Biochemical and physicochemical processes contributing to the removal of endocrine-disrupting chemicals and pharmaceuticals by the aquatic ascomycete Phoma sp. UHH 5-1-03

Applied Microbiology and Biotechnology

Volumn 100, Issue 5, 2016, Pages 2381-2399

  Hofmann, Ulrike ^a   Schlosser, Dietmar ^a  

^a HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

Author keywords

Aquatic fungi; Biosorption; Biotransformation; Laccase; Metabolite formation; Micropollutants

Indexed keywords

AMIDES; BIOCONVERSION; BIOMOLECULES; BIOSORPTION; CARBOXYLATION; CELLS; CYTOLOGY; ENDOCRINE DISRUPTERS; FUNGI; HYDROXYLATION; MASS SPECTROMETRY; METABOLITES; PHENOLS;

AQUATIC FUNGI; BIOTRANSFORMATION; CYTOCHROME P450 MONOOXYGENASES; DECARBOXYLATION REACTIONS; ENDOCRINE DISRUPTING CHEMICALS; HYDROXYLATED METABOLITES; LACCASES; MICROPOLLUTANTS;

ENZYMES;

4,4' ISOPROPYLIDENEDIPHENOL; CARBAMAZEPINE; DICLOFENAC; ENDOCRINE DISRUPTOR; ETHINYLESTRADIOL; FORMAMIDE; LACCASE; NONYLPHENOL; SULFAMETHOXAZOLE; TRICLOSAN; FRESH WATER; WATER POLLUTANT;

BIOACCUMULATION; BIOCHEMICAL COMPOSITION; BIOREMEDIATION; BIOTRANSFORMATION; CHEMICAL REACTION; DRUG; ENDOCRINE DISRUPTOR; ENZYME ACTIVITY; FRESHWATER ENVIRONMENT; FUNGUS; METABOLITE; PHYSICOCHEMICAL PROPERTY; POLLUTANT REMOVAL;

ARTICLE; BIOCHEMISTRY; BIODEGRADATION; BIOSORPTION; BIOTRANSFORMATION; CHEMICAL STRUCTURE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYCLIZATION; DEAMINATION; DECARBOXYLATION; DRY WEIGHT; ENZYME ACTIVITY; ENZYME MECHANISM; FUNGAL BIOMASS; FUNGAL METABOLISM; FUNGAL STRAIN; FUNGUS CULTURE; HYDROPHOBICITY; HYDROXYLATION; MOLECULAR WEIGHT; MYCELIUM; NONHUMAN; OXIDATION; OXIDATIVE COUPLING; PH; PHOMA; PHYSICAL CHEMISTRY; WATER POLLUTION; ADSORPTION; ASCOMYCETES; CHEMICAL PHENOMENA; CHEMISTRY; MASS SPECTROMETRY; METABOLISM; MICROBIOLOGY; WATER POLLUTANT;

FUNGI; PHOMA;

ADSORPTION; ASCOMYCOTA; BIOTRANSFORMATION; CHEMICAL PHENOMENA; ENDOCRINE DISRUPTORS; FRESH WATER; MASS SPECTROMETRY; METABOLIC NETWORKS AND PATHWAYS; WATER POLLUTANTS, CHEMICAL;

EID: 84958849250     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-015-7113-0     Document Type: Article

References (84)

1. Ammann E, Gasser C, Hommes G, Corvini PX (2014) Immobilization of defined laccase combinations for enhanced oxidation of phenolic contaminants. Appl Microbiol Biotechnol 98(3):1397–1406. doi:10.1007/s00253-013-5055-y
2. Ardao I, Magnin D, Agathos SN (2015) Bioinspired production of magnetic laccase-biotitania particles for the removal of endocrine disrupting chemicals. Biotech Bioeng 112(10):1986–1996. doi:10.1002/bit.25612
3. Badia-Fabregat M, Rosell M, Caminal G, Vicent T, Marco-Urrea E (2014) Use of stable isotope probing to assess the fate of emerging contaminants degraded by white-rot fungus. Chemosphere 103:336–342. doi:10.1016/j.chemosphere.2013.12.029
4. Blanchette RA, Abad AR, Farrell RL, Leathers TD (1989) Detection of lignin peroxidase and xylanase by immunocytochemical labeling in wood decayed by basidiomycetes. Appl Environ Microb 55(6):1457–1465
5. Cabana H, Jiwan J-LH, Rozenberg R, Elisashvili V, Penninckx M, Agathos SN, Jones JP (2007) Elimination of endocrine disrupting chemicals nonylphenol and bisphenol A and personal care product ingredient triclosan using enzyme preparation from the white rot fungus Coriolopsis polyzona. Chemosphere 67(4):770–778. doi:10.1016/j.chemosphere.2006.10.037
6. Cajthaml T (2014) Biodegradation of endocrine-disrupting compounds by ligninolytic fungi: mechanisms involved in the degradation. Environ Microbiol, article first published online: 18 April 2014 doi:10.1111/1462-2920.12460
7. Camarero S, Ibarra D, Martínez ÁT, Romero J, Gutiérrez A, del Río JC (2007) Paper pulp delignification using laccase and natural mediators. Enzyme Microb Technol 40(5):1264–1271. doi:10.1016/j.enzmictec.2006.09.016
8. Castiglioni S, Bagnati R, Calamari D, Fanelli R, Zuccato E (2005) A multiresidue analytical method using solid-phase extraction and high-pressure liquid chromatography tandem mass spectrometry to measure pharmaceuticals of different therapeutic classes in urban wastewaters. J Chromatogr A 1092(2):206–215. doi:10.1016/j.chroma.2005.07.012
9. Castiglioni S, Bagnati R, Fanelli R, Pomati F, Calamari D, Zuccato E (2006) Removal of pharmaceuticals in sewage treatment plants in Italy. Environ Sci Technol 40(1):357–363
10. Chau HW, Si BC, Goh YK, Vujanovic V (2009) A novel method for identifying hydrophobicity on fungal surfaces. Mycol Res 113(10):1046–1052. doi:10.1016/j.mycres.2009.06.007
11. Chen B, Wang Y, Hu D (2010) Biosorption and biodegradation of polycyclic aromatic hydrocarbons in aqueous solutions by a consortium of white-rot fungi. J Hazard Mater 179(1–3):845–851
12. Daniel G, Nilsson T, Pettersson B (1989) Intra- and extracellular localization of lignin peroxidase during the degradation of solid wood and wood fragments by Phanerochaete chrysosporium by using transmission electron microscopy and immuno-gold labeling. Appl Environ Microbiol 55(4):871–881
13. Dann AB, Hontela A (2011) Triclosan: environmental exposure, toxicity and mechanisms of action. J Appl Toxicol 31(4):285–311
14. de Ridder DJ, Villacorte L, Verliefde AR, Verberk JQ, Heijman SG, Amy GL, van Dijk JC (2010) Modeling equilibrium adsorption of organic micropollutants onto activated carbon. Water Res 44(10):3077–3086. doi:10.1016/j.watres.2010.02.034
15. Delgado LF, Faucet-Marquis V, Pfohl-Leszkowicz A, Dorandeu C, Marion B, Schetrite S, Albasi C (2011) Cytotoxicity micropollutant removal in a crossflow membrane bioreactor. Bioresource Technol 102(6):4395–4401. doi:10.1016/j.biortech.2010.12.107
16. Eibes G, Debernardi G, Feijoo G, Moreira MT, Lema JM (2011) Oxidation of pharmaceutically active compounds by a ligninolytic fungal peroxidase. Biodegradation 22(3):539–550
17. EU (2013) Directive 2013/39/EU of the European parliament and of the council of 12 August 2013 amending directives 2000/60/EC and 2008/105/EC as regards priority substances in the field of water policy. Brussels, Belgium
18. Fernandez-Sanchez C, Tzanov T, Gübitz GM, Cavaco-Paulo A (2002) Voltammetric monitoring of laccase-catalysed mediated reactions. Bioelectrochemistry 58(2):149–156
19. Gil-ad NL, Bar-Nun N, Mayer AM (2001) The possible function of the glucan sheath of Botrytis cinerea: effects on the distribution of enzyme activities. FEMS Microbiol Lett 199(1):109–113. doi:10.1016/S0378-1097(01)00165-3
20. Golan-Rozen N, Chefetz B, Ben-Ari J, Geva J, Hadar Y (2011) Transformation of the recalcitrant pharmaceutical compound carbamazepine by Pleurotus ostreatus: role of cytochrome P450 monooxygenase and manganese peroxidase. Environ Sci Technol 45(16):6800–6805. doi:10.1021/es200298t
21. Grassi M, Rizzo L, Farina A (2013) Endocrine disruptors compounds, pharmaceuticals and personal care products in urban wastewater: implications for agricultural reuse and their removal by adsorption process. Environ Sci Pollut R 20(6):3616–3628. doi:10.1007/s11356-013-1636-7
22. Hai FI, Nghiem LD, Khan SJ, Price WE, Yamamoto K (2013) Wastewater reuse: removal of emerging trace organic contaminants. In: Hai FI, Yamamoto K, Lee C-H (eds) Membrane biological reactors. IWA Publishing, London, UK, pp 163–203
23. Hanano A, Shaban M, Almousally I, Al-Ktaifani M (2015) Saccharomyces cerevisiae SHSY detoxifies petroleum n-alkanes by an induced CYP52A58 and an enhanced order in cell surface hydrophobicity. Chemosphere 135:418–426. doi:10.1016/j.chemosphere.2014.11.011
24. Harms H, Schlosser D, Wick LY (2011) Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat Rev Micro 9(3):177–192
25. Hata T, Kawai S, Okamura H, Nishida T (2010a) 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(5):681–689. doi:10.1007/s10532-010-9334-3
26. Hata T, Shintate H, Kawai S, Okamura H, Nishida T (2010b) Elimination of carbamazepine by repeated treatment with laccase in the presence of 1-hydroxybenzotriazole. J Hazard Mater 181(1–3):1175–1178. doi:10.1016/j.jhazmat.2010.05.103
27. Hundt K, Martin D, Hammer E, Jonas U, Kindermann MK, Schauer F (2000) Transformation of triclosan by Trametes versicolor and Pycnoporus cinnabarinus. Appl Environ Microbiol 66(9):4157–4160. doi:10.1128/aem.66.9.4157-4160.2000
28. Jackson J, Sutton R (2008) Sources of endocrine-disrupting chemicals in urban wastewater, Oakland, CA. Sci Total Environ 405(1–3):153–160. doi:10.1016/j.scitotenv.2008.06.033
29. Jahangiri E, Reichelt S, Thomas I, Hausmann K, Schlosser D, Schulze A (2014) Electron beam-induced immobilization of laccase on porous supports for waste water treatment applications. Molecules 19(8):11860–11882
30. Johannes C, Majcherczyk A (2000) Laccase activity tests and laccase inhibitors. J Biotechnol 78(2):193–199. doi:10.1016/S0168-1656(00)00208-X
31. Johnsen AR, Wick LY, Harms H (2005) Principles of microbial PAH-degradation in soil. Environ Pollut 133(1):71–84. doi:10.1016/j.envpol.2004.04.015
32. Junghanns C, Krauss G, Schlosser D (2008a) Potential of aquatic fungi derived from diverse freshwater environments to decolourise synthetic azo and anthraquinone dyes. Bioresource Technol 99(5):1225–1235. doi:10.1016/j.biortech.2007.02.015
33. Junghanns C, Moeder M, Krauss G, Martin C, Schlosser D (2005) Degradation of the xenoestrogen nonylphenol by aquatic fungi and their laccases. Microbiology-SGM 151:45–57. doi:10.1099/mic.0.27431-0
34. Junghanns C, Neumann JF, Schlosser D (2012) Application of the aquatic fungus Phoma sp. (DSM22425) in bioreactors for the treatment of textile dye model effluents. J Chem Technol Biotechnol 87:1276–1283
35. Junghanns C, Parra R, Keshavarz T, Schlosser D (2008b) Towards higher laccase activities produced by aquatic ascomycetous fungi through combination of elicitors and an alternative substrate. Eng Life Sci 8(3):277–285. doi:10.1002/elsc.200800042
36. Junghanns C, Pecyna MJ, Böhm D, Jehmlich N, Martin C, von Bergen M, Schauer F, Hofrichter M, Schlosser D (2009) Biochemical and molecular genetic characterisation of a novel laccase produced by the aquatic ascomycete Phoma sp. UHH 5-1-03. Appl Microbiol Biotechnol 84(6):1095–1105. doi:10.1007/s00253-009-2028-2
37. Kang S-I, Kang S-Y, Hur H-G (2008) Identification of fungal metabolites of anticonvulsant drug carbamazepine. Appl Microbiol Biotechnol 79(4):663–669. doi:10.1007/s00253-008-1459-5
38. Kim YJ, Nicell JA (2006) Impact of reaction conditions on the laccase-catalyzed conversion of bisphenol A. Bioresource Technol 97(12):1431–1442
39. Krauss G-J, Solé M, Krauss G, Schlosser D, Wesenberg D, Bärlocher F (2011) Fungi in freshwaters: ecology, physiology and biochemical potential. FEMS Microbiol Rev 35(4):620–651. doi:10.1111/j.1574-6976.2011.00266.x
40. Kresinova Z, Moeder M, Ezechias M, Svobodova K, Cajthaml T (2012) Mechanistic study of 17α-ethinylestradiol biodegradation by Pleurotus ostreatus: tracking of extracelullar and intracelullar degradation mechanisms. Environ Sci Technol 46(24):13377–13385. doi:10.1021/es3029507
41. Kümmerer K (2011) Emerging contaminants. Treatise on water science. Elsevier, Oxford, pp 69–87
42. Larcher S, Yargeau V (2012) Biodegradation of sulfamethoxazole: current knowledge and perspectives. Appl Microbiol Biotechnol 96(2):309–318
43. Lee SM, Koo BW, Choi JW, Choi DH, An BS, Jeung EB, Choi IG (2005) Degradation of bisphenol A by white rot fungi, Stereum hirsutum and Heterobasidium insulare, and reduction of its estrogenic activity. Biol Pharm Bull 28(2):201–207
44. Libardi Junior N, Miranda Gern RM, Furlan SA, Schlosser D (2012) Laccase production by the aquatic ascomycete Phoma sp UHH 5-1-03 and the white rot basidiomycete Pleurotus ostreatus DSM 1833 during submerged cultivation on banana peels and enzyme applicability for the removal of endocrine-disrupting chemicals. Appl Biochem Biotech 167(5):1144–1156. doi:10.1007/s12010-012-9601-3
45. Linder MB, Szilvay GR, Nakari-Setälä T, Penttilä ME (2005) Hydrophobins: the protein-amphiphiles of filamentous fungi. FEMS Microbiol Rev 29(5):877–896. doi:10.1016/j.femsre.2005.01.004
46. Luo Y, Guo W, Ngo HH, Nghiem LD, Hai FI, Zhang J, Liang S, Wang XC (2014) A review on the occurrence of micropollutants in the aquatic environment and their fate and removal during wastewater treatment. Sci Total Environ 474:619–641
47. Marco-Urrea E, Pérez-Trujillo M, Cruz-Morató C, Caminal G, Vicent T (2010) Degradation of the drug sodium diclofenac by Trametes versicolor pellets and identification of some intermediates by NMR. J Hazard Mater 176(1–3):836–842. doi:10.1016/j.jhazmat.2009.11.112
48. Marco-Urrea E, Perez-Trujillo M, Vicent T, Caminal G (2009) Ability of white-rot fungi to remove selected pharmaceuticals and identification of degradation products of ibuprofen by Trametes versicolor. Chemosphere 74(6):765–772. doi:10.1016/j.chemosphere.2008.10.040
49. Margot J, Kienle C, Magnet A, Weil M, Rossi L, de Alencastro LF, Abegglen C, Thonney D, Chevre N, Scharer M, Barry DA (2013) Treatment of micropollutants in municipal wastewater: ozone or powdered activated carbon? Sci Total Environ 462:480–498
50. Martin C, Moeder M, Daniel X, Krauss G, Schlosser D (2007) Biotransformation of the polycyclic musks HHCB and AHTN and metabolite formation by fungi occurring in freshwater environments. Environ Sci Technol 41(15):5395–5402
51. Murray KE, Thomas SM, Bodour AA (2010) Prioritizing research for trace pollutants and emerging contaminants in the freshwater environment. Environ Pollut 158(12):3462–3471. doi:10.1016/j.envpol.2010.08.009
52. Murugesan K, Chang Y-Y, Kim Y-M, Jong-Rok J, Kim E-J, Chang Y-S (2010) Enhanced transformation of triclosan by laccase in the presence of redox mediators. Water Res 44(1):298–308. doi:10.1016/j.watres.2009.09.058
53. Nazly N, Knowles CJ, Beardsmore AJ, Naylor WT, Corcoran EG (1983) Detoxification of cyanide by immobilised fungi. J Chem Tech Biot B 33(2):119–126. doi:10.1002/jctb.280330207
54. Nguyen LN, Hai FI, Yang S, Kang J, Leusch FDL, Roddick F, Price WE, Nghiem LD (2014) Removal of pharmaceuticals, steroid hormones, phytoestrogens, UV-filters, industrial chemicals and pesticides by Trametes versicolor: role of biosorption and biodegradation. Int Biodeter Biodegr 88:169–175. doi:10.1016/j.ibiod.2013.12.017
55. Nicole M, Chamberland H, Rioux D, Lecours N, Rio B, Geiger JP, Ouellette GB (1993) A cytochemical study of extracellular sheaths associated with Rigidoporus lignosus during wood decay. Appl Environ Microbiol 59(8):2578–2588
56. Nodler K, Licha T, Barbieri M, Perez S (2012) Evidence for the microbially mediated abiotic formation of reversible and non-reversible sulfamethoxazole transformation products during denitrification. Water Res 46(7):2131–2139. doi:10.1016/j.watres.2012.01.028
57. Palomo ME, Ballesteros MP, Frutos P (1999) Analysis of diclofenac sodium and derivatives. J Pharmaceut Biomed 21(1):83–94. doi:10.1016/S0731-7085(99)00089-8
58. Ranjith NK, Sasikala C, Ramana CV (2007) Catabolism of L-phenylalanine and L-tyrosine by Rhodobacter sphaeroides OU5 occurs through 3,4-dihydroxyphenylalanine. Res Microbiol 158(6):506–511. doi:10.1016/j.resmic.2007.04.008
59. Rodarte-Morales AI, Feijoo G, Moreira MT, Lema JM (2011) Degradation of selected pharmaceutical and personal care products (PPCPs) by white-rot fungi. World J Microb Biot 27(8):1839–1846 doi:10.1007/s11274-010-0642-x
60. Rodarte-Morales AI, Moreira MT, Feijoo G, Lema JM (2010) Evaluation of two fungal strains for the degradation of pharmaceutical and personal care products. Chem Eng Trans 20:31–36
61. Semple KT, Doick KJ, Wick LY, Harms H (2007) Microbial interactions with organic contaminants in soil: definitions, processes and measurement. Environ Pollut 150(1):166–176. doi:10.1016/j.envpol.2007.07.023
62. Singh S, Harms H, Schlosser D (2014) Screening of ecologically diverse fungi for their potential to pretreat lignocellulosic bioenergy feedstock. Appl Microbiol Biotechnol 98(7):3355–3370. doi:10.1007/s00253-014-5563-4
63. Spina F, Cordero C, Schilirò T, Sgorbini B, Pignata C, Gilli G, Bicchi C, Varese GC (2015) Removal of micropollutants by fungal laccases in model solution and municipal wastewater: evaluation of estrogenic activity and ecotoxicity. J Clean Prod 100:185–194. doi:10.1016/j.jclepro.2015.03.047
64. Stanier RY, Palleroni NJ, Doudoroff M (1966) The aerobic pseudomonads: a taxonomic study. J Gen Microbiol 43(2):159–271
65. Suárez S, Carballa M, Omil F, Lema J (2008) How are pharmaceutical and personal care products (PPCPs) removed from urban wastewaters? Rev Environ Sci Biotechnol 7(2):125–138. doi:10.1007/s11157-008-9130-2
66. Suzuki K, Hirai H, Murata H, Nishida T (2003) Removal of estrogenic activities of 17beta-estradiol and ethinylestradiol by ligninolytic enzymes from white rot fungi. Water Res 37(8):1972–1975
67. Syed K, Shale K, Pagadala NS, Tuszynski J (2014) Systematic identification and evolutionary analysis of catalytically versatile cytochrome P450 monooxygenase families enriched in model basidiomycete fungi. PLoS One 9(1):e86683. doi:10.1371/journal.pone.0086683
68. Synytsya A, Novák M (2013) Structural diversity of fungal glucans. Carbohyd Polym 92(1):792–809. doi:10.1016/j.carbpol.2012.09.077
69. Thatcher RC, Weaver TL (1976) Carbon-nitrogen cycling through microbial formamide metabolism. Science 192(4245):1234–1235. doi:10.1126/science.192.4245.1234
70. Touahar IE, Haroune L, Ba S, Bellenger J-P, Cabana H (2014) Characterization of combined cross-linked enzyme aggregates from laccase, versatile peroxidase and glucose oxidase, and their utilization for the elimination of pharmaceuticals. Sci Total Environ 481:90–99. doi:10.1016/j.scitotenv.2014.01.132
71. Tran NH, Urase T, Kusakabe O (2010) Biodegradation characteristics of pharmaceutical substances by whole fungal culture Trametes versicolor and its laccase. J Water Environ Technol 8(2):125–140. doi:10.2965/jwet.2010.125
72. Travkin V, Baskunov BP, Golovlev EL, Boersma MG, Boeren S, Vervoort J, van Berkel WJH, Rietjens IMCM, Golovleva LA (2002) Reductive deamination as a new step in the anaerobic microbial degradation of halogenated anilines. FEMS Microbiol Lett 209(2):307–312. doi:10.1111/j.1574-6968.2002.tb11149.x
73. Tsutsumi Y, Haneda T, Nishida T (2001) Removal of estrogenic activities of bisphenol A and nonylphenol by oxidative enzymes from lignin-degrading basidiomycetes. Chemosphere 42(3):271–276
74. Uchida H, Fukuda T, Miyamoto H, Kawabata T, Suzuki M, Uwajima T (2001) Polymerization of bisphenol A by purified laccase from Trametes villosa. Biochem Biophys Res Commun 287(2):355–358
75. van Leeuwen JS, Vredenburg G, Dragovic S, Tjong TFJ, Vos JC, Vermeulen NPE (2011) Metabolism related toxicity of diclofenac in yeast as model system. Toxicol Lett 200(3):162–168. doi:10.1016/j.toxlet.2010.11.010
76. Wang J, Majima N, Hirai H, Kawagishi H (2012) Effective removal of endocrine-disrupting compounds by lignin peroxidase from the white-rot fungus Phanerochaete sordida YK-624. Curr Microbiol 64(3):300–303
77. Wang J, Yamada Y, Notake A, Todoroki Y, Tokumoto T, Dong J, Thomas P, Hirai H, Kawagishi H (2014) Metabolism of bisphenol A by hyper lignin-degrading fungus Phanerochaete sordida YK-624 under non-ligninolytic condition. Chemosphere 109:128–133. doi:10.1016/j.chemosphere.2014.01.029
78. Wang J, Yamamoto R, Yamamoto Y, Tokumoto T, Dong J, Thomas P, Hirai H, Kawagishi H (2013) Hydroxylation of bisphenol A by hyper lignin-degrading fungus Phanerochaete sordida YK-624 under non-ligninolytic condition. Chemosphere 93(7):1419–1423. doi:10.1016/j.chemosphere.2013.07.026
79. Webster R, Pacey M, Winchester T, Johnson P, Jezequel S (1998) Microbial oxidative metabolism of diclofenac: production of 4'-hydroxydiclofenac using Epiccocum nigrum IMI354292. Appl Microbiol Biotechnol 49(4):371–376
80. Witorsch RJ (2014) Critical analysis of endocrine disruptive activity of triclosan and its relevance to human exposure through the use of personal care products. Crit Rev Toxicol 44(6):535–555. doi:10.3109/10408444.2014.910754
81. Woolley JL Jr, Sigel CW (1982) The role of dietary nitrate and nitrite in the reductive deamination of sulfadiazine by the rat, guinea pig, and neonatal calf. Life Sci 30(25):2229–2234
82. Yang S, Hai FI, Nghiem LD, Price WE, Roddick F, Moreira MT, Magram SF (2013a) Understanding the factors controlling the removal of trace organic contaminants by white-rot fungi and their lignin modifying enzymes: a critical review. Bioresource Technol 141:97–108. doi:10.1016/j.biortech.2013.01.173
83. Yang S, Hai FI, Nghiem LD, Roddick F, Price WE (2013b) Removal of trace organic contaminants by nitrifying activated sludge and whole-cell and crude enzyme extract of Trametes versicolor. Water Sci Technol 67(6):1216–1223. doi:10.2166/wst.2013.684
84. Zhang Y, Geissen SU (2010) In vitro degradation of carbamazepine and diclofenac by crude lignin peroxidase. J Hazard Mater 176(1–3):1089–1092