnol 76: 423–429.Google Scholar
  220. Zheng Z, Obbard JP (2002a) Removal of surfactant solubilized polycyclic aromatic hydrocarbons by Phanerochaete chrysosporium in a rotating biological contactor reactor. J Biotechnol 96: 241–249.PubMedGoogle Scholar
  221. Zheng Z, Obbard JP (2002b) Polycyclic aromatic hydrocarbon removal from soil by surfactant solubilization and Phanerochaete chrysosporium oxidation. J Environ Qual 31: 1842–1847.PubMedGoogle Scholar
  222. Zumárraga M, Plou FJ, García-Arellano H, Ballesteros A, Alcalde M (2007) Bioremediation of polycyclic aromatic hydrocarbons by fungal laccases engineered by directed evolution. Biocatal Biotransform 25: 219–228.Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  • C. E. Cerniglia
    • 1
  • J. B. Sutherland
    • 1
  1. 1.Division of Microbiology, National Center for Toxicological ResearchFood and Drug AdministrationARUSA

Personalised recommendations