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Fungal-Mediated Biodegradation of Ingredients in Personal Care Products

  • M. Silvia Díaz-CruzEmail author
  • Pablo Gago-Ferrero
  • Marina Badia-Fabregat
  • Gloria Caminal
  • Teresa Vicent
  • Damià Barceló
Chapter
Part of the The Handbook of Environmental Chemistry book series (HEC, volume 36)

Abstract

Many efforts have been devoted in developing technologies to remove emerging organic pollutants from freshwater systems. This chapter examined the applications of the environmental friendly technology based on fungal-mediated treatment for the degradation of ingredients in personal care products (PCPs), which are frequently detected at relevant concentrations in the aquatic environment. PCPs are daily-use products used in large quantity that includes several groups of substances (UV filters, preservatives, fragrances, etc.). Removal efficiencies reported varied significantly among different experimental set-up, organic substance, and type of fungi. The mechanisms and factors governing the degradation of PCPs by fungi, mainly white-rot fungi and their specific lignin-modifying enzymes, are reviewed and discussed. Beyond, the identification of the intermediate products and metabolites produced as well as the degradation pathways available for some PCPs are presented.

Keywords

Biocides Biodegradation Enzymes Fragrances Insect repellents Metabolites Parabens Personal care products Redox mediators Sewage sludge Triclosan UV filters Wastewater White-rot fungi 

Abbreviations

1-HBT

1-Hydroxybenzotriazole

4DHB

4-Dihydroxybenzophenone

4-MBC

4-Methylbenzylidene camphor

ABTS

2,2′-Azino-bis(3-ethylbenzothiazoline-6-sulfonic acid

AOPs

Advanced oxidation processes

BP1

Benzophenone 1

BP3

Benzophenone 3

CAS

Conventional activated sludge

CLEAs

Cross-linking of enzyme aggregates

dw

Dry weight

DEET

N,N-Diethyl-meta-toluamide

DMP

2,6-Dimethoxyphenol

EDC

Endocrine-disrupting chemicals

FBR

Fluidized bed reactor

GOD

Glucose oxidase

Km

Michaelis–Menten constant

Kow

Octanol–water partition coefficient

l.w.

Lipid weight

LIPs

Lignin peroxidases

LMEs

Lignin-modifying enzymes

MBR

Membrane bioreactor

MnPs

Manganese-dependent peroxidases

MS

Mass spectrometry

MS/MS

Tandem mass spectrometry

NCPA

N-(4-Cyanophenyl)acetohydroxamic acid

NHA

N-Hydroxyacetanilide

OC

Octocrylene

PAHs

Polycyclic aromatic hydrocarbons

PBR

Packed bed reactor

PCBs

Polychlorinated biphenyls

PCPs

Personal care products

PEG

Poly-(ethylene glycol)

POPs

Persistent organic pollutants

TCS

Triclosan

TNT

Trinitrotoluene

TrOC

Trace organic contaminant

UV-F

UV filters

VP

Versatile peroxidases

WRF

White-rot fungi

Notes

Acknowledgements

This work has been financially supported by the Generalitat de Catalunya (Consolidated Research Group “2014 SGR 418 – Water and Soil Quality Unit”).

References

  1. 1.
    Jobling S, Casey D, Rodgers-Gray T, Oehlmann J, Schulte-Oehlmann U, Pawlowski S, Baunbeck T, Turner AP, Tyler CR (2003) Comparative responses of molluscs and fish to environmental estrogens and an estrogenic effluent. Aquat Toxicol 65:205–220CrossRefGoogle Scholar
  2. 2.
    Ishibashi H, Matsumura N, Hirano M, Matsuoka M, Shiratsuchi H, Ishibashi Y, Takao Y, Arizono K (2004) Effects of triclosan on the early life stages and reproduction of medaka Oryzias latipes and induction of hepatic vitellogenin. Aquat Toxicol 67:167–179CrossRefGoogle Scholar
  3. 3.
    Klaschka U, Carsten von der Ohe P, Bschorer A, Krezmer S, Sengl M, Letzel M (2013) Occurrences and potential risks of 16 fragrances in five German sewage plants and their receiving waters. Environ Sci Pollut Res 20:2456–2471CrossRefGoogle Scholar
  4. 4.
    Cabeza Y, Candela L, Ronen D, Teijon G (2012) Monitoring the occurrence of emerging contaminants in treated wastewater and groundwater between 2008 and 2010. The Baix Llobregat (Barcelona, Spain). J Hazard Mater 239–240:32–39CrossRefGoogle Scholar
  5. 5.
    Alexander JT, Hai FI, Al-aboud T (2012) Chemical coagulation-based processes for trace organic contaminant removal: current state and future potential. J Environ Manage 111:195–207CrossRefGoogle Scholar
  6. 6.
    Wright JM, Schwartz J, Dockery DW (2004) The effect of disinfection by-products and mutagenic activity on birth weight and gestational duration. Environ Health Perspect 112(8):920–925CrossRefGoogle Scholar
  7. 7.
    Díaz-Cruz MS, Barceló D (2009) Chemical analysis and ecotoxicological effects of organic UV-absorbing compounds in aquatic ecosystems. Trends Anal Chem 28:708–717CrossRefGoogle Scholar
  8. 8.
    García-Galán MJ, Díaz-Cruz MS, Barceló D (2011) Occurrence of sulfonamide residues along the Ebro river basin. Removal in wastewater treatment plants and environmental risk assessment. Environ Int 37:462–473CrossRefGoogle Scholar
  9. 9.
    Gago-Ferrero P, Díaz-Cruz MS, Barceló D (2011) Occurrence of multiclass UV filters in treated sewage sludge from wastewater treatment plants. Chemosphere 84:795–806CrossRefGoogle Scholar
  10. 10.
    Ternes TA, Herrmann N, McDowell D, Ried A, Kampmann M, Teiser B (2003) Ozonation: a tool for removal of pharmaceuticals, contrast media and musk fragrances from wastewater? Water Res 37:1976–1982CrossRefGoogle Scholar
  11. 11.
    Gago-Ferrero P, Demeestere K, Díaz-Cruz MS, Barceló D (2013) Ozonation and peroxone oxidation process of BP3 in water: kinetics, parametric study and identification of intermediate products. Sci Total Environ 443:209–217CrossRefGoogle Scholar
  12. 12.
    Clara M, Strenn B, Gans O, Martınez E, Kreuzinger N, Kroiss H (2005) Removal of selected pharmaceuticals, fragrances and endocrine disrupting compounds in a membrane bioreactor and conventional wastewater treatment plants. Water Res 39:4797–4807CrossRefGoogle Scholar
  13. 13.
    Ikehata K, Naghashkar N, El-Din MG (2006) Degradation of aqueous pharmaceuticals by ozonation and advanced oxidation processes: a review. Ozone Sci Eng 28:353–414CrossRefGoogle Scholar
  14. 14.
    Esplugas S, Bila DM, Krause LGT, Dezotti M (2007) Ozonation and advanced oxidation technologies to remove endocrine disrupting chemicals (EDCs) and pharmaceuticals and personal care products (PPCPs) in water effluents. J Hazard Mater 149:631–642CrossRefGoogle Scholar
  15. 15.
    Reif R, Suarez S, Omil F, Lema JM (2008) Fate of pharmaceuticals and cosmetic ingredients during the operation of a MBR treating sewage. Desalination 221:511–517CrossRefGoogle Scholar
  16. 16.
    García-Galán MJ, Frömel T, Müller J, González S, López R, Peschka M, Knepper T, Díaz-Cruz MS, Barceló D (2012) Biodegradation studies of N4acetylsulfapyridine and N4-acetylsulfamethazine in environmental water applying mass spectrometry techniques. Anal Bioanal Chem 402:2885–2896CrossRefGoogle Scholar
  17. 17.
    Gao D, Du L, Yang J, Wu WM, Liang H (2010) A critical review of the application of white rot fungi to environmental pollution control. Crit Rev Biotechnol 30:70–77CrossRefGoogle Scholar
  18. 18.
    Ding J, Cong J, Zhou J, Gao S (2008) Polycyclic aromatic hydrocarbon biodegradation and extracellular enzyme secretion in agitated and stationary cultures of Phanerochaete chrysosporium. J Environ Sci 20:88–93CrossRefGoogle Scholar
  19. 19.
    Quintero JC, Lu-Chau TA, Moreira MT, Feijoo G, Lema JM (2007) Bioremediation of HCH present in soil by the white rot fungi Bjerkandera adusta in a slurry batch reactor. Int Biodeter Biodegrad 60:319–326CrossRefGoogle Scholar
  20. 20.
    Valentın L, Lu-Chau TA, Lopez C, Feijoo G, Moreira MT, Lema JM (2007) Biodegradation of dibenzothiophene, fluoranthene, pyrene and chrysene in a soil slurry reactor by the white-rot fungus Bjerkandera sp. BOS55. Process Biochem 42:641–648CrossRefGoogle Scholar
  21. 21.
    Cabana H, Jones JP, Agathos SN (2007) Preparation and characterization of cross-linked laccase aggregates and their application to the elimination of endocrine disrupting chemicals. J Biotechnol 132:23–31CrossRefGoogle Scholar
  22. 22.
    Soares A, Jonasson K, Terrazas E, Guieysse B, Mattiasson B (2005) The ability of white-rot fungi to degrade the endocrine-disrupting compound nonylphenol. Appl Microbiol Biotechnol 66:719–725CrossRefGoogle Scholar
  23. 23.
    Tanaka T, Yamada K, Tonosaki T, Konishi T, Goto H, Taniguchi M (2000) Enzymatic degradation of alkylphenols, bisphenol A, synthetic estrogen and phthalic ester. Water Sci Technol 42:89–95Google Scholar
  24. 24.
    Auriol M, Filali-Meknassi Y, Adams CD, Tyagi RD, Noguerol TN, Piña B (2008) Removal of estrogenic activity of natural and synthetic hormones from a municipal wastewater: efficiency of horseradish peroxidase and laccase from Trametes versicolor. Chemosphere 70:445–452CrossRefGoogle Scholar
  25. 25.
    Auriol M, Filali-Meknassi Y, Tyagi RD, Adams CD (2007) Laccase-catalyzed conversion of natural and synthetic hormones from a municipal wastewater. Water Res 41:3281–3288CrossRefGoogle Scholar
  26. 26.
    Blánquez P, Guieysse B (2008) Continuous biodegradation of 17b-estradiol and17a-ethynylestradiol by Trametes versicolor. J Hazard Mater 150:459–462CrossRefGoogle Scholar
  27. 27.
    Tanaka T, Tonosaki T, Nose M, Tomidokoro N, Kadomura N, Fujii T, Taniguchi M (2001) Treatment of model soils contaminated with phenolic endocrine-disrupting chemicals with laccase from Trametes sp. in a rotating reactor. J Biosci Bioeng 92:312–316CrossRefGoogle Scholar
  28. 28.
    Eibes G, Debernardi G, Feijoo G, Moreira MT, Lema JM (2011) Oxidation of pharmaceutically active compounds by a ligninolytic fungal peroxidase. Biodegradation 22:539–550CrossRefGoogle Scholar
  29. 29.
    Marco-Urrea E, Pérez-Trujillo M, Blánquez P, Vicent T, Caminal G (2010) Biodegradation of the analgesic naproxen by Trametes versicolor and identification of intermediates using HPLC-DAD-MS and NMR. Bioresour Technol 101:2159–2166CrossRefGoogle Scholar
  30. 30.
    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 176:836–842CrossRefGoogle Scholar
  31. 31.
    Marco-Urrea E, Pérez-Trujillo M, Cruz-Morató C, Caminal G, Vicent T (2010) White-rot fungus-mediated degradation of the analgesic ketoprofen and identification of intermediates by HPLC-DAD-MS and NMR. Chemosphere 78:474–481CrossRefGoogle Scholar
  32. 32.
    Marco-Urrea E, Pérez-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 74:765–772CrossRefGoogle Scholar
  33. 33.
    Tran NH, Urase Kusakabe O (2010) Biodegradation characteristics of pharmaceutical substances by whole fungal culture Trametes versicolor and its laccase. J Water Environ Technol 8:125–140CrossRefGoogle Scholar
  34. 34.
    Accinelli C, Saccà ML, Batisson I, Fick J, Mencarelli M, Grabic R (2010) Removal of oseltamivir (Tamiflu) and other selected pharmaceuticals from wastewater using a granular bioplastic formulation entrapping propagules of Phanerochaete chrysosporium. Chemosphere 81:436–443CrossRefGoogle Scholar
  35. 35.
    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 Microbiol Biotechnol 27:1839–1846CrossRefGoogle Scholar
  36. 36.
    Schwarz J, Aust MO, Thiele-Bruhn S (2010) Metabolites from fungal laccase-catalysed transformation of sulfonamides. Chemosphere 81:1469–1476CrossRefGoogle Scholar
  37. 37.
    Hata T, Shintate H, Kawai S, Okamura H, Nishida T (2010) Elimination of carbamazepine by repeated treatment with laccase in the presence of 1-hydroxybenzotriazole. J Hazard Mater 181:1175–1178CrossRefGoogle Scholar
  38. 38.
    Jelić A, Cruz-Morató C, Marco-Urrea E, Sarrà M, Pérez S, Vicent T, Petrović M, Barceló D (2012) Degradation of carbamazepine by Trametes versicolor in an air pulsed fluidized bed bioreactor and identification of intermediates. Water Res 46:955–964CrossRefGoogle Scholar
  39. 39.
    Marco-Urrea E, Radjenović J, Caminal G, Petrović M, Vicent T, Barceló D (2010) Oxidation of atenolol, propranolol, carbamazepine and clofibric acid by a biological Fenton-like system mediated by the white-rot fungus Trametes versicolor. Water Res 44:521–532CrossRefGoogle Scholar
  40. 40.
    Nyanhongo GS, Gübitz G, Sukyai P, Leitner C, Haltrich D, Ludwig R (2007) Oxidoreductases from Trametes spp. in biotechnology: a wealth of catalytic activity. Food Technol Biotechnol 45:250–268Google Scholar
  41. 41.
    Pointing SB (2001) Feasibility of bioremediation by white-rot fungi. Appl Microbiol Biotechnol 57:20–33CrossRefGoogle Scholar
  42. 42.
    Lundell TK, Mäkelä MR, Hildén K (2010) Lignin-modifying enzymes in filamentous basidiomycetes: ecological, functional and phylogenetic review. J Basic Microbiol 50:1–16CrossRefGoogle Scholar
  43. 43.
    Guillén F, Gómez-Toribio V, Martínez MJ, Martínez AT (2000) Production of hydroxyl radical by the synergistic action of fungal laccase and aryl alcohol oxidase. Arch Biochem Biophys 383:142–147CrossRefGoogle Scholar
  44. 44.
    Bending GD, Friloux M, Walke A (2002) Degradation of contrasting pesticides by white rot fungi and its relationship with ligninolytic potential. FEMS Microbiol Lett 212:59–63CrossRefGoogle Scholar
  45. 45.
    Cajthaml T, Kresinová Z, Svobodová K, Möder M (2009) Biodegradation of endocrine-disrupting compounds and suppression of estrogenic activity by ligninolytic fungi. Chemosphere 75:745–750CrossRefGoogle Scholar
  46. 46.
    Yang S, Hai FI, Nyghiem DL, Roddick F, Price WE (2013) Removal of trace organic contaminants by nitrifying activated sludge and whole-cell and crude enzyme extract of Trametes versicolor. Water Sci Technol 67:1216–1223CrossRefGoogle Scholar
  47. 47.
    Hatakka A (1994) Lignin-modifying enzymes from selected white-rot fungi – production and role in lignin degradation. FEMS Microbiol Rev 13:125–135CrossRefGoogle Scholar
  48. 48.
    Hofrichter M, Ullrich R, Pecyna MJ, Liers C, Lundell T (2010) New and classic families of secreted fungal heme peroxidases. Appl Microbiol Biotechnol 87:871–897CrossRefGoogle Scholar
  49. 49.
    Cullen D (1997) Recent advances on the molecular genetics of ligninolytic fungi. J Biotechnol 53:273–289CrossRefGoogle Scholar
  50. 50.
    Joshi DK, Gold MH (1993) Degradation of 2,4,5-trichlorophenol by the lignin-degrading basidiomycete Phanerochaete chrysosporium. Appl Environ Microbiol 59:1779–1785Google Scholar
  51. 51.
    Michels J, Gottschalk G (1994) Inhibition of the lignin peroxidase of Phanerochaete chrysosporium by hydroxylaminodinitrotoluene, a nearly intermediate in the degradation of 2,4,6-trinitrotoluene. Appl Environ Microbiol 60:187–194Google Scholar
  52. 52.
    Wesenberg D, Kyriakides I, Agathos SN (2003) White-rot fungi and their enzymes for the treatment of industrial dye effluents. Biotechnol Adv 22:161–187CrossRefGoogle Scholar
  53. 53.
    Wariishi H, Valli K, Gold MH (1992) Manganese (I1) oxidation by manganese peroxidase from the basidiomycete phanerochaete chrysosporium. Kinetic mechanism and role of chelators. J Biol Chem 267:23688–23695Google Scholar
  54. 54.
    Camarero S, Sarkar S, Ruiz-Dueñas FJ, Martínez MJ, Martínez AT (1999) Description of a versatile peroxidase involved in natural degradation of lignin that has both Mn-peroxidase and lignin-peroxidase substrate binding sites. J Biol Chem 274:10324–10330CrossRefGoogle Scholar
  55. 55.
    Mester T, Field JA (1998) Characterization of a novel manganese peroxidase-lignin peroxidase hybrid isozyme produced by Bjerkandera spp. strain BOS55 in the absence of manganese. J Biol Chem 273:15412–15417CrossRefGoogle Scholar
  56. 56.
    Heinfling A, Martinez MJ, Martinez AT, Bergbauer M, Szewzyk U (1998) Purification and characterization of peroxidases from the dye-decolorizing fungus Bjerkandera adusta. FEMS Microbiol Lett 165:43–50CrossRefGoogle Scholar
  57. 57.
    Thurston C (1994) The structure and function of fungal laccases. Microbiology 140:19–26CrossRefGoogle Scholar
  58. 58.
    Otto B, Schlosser D (2014) First laccase in green algae: purification and characterization of an extracellular phenol oxidase from Tetracystis Aeria. Planta 240(6):1225–1236. doi: 10.1007/s00425-014-2144-9 CrossRefGoogle Scholar
  59. 59.
    Sharma KK, Kuhad RC (2008) Laccase: enzyme revisited and function redefined. Indian J Microbiol 48(3):309–316CrossRefGoogle Scholar
  60. 60.
    Reddy CA (1995) The potential for white-rot fungi in the treatment of pollutants. Curr Opin Biotechnol 6:320–328CrossRefGoogle Scholar
  61. 61.
    Fakoussa RM, Hofrichter M (1999) Biotechnology and microbiology of coal degradation. Appl Microbiol Biotechnol 52:25–40CrossRefGoogle Scholar
  62. 62.
    Rodríguez-Couto S, Toca-Herrera JL (2006) Industrial and biotechnological applications of laccases: a review. Biotechnol Adv 24:500–513CrossRefGoogle Scholar
  63. 63.
    Asgher M, Bhati HN, Ashraf M, Legge RL (2008) Recent developments in biodegradation of industrial pollutants by white rot fungi and their enzyme system. Biodegradation 19:771–783CrossRefGoogle Scholar
  64. 64.
    Bourbonnais R, Paice MG (1990) Oxidation of non-phenolic substrates. An expanded role for laccase in lignin biodegradation. FEBS Lett 267:99–102CrossRefGoogle Scholar
  65. 65.
    Call HP, Mücke I (1997) History, overview and applications of mediated lignolytic systems, especially laccase-mediator-systems. J Biotechnol 53:163–202CrossRefGoogle Scholar
  66. 66.
    Cañas AI, Camarero S (2010) Laccases and their natural mediators: biotechnological tools for sustainable eco-friendly processes. Biotechnol Adv 28(6):694–705CrossRefGoogle Scholar
  67. 67.
    Bezalel L, Hadar Y, Cerniglia CE (1997) Enzymatic mechanism involved in Phenanthrene degradation by the white-rot fungus Pleurotus ostreatus. Appl Environ Microbiol 63:2495–2501Google Scholar
  68. 68.
    Marco-Urrea E, Gabarrell X, Sarrà M, Caminal G, Vicent T, Adinarayana-Reddy C (2006) Novel aerobic perchloroethylene degradation by the white-rot fungus Trametes versicolor. Environ Sci Technol 40:7796–7802CrossRefGoogle Scholar
  69. 69.
    Marco-Urrea E, Parella T, Gabarrell X, Caminal G, Vicent T, Adinarayana Reddy C (2008) Mechanistics of trichloroethylene mineralization by the white-rot fungus Trametes versicolor. Chemosphere 70:404–410CrossRefGoogle Scholar
  70. 70.
    Bernhardt R (2006) Cytochromes P450 as versatile biocatalysts. J Biotechnol 24:128–145CrossRefGoogle Scholar
  71. 71.
    Cabana H, Jones JP, Agathos SN (2007) Elimination of endocrine disrupting chemicals using white rot fungi and their lignin modifying enzymes: a review. Eng Life Sci 7:429–456CrossRefGoogle Scholar
  72. 72.
    Cerniglia CE (1997) Fungal metabolism of polycyclic aromatic hydrocarbons: past, present and future applications in bioremediation. J Ind Microbiol Biotechnol 19(5–6):324–333CrossRefGoogle Scholar
  73. 73.
    Harms H, Schlosser D, Wick LY (2011) Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat Rev Microbiol 9(3):177–192CrossRefGoogle Scholar
  74. 74.
    Pinedo-Rivilla C, Aleu J, Collado I (2009) Pollutants biodegradation by fungi. Curr Org Chem 13(12):1194–1214CrossRefGoogle Scholar
  75. 75.
    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 Biodet Biodegr 88:169–175CrossRefGoogle Scholar
  76. 76.
    Badia-Fabregat M, Rodríguez-Rodríguez CE, Gago-Ferrero P, Olivares A, Piña B, Díaz-Cruz MS, Barceló D, Caminal G, Vicent T (2012) Degradation of several UV filters in a solid-state fermentation of WWTP sludge and 4-MBC in liquid medium by the ligninolytic fungus Trametes versicolor. J Environ Manage 104:114–120CrossRefGoogle Scholar
  77. 77.
    Gago-Ferrero P, Badia-Fabregat M, Olivares A, Blanquez P, Piña B, Caminal G, Vicent T, Díaz-Cruz MS, Barceló D (2012) Evaluation of fungal- and photo-degradation as potential treatments for the removal of sunscreens BP3 and BP1. Sci Total Environ 427–728:355–363CrossRefGoogle Scholar
  78. 78.
    Mizuno H, Hirai H, Kawai S, Nishida T (2009) Removal of estrogenic activity of iso-butylparaben and N-butylparaben by laccase in the presence of 1-hydroxybenzotriazole. Biodegradation 20(4):533–539CrossRefGoogle Scholar
  79. 79.
    Nguyen LN, Hai FI, Yang S, Kang J, Leusch FDL, Roddick F, Price WE, Nghiem LD (2013) Removal of trace organic contaminants by an MBR comprising a mixed culture of bacteria and white-rot fungi. Bioresour Technol 143:234–241CrossRefGoogle Scholar
  80. 80.
    Yang S (2012) Removal of micropollutants by a fungus-augmented membrane bioreactor. Master of Engineering - Research thesis, University of Wollongong. http://ro.uow.edu.au/theses/3690
  81. 81.
    Blánquez P, Caminal G, Sarrà M, Vicent T (2007) The effect of HRT on the decolourisation of the grey lanaset G textile dye by Trametes versicolor. Chem Eng J 126(2–3):163–169CrossRefGoogle Scholar
  82. 82.
    Rodríguez-Rodríguez CE, Barón E, Gago-Ferrero P, Jelić A, Llorca M, Farré M, Díaz-Cruz MS et al (2012) Removal of pharmaceuticals, polybrominated flame retardants and UV-filters from sludge by the fungus Trametes versicolor in bioslurry reactor. J Hazard Mater 233–234:235–243CrossRefGoogle Scholar
  83. 83.
    Rodríguez-Rodríguez CE, Lucas D, Barón E, Gago-Ferrero P, Molins-Delgado D, Rodríguez-Mozaz S, Eljarrat E, Díaz-Cruz MS et al (2014) Re-inoculation strategies enhance the degradation of emerging pollutants in fungal bioaugmentation of sewage sludge. Bioresour Technol 168:180–189CrossRefGoogle Scholar
  84. 84.
    Songulashvili G, Jiménez-Tobón GA, Jaspers C, Penninckx MJ (2012) Immobilized laccase of Cerrena unicolor for elimination of endocrine disruptor micropollutants. Fungal Biol 116:883–889CrossRefGoogle Scholar
  85. 85.
    Cabana H, Alexandre C, Agathos SN, Jones JP (2009) Immobilization of laccase from the white rot fungus Coriolopsis polyzona and use of the immobilized biocatalyst for the continuous elimination of endocrine disrupting chemicals. Bioresour Technol 100:3447–3458CrossRefGoogle Scholar
  86. 86.
    Taboada-Puig R, Junghanns C, Demarche P, Moreira MT, Feijoo G, Lema JM, Agathos SN (2011) Combined cross-linked enzyme aggregates from versatile peroxidase and glucose oxidase: production, partial characterization and application for the elimination of endocrine disruptors. Bioresour Technol 102:6593–6599CrossRefGoogle Scholar
  87. 87.
    Kim YJ, Nicell JA (2006) Laccase catalysed oxidation of aqueous triclosan. J Chem Technol Biotechnol 81:1344–1352CrossRefGoogle Scholar
  88. 88.
    Garcia HA, Hoffman CM, Kinney KA, Lawler DF (2011) Laccase-catalyzed oxidation of oxybenzone in municipal wastewater primary effluent. Water Res 45(5):1921–1932CrossRefGoogle Scholar
  89. 89.
    Tran NH, Hu J, Urase T (2013) Removal of the insect repellent N, N-diethyl-m-toluamide (DEET) by laccase-mediated systems. Bioresour Technol 147:667–671CrossRefGoogle Scholar
  90. 90.
    Cabana H, Jiwan JLH, 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 67:770–778CrossRefGoogle Scholar
  91. 91.
    Eibes G, López C, Moreira MT, Feijoo G, Lema JM (2007) Strategies for the design and operation of enzymatic reactors for the degradation of highly and poorly soluble recalcitrant compounds. Biocatal Biotrans 25:260–268CrossRefGoogle Scholar
  92. 92.
    Bornscheuer UT (2003) Immobilizing enzymes: how to create more suitable biocatalysts? Angew Chem Int Ed 42:3336–3337CrossRefGoogle Scholar
  93. 93.
    Coniglio A, Galli C, Gentili P, Vadalà R (2008) Oxidation of amides by laccase generated aminoxyl radicals. J Mol Catal B: Enzym 50:40–49CrossRefGoogle Scholar
  94. 94.
    Yang S, Hai FI, Nghiem LD, Price WE, Roddick F, Moreira MT, Magram SF (2013) Understanding the factors controlling the removal of trace organic contaminants by white-rot fungi and their lignin-modifying enzymes: a critical review. Bioresour Technol 141:97–108CrossRefGoogle Scholar
  95. 95.
    d’Acunzo F, Galli C, Gentili P, Sergi F (2006) Mechanistic and steric issues in the oxidation of phenolic and non-phenolic compounds by laccase or laccase mediator systems. The case of bifunctional substrates. New J Chem 30:583–591CrossRefGoogle Scholar
  96. 96.
    Baldrian P (2003) Interactions of heavy metals with white-rot fungi. Enzyme Microb Technol 32:78–91CrossRefGoogle Scholar
  97. 97.
    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 66:4157–4160CrossRefGoogle Scholar
  98. 98.
    Rüdel H, Böhmer W, Müller M, Fliedner A, Ricking M, Teubner D, Schröter-Kermani C (2013) Retrospective study of triclosan and methyl-triclosan residues in fish and suspended particulate matter: results from the German Environmental Specimen Bank. Chemosphere 91:1517–1524CrossRefGoogle Scholar
  99. 99.
    Buser HR, Müller MD, Balmer ME, Poiger T, Buerge IJ (2005) Stereoisomer composition of the chiral UV filter 4-methylbenzylidene camphor in environmental samples. Environ Sci Technol 39:3013–3019CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • M. Silvia Díaz-Cruz
    • 1
    Email author
  • Pablo Gago-Ferrero
    • 1
    • 2
  • Marina Badia-Fabregat
    • 3
  • Gloria Caminal
    • 4
  • Teresa Vicent
    • 3
  • Damià Barceló
    • 1
    • 5
  1. 1.Department of Environmental ChemistryInstitute of Environmental Assessment and Water Research (IDAEA), Spanish Council for Scientific Research (CSIC)BarcelonaSpain
  2. 2.Laboratory of Analytical Chemistry, Department of ChemistryNational and Kapodistrian University of AthensAthensGreece
  3. 3.Departament d’Enginyeria Química, Escola d’EnginyeriaUniversitat Autònoma de BarcelonaBarcelonaSpain
  4. 4.Institut de Química Avançada de Catalunya (IQAC-CSIC)BarcelonaSpain
  5. 5.Catalan Institute for Water Research (ICRA), H2O BuildingScientific and Technological Park of the University of GironaGironaSpain

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