Untapped potential: Exploiting fungi in bioremediation of hazardous chemicals

Nature Reviews Microbiology

Volumn 9, Issue 3, 2011, Pages 177-192

  Harms, Hauke ^a   Schlosser, Dietmar ^a   Wick, Lukas Y ^a  

^a HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BENZENE; CYTOCHROME P450; DYE; ETHYLBENZENE; FUNGAL ENZYME; LACCASE; LIGNIN PEROXIDASE; MANGANESE PEROXIDASE; MONOPHENOL MONOOXYGENASE; NITROREDUCTASE; ORGANOCHLORINE DERIVATIVE; OXIDOREDUCTASE; PEROXIDASE; PESTICIDE; PHENOL HYDROXYLASE; POLYCYCLIC AROMATIC HYDROCARBON; POLYMER; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); REDUCTIVE DEHALOGENASE; TOLUENE; UNCLASSIFIED DRUG; VERSATILE PEROXIDASE; XYLENE;

ASCOMYCETES; BASIDIOMYCETES; BIOREMEDIATION; CATABOLISM; DANGEROUS GOODS; ECOLOGICAL NICHE; ENVIRONMENTAL EXPLOITATION; ENZYME DEGRADATION; ENZYME LOCALIZATION; FUNGUS; MUCOROMYCOTINA; NONHUMAN; PHANEROCHAETE; PRIORITY JOURNAL; REVIEW; SPECIES DIVERSITY;

AIR POLLUTANTS; BIODEGRADATION, ENVIRONMENTAL; FUNGI; HAZARDOUS SUBSTANCES; SOIL POLLUTANTS; WATER POLLUTANTS, CHEMICAL;

FUNGI;

EID: 79951852806     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro2519     Document Type: Review

References (150)

1. Semple, K. T. et al. Defining bioavailability and bioaccessibility of contaminated soil and sediment is complicated. Environ. Sci. Technol. 38, 228A-231A (2004). (Pubitemid 38856351)
2. Kendrick, B. The Fifth Kingdom 3rd edn (Focus, 2000).
3. Cerniglia, C. E. & Sutherland, J. B. in Handbook of Hydrocarbon and Lipid Microbiology (eds Timmis, K. N., McGenity, T., van der Meer, J. R. & de Lorenzo, V.) 2079-2110 (Springer, 2010).
4. Stajich, J. E. et al. The fungi. Curr. Biol. 19, R840-R845 (2009).
5. Glass, N. L., Rasmussen, C., Rocca, M. G. & Read, N. D. Hyphal homing, fusion, and mycelial interconnectedness. Trends Microbiol. 12, 135-141 (2004). (Pubitemid 38314757)
6. Ferguson, B. A., Dreisbach, T. A., Parks, C. G., Filip, G. M. & Schmitt, C. L. Coarse-scale population structure of pathogenic Armillaria species in a mixedconifer forest in the Blue Mountains of northeast Oregon. Can. J. For. Res. 33, 612-623 (2003). (Pubitemid 36755506)
7. Allen, M. F. Mycorrhizal fungi: highways for water and nutrients in arid soils. Vadose Zone J. 6, 291-297 (2007). (Pubitemid 47252313)
8. Ritz, K. & Young, I. M. Interactions between soil structure and fungi. Mycologist 18, 52-59 (2004). (Pubitemid 39040374)
9. Paul, E. A. & Clark, F. E. Soil Microbiology and Biochemistry (Academic, 1996).
10. Bornyasz, M. A., Graham, R. C. & Allen, M. F. Ectomycorrhizae in a soil-weathered granitic bedrock regolith: linking matrix resources to plants. Geoderma 126, 141-160 (2005). (Pubitemid 40383734)
11. Rillig, M. C. & Mummey, D. L. Mycorrhizas and soil structure. New Phytol. 171, 41-53 (2006). (Pubitemid 43847063)
12. Read, D. J. & Perez-Moreno, J. Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? New Phytol. 157, 475-492 (2003). (Pubitemid 36339234)
13. Wösten, H. A. B. et al. How a fungus escapes the water to grow into air. Curr. Biol. 9, 85-88 (1999). (Pubitemid 29083532)
14. Bonfante, P. & Anca, I. A. Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu. Rev. Microbiol. 63, 363-383 (2009).
15. Warmink, J. A., Nazir, R. & van Elsas, J. D. Universal and species-specific bacterial 'fungiphiles' in the mycospheres of different basidiomycetous fungi. Environ. Microbiol. 11, 300-312 (2009).
16. Bebber, D. P., Hynes, J., Darrah, P. R., Boddy, L. & Fricker, M. D. Biological solutions to transport network design. Proc. R. Soc. B 274, 2307-2315 (2007). (Pubitemid 47372884)
17. Tero, A. et al. Rules for biologically inspired adaptive network design. Science 327, 439-442 (2010).
18. Govindarajulu, M. et al. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435, 819-823 (2005). (Pubitemid 40839732)
19. Darrah, P. R., Tlalka, M., Ashford, A., Watkinson, S. C. & Fricker, M. D. The vacuole system is a significant intracellular pathway for longitudinal solute transport in basidiomycete fungi. Eukaryot. Cell 5, 1111-1125 (2006). (Pubitemid 44100709)
20. Allen, M. F., Swenson, W., Querejeta, J. I., Egerton- Warburton, L. M. & Treseder, K. K. Ecology of mycorrhizae: a conceptual framework for complex interactions among plants and fungi. Annu. Rev. Phytopathol. 41, 271-303 (2003). (Pubitemid 37399683)
21. Bago, B. et al. Translocation and utilization of fungal storage lipid in the arbuscular mycorrhizal symbiosis. Plant Physiol. 128, 108-124 (2002). (Pubitemid 34115314)
22. Fricker, M. D. et al. Imaging complex nutrient dynamics in mycelial networks. J. Microsc. 231, 317-331 (2008).
23. Gao, Y. Z., Cheng, Z. X., Ling, W. T. & Huang, J. Arbuscular mycorrhizal fungal hyphae contribute to the uptake of polycyclic aromatic hydrocarbons by plant roots. Bioresour. Technol. 101, 6895-6901 (2010).
24. Wick, L. Y., Furuno, S. & Harms, H. in Handbook of Hydrocarbon Microbiology (eds Timmis, K. N., McGenity, T., van der Meer, J. R. & de Lorenzo, V.) 1555-1561 (Springer, 2010).
25. Kohlmeier, S. et al. Taking the fungal highway: mobilization of pollutant degrading bacteria by fungi. Environ. Sci. Technol. 39, 4640-4646 (2005). (Pubitemid 40853152)
26. Furuno, S. et al. Fungal mycelia allow chemotactic dispersal of PAH-degrading bacteria in waterunsaturated systems. Environ. Microbiol. 12, 1391-1398 (2010).
27. Hawari, J., Beaudet, S., Halasz, A., Thiboutot, S. & Ampleman, G. Microbial degradation of explosives: biotransformation versus mineralization. Appl. Microbiol. Biotechnol. 54, 605-618 (2000).
28. Pointing, S. B. Feasibility of bioremediation by whiterot fungi. Appl. Microbiol. Biotechnol. 57, 20-33 (2001).
29. Prenafeta-Boldú, F. X., Summerbell, R. & Sybren de Hoog, G. Fungi growing on aromatic hydrocarbons: biotechnology's unexpected encounter with biohazard? FEMS Microbiol. Rev. 30, 109-130 (2006).
30. Chang, Y. S. Recent developments in microbial biotransformation and biodegradation of dioxins. J. Mol. Microbiol. Biotechnol. 15, 152-171 (2008).
31. Pinedo-Rilla, C., Aleu, J. & Collado, I. G. Pollutants biodegradation by fungi. Curr. Org. Chem. 13, 1194-1214 (2009).
32. Schmit, J. & Mueller, G. An estimate of the lower limit of global fungal diversity. Biodiv. Conserv. 16, 99-111 (2007).
33. Hofrichter, M., Bublitz, F. & Fritsche, W. Unspecific degradation of halogenated phenols by the soil fungus Penicillium frequentans Bi 7/2. J. Basic Microbiol. 34, 163-172 (1994). (Pubitemid 2111812)
34. Scheibner, K., Hofrichter, M., Herre, A., Michels, J. & Fritsche, W. Screening for fungi intensively mineralizing 2,4,6-trinitrotoluene. Appl. Microbiol. Biotechnol. 47, 452-457 (1997). (Pubitemid 27217457)
35. Prince, R. C. in Handbook of Hydrocarbon and Lipid Microbiology (eds Timmis, K. N., McGenity, T., van der Meer, J. R. & de Lorenzo, V.) 2065-2078 (Springer, 2010).
36. Skinner, K., Cuiffetti, L. & Hyman, M. Metabolism and cometabolism of cyclic ethers by a filamentous fungus, a Graphium sp. Appl. Environ. Microbiol. 75, 5514-5522 (2009).
37. Junghanns, C., Krauss, G. & Schlosser, D. Potential of aquatic fungi derived from diverse freshwater environments to decolourise synthetic azo and anthraquinone dyes. Biores. Technol. 99, 1225-1235 (2008). (Pubitemid 350251704)
38. Jigami, Y., Omori, T., Minoda, Y. & Yamada, K. Screening of n-alkylbenzene assimilating yeasts and identification of oxidation products fron n-alkylbenzenes. Agric. Biol. Chem. 38, 401-408 (1974).
39. Murphy, G. & Perry, J. Assimilation of chlorinated alkanes by hydrocarbon-utilizing fungi. J. Bacteriol. 160, 1171-1174 (1984). (Pubitemid 15222719)
40. Vallini, G., Frassinetti, S., D'Andrea, F., Catelani, G. & Agnolucci, M. Biodegradation of 4-(1-nonyl)phenol by axenic cultures of the yeast Candida aquaetextoris: identification of microbial breakdown products and proposal of a possible metabolic pathway. Int. Biodeter. Biodegr. 47, 133-140 (2001). (Pubitemid 33647394)
41. Shearer, C. et al. Fungal biodiversity in aquatic habitats. Biodiv. Conserv. 16, 49-67 (2007).
42. Sack, U. et al. Comparison of phenanthrene and pyrene degradation by different wood-decaying fungi. Appl. Environ. Microbiol. 63, 3919-3925 (1997). (Pubitemid 27411348)
43. Fahr, K., Wetzstein, H.-G., Grey, R. & Schlosser, D. Degradation of 2,4-dichlorophenol and pentachlorophenol by two brown rot fungi. FEMS Microbiol. Lett. 175, 127-132 (1999). (Pubitemid 29246063)
44. Steffen, K. T., Hatakka, A. & Hofrichter, M. Removal and mineralization of polycyclic aromatic hydrocarbons by litter-decomposing basidiomycetous fungi. Appl. Microbiol. Biotechnol. 60, 212-217 (2002).
45. Steffen, K. T., Hatakka, A. & Hofrichter, M. Degradation of benzo[a]pyrene by the litterdecomposing basidiomycete Stropharia coronilla: role of manganese peroxidase. Appl. Environ. Microbiol. 69, 3957-3964 (2003). (Pubitemid 36870053)
46. Wetzstein, H.-G., Stadler, M., Tichy, H.-V., Dalhoff, A. & Karl, W. Degradation of ciprofloxacin by basidiomycetes and identification of metabolites generated by the brown rot fungus Gloeophyllum striatum. Appl. Environ. Microbiol. 65, 1556-1563 (1999). (Pubitemid 29173684)
47. Middelhoven, W. J. & Spaaij, F. Rhodotorula cresolica sp. nov., a cresol-assimilating yeast species isolated from soil. Int. J. Syst. Bacteriol. 47, 324-327 (1997). (Pubitemid 27163892)
48. Middelhoven, W. J. Catabolism of benzene compounds by ascomycetous and basidiomycetous yeasts and yeastlike fungi. A literature review and an experimental approach. Antonie van Leeuwenhoek 63, 125-144 (1993). (Pubitemid 23280398)
49. Romero, M. C., Salvioli, M. L., Cazau, M. C. & Arambarri, A. M. Pyrene degradation by yeasts and filamentous fungi. Environ. Pollut. 117, 159-163 (2002). (Pubitemid 34076458)
50. Bhatt, M., Zhao, J.-S., Halasz, A. & Hawari, J. Biodegradation of hexahydro-1,3,5-trinitro-1,3,5-triazine by novel fungi isolated from unexploded ordnance contaminated marine sediment. J. Ind. Microbiol. Biotechnol. 33, 850-858 (2006). (Pubitemid 44337599)
51. Meharg, A. W. in Fungi in Bioremediation (ed. Gadd, G. M.) 445-455 (Cambridge Univ. Press, Cambridge, UK, 2001).
52. Meharg, A. W. & Cairney, J. W. G. Ectomycorrhizas - extending the capabilities of rhizosphere remediation? Soil Biol. Biochem. 32, 1475-1484 (2000).
53. Finlay, R. D. Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J. Exp. Bot. 59, 1115-1126 (2008). (Pubitemid 351644652)
54. Huang, H. L. et al. Effect of arbuscular mycorrhizal fungus (Glomus caledonium) on the accumulation and metabolism of atrazine in maize (Zea mays L.) and atrazine dissipation in soil. Environ. Pollut. 146, 452-457 (2007).
55. Valli, K., Wariishi, H. & Gold, M. H. Degradation of 2,7-dichlorodibenzo-p-dioxin by the lignin-degrading basidiomycete Phanerochaete chrysosporium. J. Bacteriol. 174, 2131-2137 (1992).
56. Bumpus, J., Tien, M., Wright, D. & Aust, S. Oxidation of persistent environmental pollutants by a white rot fungus. Science 228, 1434-1436 (1985).
57. Takada, S., Nakamura, M., Matsueda, T., Kondo, R. & Sakai, K. Degradation of polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans by the white rot fungus Phanerochaete sordida YK-624. Appl. Environ. Microbiol. 62, 4323-4328 (1996). (Pubitemid 26399422)
58. Nakamiya, K. et al. Degradation of dioxins by cyclic ether degrading fungus, Cordyceps sinensis. FEMS Microbiol. Lett. 248, 17-22 (2005). (Pubitemid 40828310)
59. Nakamiya, K., Furuichi, T. & Ishii, K. Isolation of a fungus from denitrifying activated sludge that degrades highly chlorinated dioxins. J. Mater. Cycles Waste Manag. 4, 127-134 (2002).
60. Hofrichter, M. Review: lignin conversion by manganese peroxidase (MnP). Enzyme Microb. Technol. 30, 454-466 (2002). (Pubitemid 34326429)
61. Baldrian, P. Wood-inhabiting ligninolytic basidiomycetes in soils: ecology and constraints for applicability in bioremediation. Fungal Ecol. 1, 4-12 (2008). (Pubitemid 351689036)
62. Baldrian, P. Fungal laccases - occurence and properties. FEMS Microbiol. Rev. 30, 215-242 (2006).
63. Majeau, J.-A., Brar, S. K. & Tyagi, R. D. Laccases for removal of recalcitrant and emerging pollutants. Biores. Technol. 101, 2331-2350 (2010).
64. Asgher, M., Bhatti, H., Ashraf, M. & Legge, R. Recent developments in biodegradation of industrial pollutants by white rot fungi and their enzyme system. Biodegradation 19, 771-783 (2008).
65. Rodgers, C. J. et al. Designer laccases: a vogue for high-potential fungal enzymes? Trends Biotechnol. 28, 63-72 (2010).
66. Xu, F. Applications of oxidoreductases: recent progress. Ind. Biotechnol. 1, 38-50 (2005).
67. Halaouli, S., Asther, M., Sigoillot, J. C., Hamdi, M. & Lomascolo, A. Fungal tyrosinases: new prospects in molecular characteristics, bioengineering and biotechnological applications. J. Appl. Microbiol. 100, 219-232 (2006).
68. Ruiz-Duenas, F. J. et al. Substrate oxidation sites in versatile peroxidase and other basidiomycete peroxidases. J. Exp. Bot. 60, 441-452 (2009).
69. Martínez, A. T. Molecular biology and structurefunction of lignin-degrading heme peroxidases. Enzyme Microb. Technol. 30, 425-444 (2002). (Pubitemid 34310267)
70. Hofrichter, M., Ullrich, R., Pecyna, M., Liers, C. & Lundell, T. New and classic families of secreted fungal heme peroxidases. Appl. Microbiol. Biotechnol. 87, 871-897 (2010).
71. Lundell, T. K., Mäkelä, M. R. & Hildén, K. Lignin-modifying enzymes in filamentous basidiomycetes - ecological, functional and phylogenetic review. J. Basic Microbiol. 50, 5-20 (2010).
72. Ikehata, K., Buchanan, I. D., Pickard, M. A. & Smith, D. W. Purification, characterization and evaluation of extracellular peroxidase from two Coprinus species for aqueous phenol treatment. Biores. Technol. 96, 1758-1770 (2005). (Pubitemid 41032995)
73. Majcherczyk, A., Johannes, C. & Huttermann, A. Oxidation of polycyclic aromatic hydrocarbons (PAH) by laccase of Trametes versicolor. Enzyme Microb. Technol. 22, 335-341 (1998). (Pubitemid 28177058)
74. Reddy, G. V. B., Sollewijn Gelpke, M. D. & Gold, M. H. Degradation of 2,4,6-trichlorophenol by Phanerochaete chrysosporium: involvement of reductive dechlorination. J. Bacteriol. 180, 5159-5164 (1998). (Pubitemid 28470944)
75. Junghanns, C., Moeder, M., Krauss, G., Martin, C. & Schlosser, D. Degradation of the xenoestrogen nonylphenol by aquatic fungi and their laccases. Microbiology 151, 45-57 (2005). (Pubitemid 40207668)
76. Cabana, H., Jones, J. P. & Agathos, S. N. Preparation and characterization of cross-linked laccase aggregates and their application to the elimination of endocrine disrupting chemicals. J. Biotechnol. 132, 23-31 (2007). (Pubitemid 47505372)
77. Nyanhongo, G. S., Couto, S. R. & Guebitz, G. M. Coupling of 2,4,6-trinitrotoluene (TNT) metabolites onto humic monomers by a new laccase from Trametes modesta. Chemosphere 64, 359-370 (2006). (Pubitemid 43818053)
78. Van Aken, B. et al. Transformation and mineralization of 2,4,6-trinitrotoluene (TNT) by manganese peroxidase from the white-rot basidiomycete Phlebia radiata. Biodegradation 10, 83-91 (1999). (Pubitemid 29367343)
79. Gomez-Toribio, V., Garcia-Martin, A. B., Martinez, M. J., Martinez, A. T. & Guillén, F. Enhancing the production of hydroxyl radicals by Pleurotus eryngii via quinone redox cycling for pollutant removal. Appl. Environ. Microbiol. 75, 3954-3962 (2009).
80. Kasai, N. et al. Metabolism of mono- and dichloro-dibenzo-p-dioxins by Phanerochaete chrysosporium cytochromes P450. Appl. Microbiol. Biotechnol. 86, 773-780 (2010).
81. Yadav, J. S., Doddapaneni, H. & Subramanian, V. P450ome of the white rot fungus Phanerochaete chrysosporium: structure, evolution and regulation of expression of genomic P450 clusters. Biochem. Soc. Trans. 34, 1165-1169 (2006). (Pubitemid 46769013)
82. Subramanian, V. & Yadav, J. S. Role of P450 monooxygenases in the degradation of the endocrinedisrupting chemical nonylphenol by the white rot fungus Phanerochaete chrysosporium. Appl. Environ. Microbiol. 75, 5570-5580 (2009).
83. Marco-Urrea, E., Perez-Trujillo, M., Vicent, T. & Caminal, G. Ability of white-rot fungi to remove selected pharmaceuticals and identification of degradation products of ibuprofen by Trametes versicolor. Chemosphere 74, 765-772 (2009).
84. Hata, T., Kawai, S., Okamura, H. & Nishida, T. Removal of diclofenac and mefenamic acid by the white rot fungus Phanerochaete sordida YK-624 and identification of their metabolites after fungal transformation. Biodegradation 21, 681-689 (2010).
85. Marco-Urrea, E., Pérez-Trujillo, M., Cruz-Morató, C., Caminal, G. & Vicent, T. White-rot fungus-mediated degradation of the analgesic ketoprofen and identification of intermediates by HPLC-DAD-MS and NMR. Chemosphere 78, 474-481 (2010).
86. Hiratsuka, N, Wariishi, H. & Tanaka, H. Degradation of diphenyl ether herbicides by the lignin-degrading basidiomycete Coriolus versicolor. Appl. Microbiol. Biotechnol. 57, 563-571 (2001). (Pubitemid 33044136)
87. Ullrich, R. & Hofrichter, M. Enzymatic hydroxylation of aromatic compounds. Cell. Mol. Life Sci. 64, 271-93 (2007). (Pubitemid 46440205)
88. Martin, C. et al. Quantification of the influence of extracellular laccase and intracellular reactions on the isomer-specific biotransformation of the xenoestrogen technical nonylphenol by the aquatic hyphomycete Clavariopsis aquatica. Appl. Environ. Microbiol. 75, 4398-4409 (2009).
89. Hundt, K. et al. Transformation of triclosan by Trametes versicolor and Pycnoporus cinnabarinus. Appl. Environ. Microbiol. 66, 4157-4160 (2000).
90. Rieble, S., Joshi, D. K. & Gold, M. H. Aromatic nitroreductase from the basidiomycete Phanerochaete chrysosporium. Biochem. Biophys. Res. Comm. 205, 298-304 (1994). (Pubitemid 24381625)
91. Esteve-Nunez, A., Caballero, A. & Ramos, J. L. Biological degradation of 2,4,6-trinitrotoluene. Microbiol. Mol. Biol. Rev. 65, 335-352 (2001).
92. Bhushan, B. et al. Biotransformation of hexahydro- 1,3,5-trinitro-1,3,5- triazine catalyzed by a NAD(P)H:nitrate oxidoreductase from Aspergillus niger. Environ. Sci. Technol. 36, 3104-3108 (2002). (Pubitemid 34774329)
93. Crocker, F., Indest, K. & Fredrickson, H. Biodegradation of the cyclic nitramine explosives RDX, HMX, and CL-20. Appl. Microbiol. Biotechnol. 73, 274-290 (2006). (Pubitemid 350262604)
94. Fournier, D. et al. Biodegradation of octahydro- 1,3,5,7-tetranitro-1,3, 5,7-tetrazocine (HMX) by Phanerochaete chrysosporium: new insight into the degradation pathway. Environ. Sci. Technol. 38, 4130-4133 (2004). (Pubitemid 39014195)
95. Brock, B. J. & Gold, M. H. 1,4-Benzoquinone reductase from the basidiomycete Phanerochaete chrysosporium: spectral and kinetic analysis. Arch. Biochem. Biophys. 331, 31-40 (1996). (Pubitemid 26230616)
96. Jensen, K. A. Jr, Ryan, Z. C., Vanden Wymelenberg, A., Cullen, D. & Hammel, K. E. An NADH:quinone oxidoreductase active during biodegradation by the brown-rot basidiomycete Gloeophyllum trabeum. Appl. Environ. Microbiol. 68, 2699-2703 (2002). (Pubitemid 34601988)
97. Gomez-Toribio, V., Garcia-Martin, A. B., Martinez, M. J., Martinez, A. T. & Guillén, F. Induction of extracellular hydroxyl radical production by white-rot fungi through quinone redox cycling. Appl. Environ. Microbiol. 75, 3944-3953 (2009).
98. Jensen, K. A. Jr, Houtman, C. J., Ryan, Z. C. & Hammel, K. E. Pathways for extracellular Fenton chemistry in the brown rot basidiomycete Gloeophyllum trabeum. Appl. Environ. Microbiol. 67, 2705-2711 (2001). (Pubitemid 33639747)
99. Kramer, C., Kreisel, G., Fahr, K., Kassbohrer, J. & Schlosser, D. Degradation of 2-fluorophenol by brownrot fungus Gloeophyllum striatum: evidence for the involvement of extracellular Fenton chemistry. Appl. Microbiol. Biotechnol. 64, 387-395 (2004). (Pubitemid 38626464)
100. Marco-Urrea, E., Aranda, E., Caminal, G. & Guillén, F. Induction of hydroxyl radical production in Trametes versicolor to degrade recalcitrant chlorinated hydrocarbons. Biores. Technol. 100, 5757-5762 (2009).
101. Valli, K. & Gold, M. H. Degradation of 2,4-dichlorophenol by the lignin-degrading fungus Phanerochaete chrysosporium. J. Bacteriol. 173, 345-352 (1991).
102. Reddy, G. V. B. & Gold, M. H. Degradation of pentachlorophenol by Phanerochaete chrysosporium: intermediates and reactions involved. Microbiology 146, 405-413 (2000). (Pubitemid 30099215)
103. Dec, J., Haider, K. & Bollag, J. Release of substituents from phenolic compounds during oxidative coupling reactions. Chemosphere 52, 549-56 (2003). (Pubitemid 36644360)
104. Reddy, G. V. B. & Gold, M. H. A two-component tetrachlorohydroquinone reductive dehalogenase system from the lignin-degrading basidiomycete Phanerochaete chrysosporium. Biochem. Biophys. Res. Comm. 257, 901-905 (1999). (Pubitemid 29303007)
105. Rode, U. & Muller, R. Transformation of the ionic X-ray contrast agent diatrizoate and related triiodinated benzoates by Trametes versicolor. Appl. Environ. Microbiol. 64, 3114-3117 (1998). (Pubitemid 28363198)
106. Martin, C., Moeder, M., Daniel, X., Krauss, G. & Schlosser, D. Biotransformation of the polycyclic musks HHCB and AHTN and metabolite formation by fungi occurring in freshwater environments. Environ. Sci. Technol. 41, 5395-5402 (2007). (Pubitemid 47221761)
107. Cajthaml, T., Kresinová, Z., Svobodová, K., Sigler, K. & Rezanka, T. Microbial transformation of synthetic estrogen 17α-ethinylestradiol. Environ. Pollut. 157, 3325-3335 (2009).
108. Banitz, T. et al. Assessing biodegradation benefits from dispersal networks. Ecol. Modell. 11 Aug 2010 (doi:10.1016/j.ecolmodel.2010.07.005).
109. Wick, L. Y. et al. Effect of fungal hyphae on the access of bacteria to phenanthrene in soil. Environ. Sci. Technol. 41, 500-505 (2007). (Pubitemid 46106282)
110. Öberg, L. G., Glas, B., Swanson, S. E., Rappe, C. & Paul, K. G. Peroxidase-catalyzed oxidation of chlorophenols to polychlorinated dibenzo-p-dioxins and dibenzofurans. Arch. Environ. Contam. Toxicol. 19, 930-938 (1990). (Pubitemid 20361964)
111. Morimoto, K. & Tatsumi, K. Effect of humic substances on the enzymatic formation of OCDD from PCP. Chemosphere 34, 1277-1283 (1997). (Pubitemid 27161608)
112. Park, J., Dec, J., Kim, J. & Bollag, J. Dehalogenation of xenobiotics as a consequence of binding to humic materials. Arch. Environ. Contam. Toxicol. 38, 405-410 (2000). (Pubitemid 30196859)
113. Johnsen, A. R., Wick, L. Y. & Harms, H. Principles of microbial PAH-degradation in soil. Environ. Pollut. 133, 71-84 (2005). (Pubitemid 41569171)
114. Juhasz, A. L. & Naidu, R. Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. Int. Biodeter. Biodegr. 45, 57-88 (2000). (Pubitemid 30629048)
115. Lamar, R. T., Davis, M. W., Dietrich, D. M. & Glaser, J. A. Treatment of a pentachlorophenol-contaminated and creosote-contaminated soil using lignin-degrading fungus Phanerochaete sordida - a field demonstration. Soil Biol. Biochem. 26, 1603-1611 (1994).
116. Singh, H. Mycoremediation Fungal Bioremediation (Wiley Interscience, Hoboken, 2006).
117. Lebeaud, T., Braud, A. & Jezequel, K. Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ. Pollut. 153, 497-522 (2008). (Pubitemid 351680329)
118. Gohre, V. & Paszkowski, U. Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223, 1115-1122 (2006).
119. Ruiz Lozano, J. M. & Azcon, R. Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Physiol. Plant. 95, 472-478 (1995). (Pubitemid 3010137)
120. Bronick, C. J. & Lal, R. Soil structure and management: a review. Geoderma 124, 3-22 (2005). (Pubitemid 39554177)
121. Schmidt, S. N., Christensen J. H. & Johnsen, A. R. Fungal PAH-metabolites resist mineralization by soil microorganisms. Environ. Sci. Technol. 44, 1677-1682 (2010).
122. Singleton, I. in Fungi in Bioremediation (ed. Gadd, G. M.) 79-96 (Cambridge Univ. Press, Cambridge, UK, 2001).
123. Volante, A. et al. Influence of three species of arbuscular mycorrhizal fungi on the persistence of aromatic hydrocarbons in contaminated substrates. Mycorrhiza 16, 43-50 (2005). (Pubitemid 41618816)
124. Wu, N. Y., Zhang, S. Z., Huang, H. L. & Christie, P. Enhanced dissipation of phenanthrene in spiked soil by arbuscular mycorrhizal alfalfa combined with a nonionic surfactant amendment. Sci. Total Environ. 394, 230-236 (2008).
125. D'Souza, D. T., Tiwari, R., Sah, A. K. & Raghukumar, C. Enhanced production of laccase by a marine fungus during treatment of colored effluents and synthetic dyes. Enzyme Microb. Technol. 38, 504-511 (2006). (Pubitemid 41774521)
126. Raghukumar, C., D'Souza-Ticlo, D. & Verma, A. Treatment of colored effluents with lignin-degrading enzymes: an emerging role of marine-derived fungi. Crit. Rev. Microbiol. 34, 189-206 (2008).
127. Junghanns, C. et al. Biochemical and molecular genetic characterisation of a novel laccase produced by the aquatic ascomycete Phoma sp. UHH 5-1-03. Appl. Microbiol. Biotechnol. 84, 1095-105 (2009).
128. Snyder, S. A., Westerhoff, P., Yoon, Y. & Sedlak, D. L. Pharmaceuticals, personal care products, and endocrine disruptors in water: implications for the water industry. Environ. Eng. Sci. 20, 449-469 (2003). (Pubitemid 37158352)
129. Gadd, G. M. Biosorption: critical review of scientific rationale, environmental importance and significance for pollution treatment. J. Chem. Technol. Biotechnol. 84, 13-28 (2009).
130. Volesky, B. & Holan, Z. R. Biosorption of heavy metals. Biotechnol. Prog. 11, 235-250 (1995).
131. Garcia, J. et al. Contaminant removal processes in subsurface-flow constructed wetlands: a review. Crit. Rev. Environ. Sci. Technol. 40, 561-661 (2010).
132. Wong, D. Structure and action mechanism of ligninolytic enzymes. Appl. Biochem. Biotechnol. 157, 174-209 (2009).
133. Kennes, C., Vaiga, M. C. Fungal biocatalysts in the biofiltration of VOC-polluted air. J. Biotechnol. 113, 305-319 (2004). (Pubitemid 39237086)
134. Kennes, C., Rene, E. R. & Veiga, M. C. Bioprocesses for air pollution control. J. Chem. Technol. Biotechnol. 84, 1419-1436 (2009).
135. Nizzetto, L. et al. Persistent organic pollutants in the global environment: some perspectives and future challenges. Environ. Sci. Technol. 44, 6526-6531 (2010).
136. Hibbett, D. et al. A higher-level phylogenetic classification of the Fungi. Mycol. Res. 111, 509-547 (2007). (Pubitemid 46915419)
137. Middelhoven, W. J., Scorzetti, G. & Fell, J. W. Trichosporon veenhuisii sp. nov., an alkaneassimilating anamorphic basidiomycetous yeast. Int. J. Syst. Evol. Microbiol. 50, 381-387 (2000). (Pubitemid 30084094)
138. Gadd, G. M. Fungal production of citric and oxalic acid: importance in metal speciation, physiology and biogeochemical processes. Adv. Microb. Physiol. 41, 47-92 (1999).
139. Burgstaller, W. & Schinner, F. Leaching metals with fungi. J. Biotechnol. 27, 91-116 (1993).
140. Sayer, J. A., Cotter-Howells, J. D., Watson, C., Hillier, S. & Gadd, G. M. Lead mineral transformation by fungi. Curr. Biol. 9, 691-694 (1999). (Pubitemid 29332350)
141. Gonzalez-Chavez, M. C., Carrillo-Gonzalez, R., Wright, S. F. & Nichols, K. A. The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environ. Pollut. 130, 317-323 (2004). (Pubitemid 38746449)
142. Eide, D. J. Metal ion transport in eukaryotic microorganisms: insights from Saccharomyces cerevisiae. Adv. Microb. Physiol. 43, 1-38 (2000). (Pubitemid 30481121)
143. Van Ho, A., Ward, D. M. & Kaplan, J. Transition metal transport in yeast. Annu. Rev. Microbiol. 56, 237-261 (2002). (Pubitemid 35217455)
144. Mehra, R. K. & Winge, D. R. Metal-ion resistance in fungi: molecular mechanisms and their regulated expression. J. Cell. Biochem. 45, 30-40 (1991).
145. Kneer, R., Kutchan, T. M., Hochberger A. & Zenk, M. H. Saccharomyces cerevisiae and Neurospora crassa contain heavy-metal sequestering phytochelatin. Arch. Microbiol. 157, 305-310 (1992).
146. Barkay, T. & Wagner-Dobler, I. Microbial transformations of mercury: potentials, challenges, and achievements in controlling mercury toxicity in the environment. Adv. Appl. Microbiol. 57, 1-52 (2005). (Pubitemid 40942001)
147. Darrah, P. R., Tlalka, M., Ashford, A., Watkinson, S. C. & Fricker, M. D. The vacuole system is a significant intracellular pathway for longitudinal solute transport in basidomycete fungi. Eukaryot. Cell 5, 1111-1115 (2006).
148. Gray, S. N. Fungi as potential bioremediation agents in soil contaminated with heavy or radioactive metals. Biochem. Soc. Trans. 28, 666-670 (1998). (Pubitemid 29008145)
149. Leyval, C. & Joner, E. J. in Trace Elements in the Rhizosphere (eds Gobran, G. R., Wenzel W. W. & Lombi, E.) 165-185 (CRC, Boca Raton, 2001).
150. Hammel, K. E. Mechanisms for polycyclic aromatic hydrocarbon degradation by ligninolytic fungi. Environ. Health Perspect. 103, 41-43 (1995).