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. 1992 Jan;58(1):221–228. doi: 10.1128/aem.58.1.221-228.1992

Degradation of 2,4-dinitrotoluene by the lignin-degrading fungus Phanerochaete chrysosporium.

K Valli 1, B J Brock 1, D K Joshi 1, M H Gold 1
PMCID: PMC195195  PMID: 1539977

Abstract

Under ligninolytic conditions, the white rot basidiomycete Phanerochaete chrysosporium mineralizes 2,4-dinitrotoluene (I). The pathway for the degradation of I was elucidated by the characterization of fungal metabolites and oxidation products generated by lignin peroxidase (LiP), manganese peroxidase (MnP), and crude intracellular cell extracts. The multistep pathway involves the initial reduction of I to yield 2-amino-4-nitrotoluene (II). II is oxidized by MnP to yield 4-nitro-1,2-benzoquinone (XII) and methanol. XII is then reduced to 4-nitro-1,2-hydroquinone (V), and the latter is methylated to 1,2-dimethoxy-4-nitrobenzene (X). 4-Nitro-1,2-hydroquinone (V) is also oxidized by MnP to yield nitrite and 2-hydroxybenzoquinone, which is reduced to form 1,2,4-trihydroxybenzene (VII). 1,2-Dimethoxy-4-nitrobenzene (X) is oxidized by LiP to yield nitrite, methanol, and 2-methoxy-1,4-benzoquinone (VI), which is reduced to form 2-methoxy-1,4-hydroquinone (IX). The latter is oxidized by LiP and MnP to 4-hydroxy-1,2-benzoquinone, which is reduced to 1,2,4-trihydroxybenzene (VII). The key intermediate 1,2,4-trihydroxybenzene is ring cleaved by intracellular cell extracts to produce, after reduction, beta-ketoadipic acid. In this pathway, initial reduction of a nitroaromatic group generates the peroxidase substrate II. Oxidation of II releases methanol and generates 4-nitro-1,2-benzoquinone (XII), which is recycled by reduction and methylation reactions to regenerate intermediates which are in turn substrates for peroxidase-catalyzed oxidation leading to removal of the second nitro group. Thus, this unique pathway apparently results in the removal of both aromatic nitro groups before ring cleavage takes place.

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Selected References

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  1. Alic M., Letzring C., Gold M. H. Mating System and Basidiospore Formation in the Lignin-Degrading Basidiomycete Phanerochaete chrysosporium. Appl Environ Microbiol. 1987 Jul;53(7):1464–1469. doi: 10.1128/aem.53.7.1464-1469.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bryant C., DeLuca M. Purification and characterization of an oxygen-insensitive NAD(P)H nitroreductase from Enterobacter cloacae. J Biol Chem. 1991 Mar 5;266(7):4119–4125. [PubMed] [Google Scholar]
  3. Bumpus J. A., Tien M., Wright D., Aust S. D. Oxidation of persistent environmental pollutants by a white rot fungus. Science. 1985 Jun 21;228(4706):1434–1436. doi: 10.1126/science.3925550. [DOI] [PubMed] [Google Scholar]
  4. Buswell J. A., Ander P., Pettersson B., Eriksson K. E. Oxidative decarboxylation of vanillic acid by Sporotrichum pulverulentum. FEBS Lett. 1979 Jul 1;103(1):98–101. doi: 10.1016/0014-5793(79)81258-2. [DOI] [PubMed] [Google Scholar]
  5. Buswell J. A., Eriksson K. E. NAD(P)H dehydrogenase (quinone) from Sporotrichum pulverulentum. Methods Enzymol. 1988;161:271–274. doi: 10.1016/0076-6879(88)61029-9. [DOI] [PubMed] [Google Scholar]
  6. Chapman P. J., Ribbons D. W. Metabolism of resorcinylic compounds by bacteria: alternative pathways for resorcinol catabolism in Pseudomonas putida. J Bacteriol. 1976 Mar;125(3):985–998. doi: 10.1128/jb.125.3.985-998.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Decad G. M., Graichen M. E., Dent J. G. Hepatic microsomal metabolism and covalent binding of 2,4-dinitrotoluene. Toxicol Appl Pharmacol. 1982 Feb;62(2):325–334. doi: 10.1016/0041-008x(82)90131-4. [DOI] [PubMed] [Google Scholar]
  8. Fernando T., Bumpus J. A., Aust S. D. Biodegradation of TNT (2,4,6-trinitrotoluene) by Phanerochaete chrysosporium. Appl Environ Microbiol. 1990 Jun;56(6):1666–1671. doi: 10.1128/aem.56.6.1666-1671.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Glenn J. K., Gold M. H. Purification and characterization of an extracellular Mn(II)-dependent peroxidase from the lignin-degrading basidiomycete, Phanerochaete chrysosporium. Arch Biochem Biophys. 1985 Nov 1;242(2):329–341. doi: 10.1016/0003-9861(85)90217-6. [DOI] [PubMed] [Google Scholar]
  10. Gold M. H., Kuwahara M., Chiu A. A., Glenn J. K. Purification and characterization of an extracellular H2O2-requiring diarylpropane oxygenase from the white rot basidiomycete, Phanerochaete chrysosporium. Arch Biochem Biophys. 1984 Nov 1;234(2):353–362. doi: 10.1016/0003-9861(84)90280-7. [DOI] [PubMed] [Google Scholar]
  11. Kersten P. J., Tien M., Kalyanaraman B., Kirk T. K. The ligninase of Phanerochaete chrysosporium generates cation radicals from methoxybenzenes. J Biol Chem. 1985 Mar 10;260(5):2609–2612. [PubMed] [Google Scholar]
  12. Kinouchi T., Ohnishi Y. Purification and characterization of 1-nitropyrene nitroreductases from Bacteroides fragilis. Appl Environ Microbiol. 1983 Sep;46(3):596–604. doi: 10.1128/aem.46.3.596-604.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kirk T. K., Farrell R. L. Enzymatic "combustion": the microbial degradation of lignin. Annu Rev Microbiol. 1987;41:465–505. doi: 10.1146/annurev.mi.41.100187.002341. [DOI] [PubMed] [Google Scholar]
  14. McCormick N. G., Cornell J. H., Kaplan A. M. Identification of biotransformation products from 2,4-dinitrotoluene. Appl Environ Microbiol. 1978 May;35(5):945–948. doi: 10.1128/aem.35.5.945-948.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Orna M. V., Mason R. P. Correlation of kinetic parameters of nitroreductase enzymes with redox properties of nitroaromatic compounds. J Biol Chem. 1989 Jul 25;264(21):12379–12384. [PubMed] [Google Scholar]
  16. Peterson F. J., Mason R. P., Hovsepian J., Holtzman J. L. Oxygen-sensitive and -insensitive nitroreduction by Escherichia coli and rat hepatic microsomes. J Biol Chem. 1979 May 25;254(10):4009–4014. [PubMed] [Google Scholar]
  17. Rickert D. E., Butterworth B. E., Popp J. A. Dinitrotoluene: acute toxicity, oncogenicity, genotoxicity, and metabolism. Crit Rev Toxicol. 1984;13(3):217–234. doi: 10.3109/10408448409003373. [DOI] [PubMed] [Google Scholar]
  18. Rickert D. E., Long R. M. Metabolism and excretion of 2,4-dinitrotoluene in male and female Fischer 344 rats after different doses. Drug Metab Dispos. 1981 May-Jun;9(3):226–232. [PubMed] [Google Scholar]
  19. Smith P. K., Krohn R. I., Hermanson G. T., Mallia A. K., Gartner F. H., Provenzano M. D., Fujimoto E. K., Goeke N. M., Olson B. J., Klenk D. C. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985 Oct;150(1):76–85. doi: 10.1016/0003-2697(85)90442-7. [DOI] [PubMed] [Google Scholar]
  20. Spain J. C., Gibson D. T. Pathway for Biodegradation of p-Nitrophenol in a Moraxella sp. Appl Environ Microbiol. 1991 Mar;57(3):812–819. doi: 10.1128/aem.57.3.812-819.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Spain J. C., Wyss O., Gibson D. T. Enzymatic oxidation of p-nitrophenol. Biochem Biophys Res Commun. 1979 May 28;88(2):634–641. doi: 10.1016/0006-291x(79)92095-3. [DOI] [PubMed] [Google Scholar]
  22. Wariishi H., Dunford H. B., MacDonald I. D., Gold M. H. Manganese peroxidase from the lignin-degrading basidiomycete Phanerochaete chrysosporium. Transient state kinetics and reaction mechanism. J Biol Chem. 1989 Feb 25;264(6):3335–3340. [PubMed] [Google Scholar]
  23. Wariishi H., Gold M. H. Lignin peroxidase compound III. Mechanism of formation and decomposition. J Biol Chem. 1990 Feb 5;265(4):2070–2077. [PubMed] [Google Scholar]
  24. Zemper E. D., Black S. H. Morphology of freeze-etched Treponema refringens (Nichols). Arch Microbiol. 1978 Jun 26;117(3):227–238. doi: 10.1007/BF00738540. [DOI] [PubMed] [Google Scholar]

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