Abstract
The degradation of the nitroaromatic pollutant 2,4,6-trinitrotoluene (TNT) by the manganese-dependent peroxidase (MnP) of the white-rot fungus Phlebia radiata and the main reduction products formed were investigated. In the presence of small amounts of reduced glutathione (10 mM), a concentrated cell-free preparation of MnP from P. radiata exhibiting an activity of 36 nkat/ml (36 nmol Mn(II) oxidized per sec and per ml) transformed 10 mg/l of TNT within three days. The same preparation was capable of completely transforming the reduced derivatives of TNT. When present at 10 mg/l, the aminodinitrotoluenes were transformed in less than two days and the diaminonitrotoluenes in less than three hours. Experiments with 14C-U-ring labeled TNT and 2-amino-4,6-dinitrotoluene showed that these compounds were mineralized by 22% and 76%, respectively, within 5 days. Higher concentrations of reduced glutathione (50 mM) led to a severe inhibition of the degradation process. It is concluded that Phlebia radiata is a good candidate for the biodegradation of TNT as well as its reduction metabolites.
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References
Barr DP & Aust SD (1994) Mechanisms white-rot fungi use to degrade pollutants. Environ. Sci. Technol. 28: 78A-87A
Bumpus JA & Aust SD (1987) Biodegradation of DDT (1,1,1-trichloro-2,2-bis(4-chlorophenyl)ethane) by the white-rot fungus Phanerochaete chrysosporium. Appl. Environ. Microbiol. 53: 2001–2008
Bumpus JA & Tatarko M (1994) Biodegradation of 2,4,6-trinitrotoluene by Phanerochaete chrysosporium: identification of initial degradation products and the discovery of a TNT metabolite that inhibits lignin peroxidase. Curr. Microbiol. 28: 185–190
Bumpus JA, Tien M, Wright D & Aust SD (1985) Oxidation of persistent environmental pollutants by a white-rot fungus. Science 228: 1434–1436
D'Annibale A, Crestini C, Di Mattia E & Giovannozzi Sermanni G (1996) Veratryl alcohol oxidation by manganese-peroxidase from Lentinus edodes. J. Biotechnol. 48: 231–239
Fernando T, Bumpus JA & Aust SD (1990) Biodegradation of TNT (2,4,6-trinitrotoluene) by Phanerochaete chrysosporium. Appl. Environ. Microbiol. 56: 1666–1671
Field JA, De Jong E, Feijoo-Costa G & de Bont JAM (1993) Screening for ligninolytic fungi applicable to the biodegradation of xenobiotics. Trends Biotechnol. 11: 44–49
Field JA, Stams AJM, Kato M & Schraa G (1995) Enhanced biodegradation of aromatic pollutants in cocultures of anaerobic and aerobic bacterial consortia. Antonie van Leeuwenhoek 67: 47–77
Forrester IT, Grabski AC, Burgess RR & Leatham GF (1988) Manganese, Mn-dependent peroxidases, and the biodegradation of lignin. Biochem. Biophys. Res. Comm. 157: 992–999
Ginns J & Lefebvre MNL (1993) Lignicolous Corticioid Fungi of North America. Systematics, Distribution, and Ecology (Basidiomycota). APS Press, St. Paul, MN, USA
Glenn JK, Akileswaran L & Gold MH (1986) Mn(II) oxidation is the principal function of the extracellular Mn-peroxidase from Phanerochaete chrysosporium. Arch. Biochem. Biophys. 251: 688–696
Hatakka AI (1994) Lignin modifying enzymes from selected white-rot fungi: production and role in lignin degradation. FEMS Microbiol. Rev. 13: 125–135
Hatakka AI & Uusi-Rauva AK (1983) Degradation of 14C-labelled poplar wood lignin by selected white-rot fungi. J. Appl. Microbiol. Biotechnol. 17: 235–242
Hawksworth DL, Kirk PM, Sutton BC & Pegler DN (1995) Ainsworth and Bisby's Dictionary of the Fungi. Cambridge University Press, Cambridge, UK
Hofrichter M, Scheibner K, Schneegass I & Fritsche W (1998) Enzymatic combustion of aromatic and aliphatic compounds by manganese peroxidase from Nematoloma frowardii. Appl. Environ. Microbiol. 64: 399–404
Kantelinen A, Hatakka AI & Viikari L (1989) Production of lignin peroxidase and laccase by Phlebia radiata. Appl. Microbiol. Biotechnol. 31: 234–239
Kantelinen A, Waldner R, Niku-Paavola M-L & Leisola MSA (1988) Comparison of two lignin-degrading fungi: Phlebia radiata and Phanerochaete chrysosporium. Appl. Microbiol. Biotechnol. 28: 193–198
Kuwahara M, Glenn JK, Morgan MA & Gold MH (1984) Separation and characterization of two extracellular H2O2-dependent oxidases from ligninolytic cultures of Phanerochaete chrysosporium. FEBS Lett. 169: 247–250
Li ZM, Comfort SD & Shea PJ (1997) Destruction of 2,4,6-trinitrotoluene by Fenton oxidation. J. Environ. Qual. 26: 480–487
Lamar RT (1992) The role of fungal lignin-degrading enzymes in xenobiotic degradation. Curr. Op. Biotechnol. 3: 261–266
Lundell T & Hatakka A (1994) Participation of Mn(II) in the catalysis of laccase, manganese peroxidase and lignin peroxidase from Phlebia radiata. FEBS Lett. 348: 291–296
Lundell T, Leonowicz A, Rogalski J & Hatakka A (1990) Formation and action of lignin-modifying enzymes in cultures of Phlebia radiata supplemented with veratric acid. Appl. Environ. Microbiol. 56: 2623–2629
Michels J & Gottschalk G (1994) Inhibition of the lignin peroxidase of Phanerochaete chrysosporium by hydroxylaminodinitrotoluene, an early intermediate in the degradation of 2,4,6-trinitrotoluene. Appl. Environ. Microbiol. 60: 187–194
McEldoon JP & Dordick JS (1991) Thiol and Mn2+-mediated oxidation of veratryl alcohol by horseradish peroxidase. J. Biol. Chem. 266: 14288–14293
Niku-Paavola M-L, Karhunen E, Salola P & Raunio V (1988) Ligninolytic enzymes of the white-rot fungus Phlebia radiata. Biochem. J. 254: 877–884
Paszczynski A & Crawford RL (1995) Potential for bioremediation of xenobiotic compounds by the white-rot fungus Phanerochaete chrysosporium. Biotechnol. Prog. 11: 368–379
Rieble S, Joshi DK & Gold MH (1994) Aromatic nitroreductase from the basidiomycete Phanerochaete chrysosporium. Biochem. Biophys. Res. Comm. 205: 298–304
Rieger P-G & Knackmuss H-J (1995) Basic knowledge and perspectives on biodegradation of 2,4,6-trinitrotoluene and related nitroaromatic compounds in contaminated soils. In: Spain JC (Ed) Biodegradation of Nitroaromatic Compounds, Chap 1 (pp 1–18). Plenum Press, New York
Scheibner K & Hofrichter M. (1998) Conversion of aminonitrotoluenes by fungal manganese peroxidase. J. Basic Microbiol. 38: 63–71
Scheibner K, Hofrichter M & Fritsche W (1997) Mineralization of 2-amino-4,6-dinitrotoluene by manganese peroxidase of the white-rot fungus Nematoloma frowardii. Biotechnol. Lett. 19: 835–839
Spiker JK, Crawford DL & Crawford RL (1992) Influence of 2,4,6-trinitrotoluene (TNT) concentration on the degradation of TNT in explosive-contaminated soils by the white-rot fungus Phanerochaete chrysosporium. Appl. Environ. Microbiol. 58: 3199–3202
Stahl JD & Aust SD (1993) Metabolism and detoxification of TNT by Phanerochaete chrysosporium. Biochem. Biophys. Res. Commun. 192: 477–482
Styles JA & Cross MF (1983) Activity of 2,4,6-trinitrotoluene in an in vitro mammalian gene mutation assay. Cancer Lett. 20: 103–108
Tien M & Kirk TK (1983) Lignin degrading enzyme from hymenomycetes Phanerochaete chrysosporium Burds. Science 221: 661–663
Valli K, Brock BJ, Joshi DK & Gold MH (1992) Degradation of 2,4-dinitrotoluene by the lignin-degrading fungus Phanerochaete chrysosporium. Appl. Environ. Microbiol. 58: 221–228
Van Aken B, Skubisz K, Naveau H & Agathos SN (1997) Biodegradation of 2,4,6-trinitrotoluene by the white-rot basidiomycete Phlebia radiata. Biotechnol. Lett. 19: 813–817
Walsh ME (1990) Environmental Transformation Products of Nitroaromatics and Nitroamines: Literature Review and Recommendations for Analytical Method Development. Special Report 90–2, U.S. Army Corps of Engineers, Cold Regions Research & Engineering Laboratory
Wariishi H, Valli K & Gold MH (1992) Manganese(II) oxidation by manganese peroxidase from the basidiomycete Phanerochaete chrysosporium. Kinetic mechanism and role of chelators. J. Biol. Chem. 267: 23688–23695
Wariishi H, Valli K, Renganathan V & Gold MH (1989) Thiol-mediated oxidation of nonphenolic lignin model compounds by manganese peroxidase of Phanerochaete chrysosporium. J. Biol. Chem. 264(25): 14185–14191
Won WD, DiSalvo LH & Ng J (1976) Toxicity and mutagenicity of 2,4,6-trinitrotoluene and its microbial metabolites. Appl. Environ. Microbiol. 31: 576–580
Zbarskii VL, Sonis MA & Orlova EY (1971) Dinitrophenylcarboxylic acids in the Schmidt reaction. Z. Prikl. Khim. 44: 2578–2579
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Van Aken, B., Hofrichter, M., Scheibner, K. 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). https://doi.org/10.1023/A:1008371209913
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DOI: https://doi.org/10.1023/A:1008371209913