Chlorobenzoic acid degradation by Lentinus (Panus) tigrinus: In vivo and in vitro mechanistic study-evidence for P-450 involvement in the transformation

Journal of Hazardous Materials

Volumn 260, Issue , 2013, Pages 975-983

  Stella, T ^a,b,c   Covino, S ^a   Kresinova Z ^a   D'Annibale, A ^b   Petruccioli, M ^b   Cvancarova M ^a,c   Cajthaml, T ^a,c  

^a INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^b UNIVERSITY OF TUSCIA   (Italy)

^c CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Biodegradation; Chlorobenzoic acid; Cytochrome P 450 monooxygenase; Lentinus tigrinus; Ligninolytic enzymes

Indexed keywords

CHLOROBENZOIC ACID; CULTIVATION CONDITIONS; DEGRADATION INTERMEDIATES; DEGRADATION PROCESS; LIGNINOLYTIC ENZYMES; METHYLATION REACTION; MONOOXYGENASES; TIGRINUS;

ALKYLATION; BIODEGRADATION; CULTIVATION; HYDROXYLATION; ISOENZYMES; ISOMERS; PURIFICATION;

REACTION INTERMEDIATES;

CARBON MONOXIDE; CHLOROBENZOIC ACID DERIVATIVE; CYTOCHROME P450; GLUCOSE; LACCASE; MANGANESE PEROXIDASE; PIPERONYL BUTOXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

BIODEGRADATION; BIOTRANSFORMATION; CYTOCHROME; ENZYME ACTIVITY; INHIBITION; MUSHROOM; REDOX CONDITIONS;

ARTICLE; CHLORINATION; CONTROLLED STUDY; CULTURE MEDIUM; DEGRADATION; FUNGUS CULTURE; HYDROXYLATION; IN VITRO STUDY; IN VIVO STUDY; INCUBATION TIME; LENTINUS; LENTINUS TIGRINUS; MALT; METHYLATION; MICROSOME; NONHUMAN; OXIDATION REDUCTION REACTION; QUANTITATIVE ANALYSIS; REDUCTION;

BIODEGRADATION; CHLOROBENZOIC ACID; CYTOCHROME P-450 MONOOXYGENASE; LENTINUS TIGRINUS; LIGNINOLYTIC ENZYMES;

ALIIVIBRIO FISCHERI; BIODEGRADATION, ENVIRONMENTAL; BIOMASS; CHLORINE; CHLOROBENZOATES; CULTURE MEDIA; CYTOCHROME P-450 ENZYME SYSTEM; LACCASE; LENTINULA; LUMINESCENCE; MICROSOMES; OXYGEN; PEROXIDASES; SUBSTRATE SPECIFICITY; TOXICITY TESTS; WATER POLLUTANTS, CHEMICAL; WATER PURIFICATION;

EID: 84880773327     PISSN: 03043894     EISSN: 18733336     Source Type: Journal    
DOI: 10.1016/j.jhazmat.2013.07.004     Document Type: Article

References (46)

1. Field J.A., Sierra-Alvarez R. Microbial transformation of chlorinated benzoates. Environ. Sci. Biotechnol. 2008, 7:191-210.
2. Sorensen S.R., Holtze M.S., Simonsen A., Aamand J. Degradation and mineralization of nanomolar concentrations of the herbicide dichlobenil and its persistent metabolite 2,6-dichlorobenzamide by Aminobacter spp. isolated from dichlobenil-treated soils. Appl. Environ. Microb. 2007, 73:399-406.
3. Muccini M., Layton A.C., Sayler G.S., Schultz T.W. Aquatic toxicities of halogenated benzoic acids to Tetrahymena pyriformis. B. Environ. Contam. Toxicol. 1999, 62:616-622.
4. Zhao Y.H., Ji G.D., Cronin M.T.D., Dearden J.C. QSAR study of the toxicity of benzoic acids to Vibrio fischeri, Daphnia magna and carp. Sci. Total Environ. 1998, 216:205-215.
5. Lee P.Y., Chen C.Y. Toxicity and quantitative structure-activity relationships of benzoic acids to Pseudokirchneriella subcapitata. J. Hazard. Mater. 2009, 165:156-161.
6. Gichner T., Lovecká P., Vrchotová B. Genomic damage induced in tobacco plants by chlorobenzoic acids metabolic products of polychlorinated biphenyls. Mutat. Res. 2008, 657:140-145.
7. Svobodová K., Plačková M., Novotná V., Cajthaml T., Estrogenic androgenic activity of PCBs, their chlorinated metabolites and other endocrine disruptors estimated with two in vitro yeast assays. Sci. Total. Environ. 2009, 407:5921-5925.
8. Pieper D.H. Aerobic degradation of polychlorinated biphenyls. Appl. Microbiol. Biotechnol. 2005, 67:170-191.
9. Ohtsubo Y., Kudo T., Tsuda M., Nagata Y. Strategies for bioremediation of polychlorinated biphenyls. Appl. Microbiol. Biotechnol. 2004, 65:250-258.
10. Adebusoye S.A., Picardal F.W., Ilori M.O., Amund O.O. Influence of chlorobenzoic acids on the growth and degradation potentials of PCB-degrading microorganisms. World J. Microb. Biot. 2008, 24:1203-1208.
11. Furukawa K., Fujihara H. Microbial degradation of polychlorinated biphenyls: biochemical and molecular features. J. Biosci. Bioeng. 2008, 105:433-449.
12. Dietrich D., Hickey W.J., Lamar R.T. Degradation of 4,4'-dichlorobiphenyl, 3,3',4,4'-tetrachlorobiphenyl and 2,2',4,4',5,5'-hexachlorobiphenyl by the white rot fungus Phanerochaete chrysosporium. Appl. Environ. Microbiol. 1995, 61:3904-3909.
13. Reddy G.J.B., Gold M.H. Degradation of pentachlorophenol by Phanerochaete chrysosporium. Met. Enzym. 2000, 161:238-249.
14. Kamei I., Kogura R., Kondo R. Metabolism of 4,4'-dichlorobiphenyl by white rot fungi Phanerochaete chrysosporium and Phanerochaete sp. MZ142. Appl. Environ. Microbiol. 2006, 72:566-575.
15. Křesinová Z., Moeder M., Ezechiáš M., Svobodová K., Cajthaml T. Mechanistic study of 17 alpha-ethinylestradiol biodegradation by Pleurotus ostreatus: tracking of extracelullar and intracelullar degradation mechanisms. Environ. Sci. Technol. 2012, 46:13377-13385.
16. Cajthaml T., Erbanová P., Kollmann A., Novotný Č., Šašek V. Degradation of PAHs by ligninolytic enzymes of Irpex lacteus. Folia Microbiol. 2008, 53:289-294.
17. Cajthaml T., Křesinová Z., Svobodová K., Möder M. Biodegradation of endocrine disrupting compounds and suppression of estrogenic activity by ligninolytic fungi. Chemosphere 2009, 75:745-750.
18. Čvančarová M., Křesinová Z., Filipová A., Covino S., Cajthaml T. Biodegradation of PCBs by ligninolytic fungi and characterization of the degradation products. Chemosphere 2012, 88:1317-1323.
19. Dittmann J., Heyser W., Bücking H. Biodegradation of aromatic compounds by white rot and ectomycorrhizal fungal species and the accumulation of chlorinated benzoic acid in ectomycorrhizal pine seedlings. Chemosphere 2002, 49:297-306.
20. Muzikář M., Křesinová Z., Svobodová K., Filipová A., Čvančarová M., Cajthamlová K., Cajthaml T. Biodegradation of chlorobenzoic acids by ligninolytic fungi. J. Hazard. Mater. 2011, 196:386-394.
21. Federici E., Giubilei M.A., Santi G., Zanaroli G., Negroni A., Fava F., Petruccioli M., D'Annibale A. Bioaugmentation of a historically contaminated soil by polychlorinated biphenyls with Lentinus tigrinus. Microb. Cell Fact. 2012, 11:35.
22. Covino S., Čvančarová M., Muzikář M., Svobodova K., D'Annibale A., Petruccioli M., Federici F., Křesinová Z., Cajthaml T. An efficient PAH-degrading Lentinus (Panus) tigrinus strain: effect of inoculum formulation and pollutant bioavailability in solid matrices. J. Hazard. Mater. 2010, 183:669-676.
23. Kaal E.E.J., De Jong E., Field J.A. Stimulation of ligninolytic peroxidase activity by nitrogen nutrients in the white rot fungus Bjerkandera sp. strain BOS55. Appl. Environ. Microbiol. 1993, 59:4031-4036.
24. Cajthaml T., Erbanová P., Šašek V., Möder M. Breakdown products on metabolic pathway of degradation of benzo[a]anthracene by a white rot fungus. Chemosphere 2006, 64:560-564.
25. Lappalainen J., Juvonen R., Vaajasaari K., Karp M. A new flash method for measuring the toxicity of solid and colored samples. Chemosphere 1999, 38:1069-1083.
26. Quaratino D., Federici F., Petruccioli M., Fenice M., D'Annibale A. Production, purification and partial characterisation of a novel laccase from the white-rot fungus Panus tigrinus CBS 577.79. Antonie van Leeuwenhoek. 2007, 91:57-69.
27. Petruccioli M., Frasconi M., Quaratino D., Covino S., Favero G., Mazzei F., Federici F., D'Annibale A. Kinetic and redox properties of MnP II, a major manganese peroxidase isoenzyme from Panus tigrinus CBS 577.79. J. Biol. Inorg. Chem. 2009, 14:1153-1163.
28. Covino S., Svobodová K., Křesinová Z., Petruccioli M., Federici F., D'Annibale A., Čvančarová M., Cajthaml T. In vivo and in vitro polycyclic aromatic hydrocarbons degradation by Lentinus (Panus) tigrinus CBS 77.79. Bioresour. Technol. 2010, 101:3004-3012.
29. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
30. Omura T., Sato R. The carbon monoxide-binding pigment of liver microsomes. J. Biol. Chem. 1964, 239:2370-2378.
31. MacGregor J.F., Kourti T. Statistical process control of multivariate processes. Control Engin. Pract. 1995, 3:403-414.
32. Šašek V., Volfová O., Erbanová P., Vyas B.R.M., Matucha M. Degradation of PCBs by white rot fungi, methylotrophic and hydrocarbon utilizing yeasts and bacteria. Biotechnol. Lett. 1993, 15:521-526.
33. Quaratino D., Ciaffi M., Federici E., D'Annibale A. Response surface methodology study of Panus tigrinus laccase production in liquid cultures. Biochem. Eng. J. 2008, 39:236-245.
34. Vrchotová B., Macek T., Demnerová K., Macková M. Plant-bacteria cooperation on metabolisation of chlorobenzoic acids in soil. 5th International Symposium on Biosorption and Bioremediation 2012, pp: 64-67.
35. Goshorn R.H., Degering E.F., Tetrault P.A., Antiseptic bactericidal action of benzoic acid and inorganic salts. Effect of pH. Ind. Eng. Chem. 1938, 30:646-648.
36. Lodish H., Berk A., Zipursky S.L., Matsudaira P., Baltimore D., Darnell J. Molecular Cell Biology 2000, W.H. Freeman, New York. 4th edition.
37. Matsuzaki F., Shimizu M., Wariishi H., Proteomic metabolomic analyses of the white-rot fungus Phanerochaete chrysosporium exposed to exogenous benzoic acid. J. Proteome Res. 2008, 7:2342-2350.
38. Kamei I., Sonoki S., Haraguchi K., Kondo R. Fungal bioconversion of toxic polychlorinated biphenyls by white-rot fungus Phlebia brevispora. Appl. Microbiol. Biotechnol. 2006, 73:932-940.
39. Hage A., Schoemaker H.E., Field J.A. Reduction of aryl acids by white-rot fungi for the biocatalytic production of aryl aldehydes and alcohols. Appl. Microbiol. Biotechnol. 1999, 52:834-838.
40. Muheim A., Waldner R., Sanglard D., Reiser J., Schoemaker H.E., Leisola M.S.A. Purification and properties of an aryl-alcohol dehydrogenase from the white-rot fungus Phanerochaete chrysosporium. Eur. J. Biochem. 1991, 195:369-375.
41. Leontievsky A.A., Myasoedova N.M., Golovleva L.A., Sedaraty M., Evans C.S. Adaptation of the white rot basidiomycete Panus tigrinus for transformation of high concentrations of chlorophenols. Appl. Microbiol. Biotechnol. 2002, 59:599-604.
42. Lisov A.V., Leontievsky A.A., Golovleva L.A. Hybrid Mn-peroxidases from basidiomycetes. Appl. Biochem. Microbiol. 2007, 43:536-543.
43. Subramanian V., Yadav J.S. Role of P450 monooxygenases in the degradation of the endocrine-disrupting chemical nonylphenol by the white rot fungus Phanerochaete chrysosporium. Appl. Environ. Microbiol. 2009, 75:5570-5580.
44. Van Gorcom R.F.M., Boschloo J.G., Kuijvenhoven A., Lange J., Van Vark A.J., Bos C.J., Van Balken J.A.M., Pouwels P.H., Van den Hondel C.A.M.J.J. Isolation and molecular characterisation of the benzoate-para-hydrolase gene (BphA) of Aspergillus niger. A member of a new gene family of the cytochrome P450 superfamily. Mol. Gen. Genet. 1990, 223:192-197.
45. Boschloo J.G., Paffen A., Koot T., Van den Tweel W.J.J., Van Gorcom R.F.M., Cordewener J.H.G., Bos C.J. Genetic analysis of benzoate metabolism in Aspergillus niger. Appl. Microbiol. Biotechnol. 1990, 34:225-228.
46. Matsuzaki F., Wariishi H. Molecular characterization of cytochrome P450 catalyzing hydroxylation of benzoates from the white-rot fungus Phanerochaete chrysosporium. Biochem. Biophys Res. Commun. 2005, 334:1184-1190.