Skip to main content
Log in

Degradation of Pharmaceuticals and Personal Care Products by White-Rot Fungi—a Critical Review

  • Water Pollution (S Sengupta, Section Editor)
  • Published:
Current Pollution Reports Aims and scope Submit manuscript

Abstract

White-rot fungi (WRF) mediated treatment can offer an environmentally friendly platform for the removal of pharmaceuticals and personal care products (PPCPs) from wastewater. These PPCPs may have adverse impacts on aquatic organisms and even human and thus their removal during wastewater treatment is of significant interest to the water industry. Whole-cell WRF or their extracellular lignin modifying enzymes (LMEs) have been reported to efficiently degrade PPCPs that are persistent to conventional activated sludge process. WRF mediated treatment of PPCPs depends on a number of factors including physicochemical properties of PPCPs (e.g., hydrophobicity and chemical structure) and wastewater matrix (e.g., pH, temperature, and dissolved constituents), type of WRF species and their specific extracellular enzymes. This review critically analyzes the performance of whole-cell WRF and their LMEs for the removal of PPCPs; particularly, it offers insights into PPCP removal mechanisms (e.g., biosorption vs. biodegradation) and degradation pathways as well as the formation of intermediate byproducts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Combi T, Pintado-Herrera MG, Lara-Martin PA, Miserocchi S, Langone L, Guerra R. Distribution and fate of legacy and emerging contaminants along the Adriatic Sea: a comparative study. Environ Pollut. 2016;218:1055–64.

    Article  CAS  Google Scholar 

  2. Luo Y, Guo W, Ngo HH, Nghiem LD, Hai FI, Zhang J, et al. A review on the occurrence of micropollutants in the aquatic environment and their fate and removal during wastewater treatment. Sci Total Environ. 2014;473:619–41.

    Article  CAS  Google Scholar 

  3. Sui Q, Cao X, Lu S, Zhao W, Qiu Z, Yu G. Occurrence, sources and fate of pharmaceuticals and personal care products in the groundwater: a review. Emerging Contaminants. 2015;1(1):14–24.

    Article  Google Scholar 

  4. Gavrilescu M, Demnerová K, Aamand J, Agathos S, Fava F. Emerging pollutants in the environment: present and future challenges in biomonitoring, ecological risks and bioremediation. New Biotechnol. 2015;32(1):147–56.

    Article  CAS  Google Scholar 

  5. Pal A, He Y, Jekel M, Reinhard M, Gin KY-H. Emerging contaminants of public health significance as water quality indicator compounds in the urban water cycle. Environ Int. 2014;71:46–62.

    Article  CAS  Google Scholar 

  6. Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs Jr DR, Lee D-H, et al. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev. 2012;33(3):378–455.

    Article  CAS  Google Scholar 

  7. Chen Z-F, Ying G-G. Occurrence, fate and ecological risk of five typical azole fungicides as therapeutic and personal care products in the environment: a review. Environ Int. 2015;84:142–53.

    Article  CAS  Google Scholar 

  8. Ortiz de García S, Pinto GP, García-Encina PA, Mata RI. Ranking of concern, based on environmental indexes, for pharmaceutical and personal care products: an application to the Spanish case. J Environ Manag. 2013;129:384–97.

    Article  Google Scholar 

  9. Camargo MC, García A, Riquelme A, Otero W, Camargo CA, Hernandez-García T, et al. The problem of Helicobacter pylori resistance to antibiotics: a systematic review in Latin America. Am J Gastroenterol. 2014;109(4):485–95.

    Article  CAS  Google Scholar 

  10. Rizzo L, Manaia C, Merlin C, Schwartz T, Dagot C, Ploy M, et al. Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci Total Environ. 2013;447:345–60.

    Article  CAS  Google Scholar 

  11. Nazaret S, Aminov R. Role and prevalence of antibiosis and the related resistance genes in the environment. Front Microbiol. 2014;5. doi:10.3389/fmicb.2014.00520.

  12. Zhang Y, Arends JB, Van de Wiele T, Boon N. Bioreactor technology in marine microbiology: from design to future application. Biotechnol Adv. 2011;29(3):312–21.

    Article  CAS  Google Scholar 

  13. Benner J, Helbling DE, Kohler H-PE, Wittebol J, Kaiser E, Prasse C, et al. Is biological treatment a viable alternative for micropollutant removal in drinking water treatment processes? Water Res. 2013;47(16):5955–76.

    Article  CAS  Google Scholar 

  14. Hai FI, Yamamoto K, Fukushi K. Hybrid treatment systems for dye wastewater. Crit Rev Environ Sci Technol. 2007;37(4):315–77.

    Article  CAS  Google Scholar 

  15. Hai FI, Alturki A, Nguyen LN, Price WE, Nghiem LD. Removal of trace organic contaminants by integrated membrane processes for water reuse applications. In: Ngo HH, Guo W, Surampalli RY, Zhang TC, editors. Green Technologies for Sustainable Water Management. Reston: American Society of Civil Engineers; 2016. p. 533–78 .ISBN: 9780784414422

    Chapter  Google Scholar 

  16. Hai FI, Nghiem LD, Khan SJ, Price WE, Yamamoto K. Wastewater reuse: removal of emerging trace organic contaminants (TrOC). In: Hai FI, Yamamoto K, Lee C, editors. Membrane biological reactors: theory, modeling, design, management and applications to wastewater reuse. London: IWA Publishing; 2014. p. 165–205 .ISBN: 9781780400655

    Google Scholar 

  17. Hai FI, Nguyen LN, Nghiem LD, Liao B-Q, Koyuncu I, Price WE. Trace organic contaminants removal by combined processes for wastewater reuse. In: Fatta-Kassinos D, Dionysiou DD, Kümmerer K, editors. Advanced treatment Technologies for Urban Wastewater Reuse. 45. New York: Springer; 2014. p. 39–77 .ISBN: 9783319238869

    Chapter  Google Scholar 

  18. Hai FI, Yamamoto K, Nakajima F, Fukushi K. Factors governing performance of continuous fungal reactor during non-sterile operation—the case of a membrane bioreactor treating textile wastewater. Chemosphere. 2009;74(6):810–7.

    Article  CAS  Google Scholar 

  19. Hai FI, Yamamoto K, Nakajima F, Fukushi K. Removal of structurally different dyes in submerged membrane fungi reactor—biosorption/PAC-adsorption, membrane retention and biodegradation. J Membr Sci. 2008;325(1):395–403.

    Article  CAS  Google Scholar 

  20. Chen M, Xu P, Zeng G, Yang C, Huang D, Zhang J. Bioremediation of soils contaminated with polycyclic aromatic hydrocarbons, petroleum, pesticides, chlorophenols and heavy metals by composting: applications, microbes and future research needs. Biotechnol Adv. 2015;33(6):745–55.

    Article  CAS  Google Scholar 

  21. Anasonye F, Winquist E, Kluczek-Turpeinen B, Räsänen M, Salonen K, Steffen KT, et al. Fungal enzyme production and biodegradation of polychlorinated dibenzo-p-dioxins and dibenzofurans in contaminated sawmill soil. Chemosphere. 2014;110:85–90.

    Article  CAS  Google Scholar 

  22. Hai FI, Yamamoto K. Suitability of membrane bioreactor for treatment of recalcitrant textile dye wastewater utilising white-rot fungi. International Journal of Environmental Engineering. 2009;2(1–3):43–55.

    Google Scholar 

  23. Hai FI, Yamamoto K, Fukushi K. Development of a submerged membrane fungi reactor for textile wastewater treatment. Desalination. 2006;192(1):315–22.

    Article  CAS  Google Scholar 

  24. Cruz-Morató C, Ferrando-Climent L, Rodriguez-Mozaz S, Barceló D, Marco-Urrea E, Vicent T, et al. Degradation of pharmaceuticals in non-sterile urban wastewater by Trametes versicolor in a fluidized bed bioreactor. Water Res. 2013;47(14):5200–10.

    Article  CAS  Google Scholar 

  25. Rodríguez-Rodríguez CE, García-Galán MJ, Blánquez P, Díaz-Cruz MS, Barceló D, Caminal G, et al. Continuous degradation of a mixture of sulfonamides by Trametes versicolor and identification of metabolites from sulfapyridine and sulfathiazole. J Hazard Mater. 2012;213:347–54.

    Article  CAS  Google Scholar 

  26. Yang S, Hai FI, Nghiem LD, Nguyen LN, Roddick F, Price WE. Removal of bisphenol A and diclofenac by a novel fungal membrane bioreactor operated under non-sterile conditions. Int Biodeterior Biodegrad. 2013;85:483–90.

    Article  CAS  Google Scholar 

  27. Nguyen LN, Hai FI, Yang S, Kang J, Leusch FD, Roddick F, et al. Removal of trace organic contaminants by an MBR comprising a mixed culture of bacteria and white-rot fungi. Bioresour Technol. 2013;148:234–41.

    Article  CAS  Google Scholar 

  28. Rodriguez Porcel E, Casas López J, Sanchez Perez J, Chisti Y. Enhanced production of lovastatin in a bubble column by Aspergillus terreus using a two-stage feeding strategy. J Chem Technol Biotechnol. 2007;82(1):58–64.

    Article  CAS  Google Scholar 

  29. Modin O, Hai FI, Nghiem LD, Basile A, Fukushi K. Gas-diffusion, extractive, biocatalytic and electrochemical membrane biological reactors. In: Hai FI, Yamamoto K, Lee C, editors. Membrane biological reactors: theory, modeling, design, management and applications to wastewater reuse. London: IWA Publishing; 2014. p. 299–333 .ISBN: 9781780400655

    Google Scholar 

  30. Hai FI, Nghiem LD, Modin O. Biocatalytic membrane reactors for the removal of recalcitrant and emerging pollutants from wastewater. In: Basile A, editor. Handbook of membrane reactors: reactor types and industrial applications. 2. Sawston: Woodhead Publishing Limited; 2013. p. 763–807 .ISBN: 9780857094155

    Chapter  Google Scholar 

  31. Yang S, Hai FI, Nghiem LD, Price WE, Roddick F, Moreira MT, et al. Understanding the factors controlling the removal of trace organic contaminants by white-rot fungi and their lignin modifying enzymes: a critical review. Bioresour Technol. 2013;141:97–108.

    Article  CAS  Google Scholar 

  32. Gao D, Du L, Yang J, Wu W-M, Liang H. A critical review of the application of white rot fungus to environmental pollution control. Crit Rev Biotechnol. 2010;30(1):70–7.

    Article  CAS  Google Scholar 

  33. Tortella G, Durán N, Rubilar O, Parada M, Diez M. Are white-rot fungi a real biotechnological option for the improvement of environmental health? Crit Rev Biotechnol. 2015;35(2):165–72.

    Article  CAS  Google Scholar 

  34. Kües U. Fungal enzymes for environmental management. Curr Opin Biotechnol. 2015;33:268–78.

    Article  CAS  Google Scholar 

  35. Rodgers CJ, Blanford CF, Giddens SR, Skamnioti P, Armstrong FA, Gurr SJ. Designer laccases: a vogue for high-potential fungal enzymes? Trends Biotechnol. 2010;28(2):63–72.

    Article  CAS  Google Scholar 

  36. Rouches E, Herpoël-Gimbert I, Steyer J, Carrere H. Improvement of anaerobic degradation by white-rot fungi pretreatment of lignocellulosic biomass: a review. Renew Sust Energ Rev. 2016;59:179–98.

    Article  CAS  Google Scholar 

  37. Pointing S. Feasibility of bioremediation by white-rot fungi. Appl Microbiol Biotechnol. 2001;57(1–2):20–33.

    CAS  Google Scholar 

  38. Lundell TK, Mäkelä MR, Hildén K. Lignin-modifying enzymes in filamentous basidiomycetes—ecological, functional and phylogenetic review. J Basic Microbiol. 2010;50(1):5–20.

    Article  CAS  Google Scholar 

  39. Guillén F, Gómez-Toribio V, Martı́nez MJ, Martı́nez AT. Production of hydroxyl radical by the synergistic action of fungal laccase and aryl alcohol oxidase. Arch Biochem Biophys. 2000;383(1):142–7.

    Article  CAS  Google Scholar 

  40. Bending GD, Friloux M, Walker A. Degradation of contrasting pesticides by white rot fungi and its relationship with ligninolytic potential. FEMS Microbiol Lett. 2002;212(1):59–63.

    Article  CAS  Google Scholar 

  41. Yang S, Hai FI, Nghiem LD, Roddick F, Price WE. Removal of trace organic contaminants by nitrifying activated sludge and whole-cell and crude enzyme extract of Trametes versicolor. Water Sci Technol. 2013;67(6):1216–23.

    Article  CAS  Google Scholar 

  42. Nguyen LN, Hai FI, Yang S, Kang J, Leusch FDL, Roddick F, Price WE, Nghiem LD. Removal of pharmaceuticals, steroid hormones, phytoestrogens, UV-filters, industrial chemicals and pesticides by Trametes versicolor: role of biosorption and biodegradation. Int Biodeterior Biodegrad. 2014;88:169–75.

    Article  CAS  Google Scholar 

  43. Marco-Urrea E, Pérez-Trujillo M, Blánquez P, Vicent T, Caminal G. Biodegradation of the analgesic naproxen by Trametes versicolor and identification of intermediates using HPLC-DAD-MS and NMR. Bioresour Technol. 2010;101(7):2159–66.

    Article  CAS  Google Scholar 

  44. Hatakka A. Lignin-modifying enzymes from selected white-rot fungi: production and role from in lignin degradation. FEMS Microbiol Rev. 1994;13(2–3):125–35.

    Article  CAS  Google Scholar 

  45. Golan-Rozen N, Chefetz B, Ben-Ari J, Geva J, Hadar Y. Transformation of the recalcitrant pharmaceutical compound carbamazepine by Pleurotus ostreatus: role of cytochrome P450 monooxygenase and manganese peroxidase. Environ Sci Technol. 2011;45(16):6800–5.

    Article  CAS  Google Scholar 

  46. Marco-Urrea E, Gabarrell X, Sarrà M, Caminal G, Vicent T, Reddy CA. Novel aerobic perchloroethylene degradation by the white-rot fungus Trametes versicolor. Environ Sci Technol. 2006;40(24):7796–802.

    Article  CAS  Google Scholar 

  47. Marco-Urrea E, Parella T, Gabarrell X, Caminal G, Vicent T, Reddy CA. Mechanistics of trichloroethylene mineralization by the white-rot fungus Trametes versicolor. Chemosphere. 2008;70(3):404–10.

    Article  CAS  Google Scholar 

  48. Bernhardt R. Cytochromes P450 as versatile biocatalysts. J Biotechnol. 2006;124(1):128–45.

    Article  CAS  Google Scholar 

  49. Rodarte-Morales A, Feijoo G, Moreira M, Lema J. Biotransformation of three pharmaceutical active compounds by the fungus Phanerochaete chrysosporium in a fed batch stirred reactor under air and oxygen supply. Biodegradation. 2012;23(1):145–56.

    Article  CAS  Google Scholar 

  50. Rodarte-Morales A, Feijoo G, Moreira M, Lema J. Operation of stirred tank reactors (STRs) and fixed-bed reactors (FBRs) with free and immobilized Phanerochaete chrysosporium for the continuous removal of pharmaceutical compounds. Biochem Eng J. 2012;66:38–45.

    Article  CAS  Google Scholar 

  51. Blánquez P, Guieysse B. Continuous biodegradation of 17β-estradiol and 17α-ethynylestradiol by Trametes versicolor. J Hazard Mater. 2008;150(2):459–62.

    Article  CAS  Google Scholar 

  52. Jelic A, Cruz-Morató C, Marco-Urrea E, Sarrà M, Perez S, Vicent T, et al. Degradation of carbamazepine by Trametes versicolor in an air pulsed fluidized bed bioreactor and identification of intermediates. Water Res. 2012;46(4):955–64.

    Article  CAS  Google Scholar 

  53. Cruz-Morató C, Lucas D, Llorca M, Rodriguez-Mozaz S, Gorga M, Petrovic M, et al. Hospital wastewater treatment by fungal bioreactor: removal efficiency for pharmaceuticals and endocrine disruptor compounds. Sci Total Environ. 2014;493:365–76.

    Article  CAS  Google Scholar 

  54. Cajthaml T, Křesinová Z, Svobodová K, Möder M. Biodegradation of endocrine-disrupting compounds and suppression of estrogenic activity by ligninolytic fungi. Chemosphere. 2009;75(6):745–50.

    Article  CAS  Google Scholar 

  55. Paice MG, Jurasek L, Bourbonnais R, Archibald F. CORIOLUS (TRAMETES) VERSICOLOR. In: Kirk TK, Chang H, editors. Biotechnology in pulp and paper manufacture: applications and fundamental investigations. USA: Reed Publishing; 2013. p. 123–30 .ISBN: 9780409901924

    Google Scholar 

  56. Durán N, Cuevas R, Cordi L, Rubilar O, Diez MC. Biogenic silver nanoparticles associated with silver chloride nanoparticles (Ag@ AgCl) produced by laccase from Trametes versicolor. SpringerPlus. 2014;3(1):1.

    Article  CAS  Google Scholar 

  57. Bergman Å, Heindel JJ, Jobling S, Kidd KA, Zoeller RT, Jobling SK. State of the science of endocrine disrupting chemicals 2012: an assessment of the state of the science of endocrine disruptors prepared by a group of experts for the United Nations Environment Programme and World Health Organization. Geneva: World Health Organization; 2013.

    Google Scholar 

  58. Rebuli ME, Patisaul HB. Assessment of sex specific endocrine disrupting effects in the prenatal and pre-pubertal rodent brain. J Steroid Biochem Mol Biol. 2016;160:148–59.

    Article  CAS  Google Scholar 

  59. Moreira M, Feijoo G, Lema J. Fungal bioreactors: applications to white-rot fungi. Rev Environ Sci Biotechnol. 2003;2(2–4):247–59.

    Article  CAS  Google Scholar 

  60. Andleeb S, Atiq N, Robson GD, Ahmed S. An investigation of anthraquinone dye biodegradation by immobilized Aspergillus flavus in fluidized bed bioreactor. Environ Sci Pollut Res. 2012;19(5):1728–37.

    Article  CAS  Google Scholar 

  61. Kunii D, Levenspiel O. Bubbling bed model for kinetic processes in fluidized beds. Gas-solid mass and heat transfer and catalytic reactions. Industrial & Engineering Chemistry Process Design and Development. 1968;7(4):481–92.

    Article  CAS  Google Scholar 

  62. Ozgun H, Dereli RK, Ersahin ME, Kinaci C, Spanjers H, van Lier JB. A review of anaerobic membrane bioreactors for municipal wastewater treatment: integration options, limitations and expectations. Sep Purif Technol. 2013;118:89–104.

    Article  CAS  Google Scholar 

  63. Mutamim NSA, Noor ZZ, Hassan MAA, Yuniarto A, Olsson G. Membrane bioreactor: applications and limitations in treating high strength industrial wastewater. Chem Eng J. 2013;225:109–19.

    Article  CAS  Google Scholar 

  64. Hai FI, Yamamoto K, Lee C-H. Membrane biological reactors: theory, modeling, design, management and applications to wastewater reuse. London: IWA Publishing; 2013 .ISBN:9781780400655

    Google Scholar 

  65. Hai FI, Yamamoto K, Fukushi K, Nakajima F. Fouling resistant compact hollow-fiber module with spacer for submerged membrane bioreactor treating high strength industrial wastewater. J Membr Sci. 2008;317(1):34–42.

    Article  CAS  Google Scholar 

  66. Babič J, Pavko A. Enhanced enzyme production with the pelleted form of D. squalens in laboratory bioreactors using added natural lignin inducer. J Ind Microbiol Biotechnol. 2012;39(3):449–57.

    Article  CAS  Google Scholar 

  67. Cao J, Zhang H-J, Xu C-P. Culture characterization of exopolysaccharides with antioxidant activity produced by Pycnoporus sanguineus in stirred-tank and airlift reactors. Journal of the Taiwan Institute of Chemical Engineers. 2014;45(5):2075–80.

    Article  CAS  Google Scholar 

  68. Ünyayar A, Demirbilek M, Turkoglu M, Celik A, Mazmanci MA, Erkurt EA, et al. Evaluation of cytotoxic and mutagenic effects of Coriolus versicolor and Funalia trogii extracts on mammalian cells. Drug Chem Toxicol. 2006;29(1):69–83.

    Article  CAS  Google Scholar 

  69. Tepwong P, Giri A, Ohshima T. Effect of mycelial morphology on ergothioneine production during liquid fermentation of Lentinula edodes. Mycoscience. 2012;53(2):102–12.

    Article  CAS  Google Scholar 

  70. Espinosa-Ortiz EJ, Rene ER, Pakshirajan K, van Hullebusch ED, Lens PN. Fungal pelleted reactors in wastewater treatment: applications and perspectives. Chem Eng J. 2016;283:553–71.

    Article  CAS  Google Scholar 

  71. Rodríguez-Rodríguez CE, Jelić A, Llorca M, Farré M, Caminal G, Petrović M, et al. Solid-phase treatment with the fungus Trametes versicolor substantially reduces pharmaceutical concentrations and toxicity from sewage sludge. Bioresour Technol. 2011;102(10):5602–8.

    Article  CAS  Google Scholar 

  72. Hai FI, Yamamoto K, Nakajima F, Fukushi K, Nghiem LD, Price WE, et al. Degradation of azo dye acid orange 7 in a membrane bioreactor by pellets and attached growth of Coriolus versicolour. Bioresour Technol. 2013;141:29–34.

    Article  CAS  Google Scholar 

  73. Hai FI, Yamamoto K, Nakajima F, Fukushi K. Application of a GAC-coated hollow fiber module to couple enzymatic degradation of dye on membrane to whole cell biodegradation within a membrane bioreactor. J Membr Sci. 2012;389:67–75.

    Article  CAS  Google Scholar 

  74. Libra JA, Borchert M, Banit S. Competition strategies for the decolorization of a textile-reactive dye with the white-rot fungi Trametes versicolor under non-sterile conditions. Biotechnol Bioeng. 2003;82(6):736–44.

    Article  CAS  Google Scholar 

  75. Van Leeuwen J, Hu Z, Yi T, Pometto III A, Jin B. Kinetic model for selective cultivation of microfungi in a microscreen process for food processing wastewater treatment and biomass production. Acta Biotechnol. 2003;23(2–3):289–300.

    Article  Google Scholar 

  76. Cheng Z, Xiang-Hua W, Ping N. Continuous Acid Blue 45 decolorization by using a novel open fungal reactor system with ozone as the bactericide. Biochem Eng J. 2013;79:246–52.

    Article  CAS  Google Scholar 

  77. Sankaran S, Khanal SK, Pometto AL, van Leeuwen JH. Ozone as a selective disinfectant for nonaseptic fungal cultivation on corn-processing wastewater. Bioresour Technol. 2008;99(17):8265–72.

    Article  CAS  Google Scholar 

  78. Blánquez P, Sarrà M, Vicent MT. Study of the cellular retention time and the partial biomass renovation in a fungal decolourisation continuous process. Water Res. 2006;40(8):1650–6.

    Article  CAS  Google Scholar 

  79. Mir-Tutusaus JA, Sarrà M, Caminal G. Continuous treatment of non-sterile hospital wastewater by Trametes versicolor: how to increase fungal viability by means of operational strategies and pretreatments. J Hazard Mater. 2016;318:561–70.

    Article  CAS  Google Scholar 

  80. Tran NH, Urase T, Kusakabe O. Biodegradation characteristics of pharmaceutical substances by whole fungal culture Trametes versicolor and its laccase. Journal of Water and Environment Technology. 2010;8(2):125–40.

    Article  Google Scholar 

  81. Nguyen LN, Hai FI, Kang J, Leusch FD, Roddick F, Magram SF, et al. Enhancement of trace organic contaminant degradation by crude enzyme extract from Trametes versicolor culture: effect of mediator type and concentration. Journal of the Taiwan Institute of Chemical Engineers. 2014;45(4):1855–62.

    Article  CAS  Google Scholar 

  82. Nguyen LN, Hai FI, Price WE, Kang J, Leusch FD, Roddick F, et al. Degradation of a broad spectrum of trace organic contaminants by an enzymatic membrane reactor: complementary role of membrane retention and enzymatic degradation. Int Biodeterior Biodegrad. 2015;99:115–22.

    Article  CAS  Google Scholar 

  83. Nguyen LN, Hai FI, Price WE, Leusch FD, Roddick F, McAdam EJ, et al. Continuous biotransformation of bisphenol A and diclofenac by laccase in an enzymatic membrane reactor. Int Biodeterior Biodegrad. 2014;95:25–32.

    Article  CAS  Google Scholar 

  84. Nguyen LN, Hai FI, Price WE, Leusch FD, Roddick F, Ngo HH, et al. The effects of mediator and granular activated carbon addition on degradation of trace organic contaminants by an enzymatic membrane reactor. Bioresour Technol. 2014;167:169–77.

    Article  CAS  Google Scholar 

  85. Nguyen LN, van de Merwe JP, Hai FI, Leusch FD, Kang J, Price WE, et al. Laccase–syringaldehyde-mediated degradation of trace organic contaminants in an enzymatic membrane reactor: removal efficiency and effluent toxicity. Bioresour Technol. 2016;200:477–84.

    Article  CAS  Google Scholar 

  86. Spina F, Varese GC. Fungal bioremediation of emerging micropollutants in municipal wastewaters. In: Purchase D, editor. Fungal applications in sustainable environmental biotechnology. Berlin: Springer; 2016. p. 115–41 .ISBN: 9783319428529

    Chapter  Google Scholar 

  87. Wen X, Jia Y, Li J. Enzymatic degradation of tetracycline and oxytetracycline by crude manganese peroxidase prepared from Phanerochaete chrysosporium. J Hazard Mater. 2010;177(1):924–8.

    Article  CAS  Google Scholar 

  88. Zhang Y, Geißen S-U. In vitro degradation of carbamazepine and diclofenac by crude lignin peroxidase. J Hazard Mater. 2010;176(1):1089–92.

    Article  CAS  Google Scholar 

  89. Ashe B, Nguyen LN, Hai FI, Lee D-J, van de Merwe JP, Leusch FD, et al. Impacts of redox-mediator type on trace organic contaminants degradation by laccase: degradation efficiency, laccase stability and effluent toxicity. Int Biodeterior Biodegrad. 2016; 113:169–76.

  90. Tran NH, Hu J, Urase T. Removal of the insect repellent N, N-diethyl-m-toluamide (DEET) by laccase-mediated systems. Bioresour Technol. 2013;147:667–71.

    Article  CAS  Google Scholar 

  91. Kim Y-J, Nicell JA. Impact of reaction conditions on the laccase-catalyzed conversion of bisphenol A. Bioresour Technol. 2006;97(12):1431–42.

    Article  CAS  Google Scholar 

  92. Kim YJ, Nicell JA. Laccase-catalysed oxidation of aqueous triclosan. J Chem Technol Biotechnol. 2006;81(8):1344–52.

    Article  CAS  Google Scholar 

  93. Saito T, Kato K, Yokogawa Y, Nishida M, Yamashita N. Detoxification of bisphenol A and nonylphenol by purified extracellular laccase from a fungus isolated from soil. J Biosci Bioeng. 2004;98(1):64–6.

    Article  CAS  Google Scholar 

  94. Tamagawa Y, Hirai H, Kawai S, Nishida T. Removal of estrogenic activity of endocrine-disrupting genistein by ligninolytic enzymes from white rot fungi. FEMS Microbiol Lett. 2005;244(1):93–8.

    Article  CAS  Google Scholar 

  95. Suzuki K, Hirai H, Murata H, Nishida T. Removal of estrogenic activities of 17β-estradiol and ethinylestradiol by ligninolytic enzymes from white rot fungi. Water Res. 2003;37(8):1972–5.

    Article  CAS  Google Scholar 

  96. Lloret L, Hollmann F, Eibes G, Feijoo G, Moreira M, Lema J. Immobilisation of laccase on Eupergit supports and its application for the removal of endocrine disrupting chemicals in a packed-bed reactor. Biodegradation. 2012;23(3):373–86.

    Article  CAS  Google Scholar 

  97. Auriol M, Filali-Meknassi Y, Tyagi RD, Adams CD. Laccase-catalyzed conversion of natural and synthetic hormones from a municipal wastewater. Water Res. 2007;41(15):3281–8.

    Article  CAS  Google Scholar 

  98. Auriol M, Filali-Meknassi Y, Adams CD, Tyagi RD, Noguerol T-N, Pina B. Removal of estrogenic activity of natural and synthetic hormones from a municipal wastewater: efficiency of horseradish peroxidase and laccase from Trametes versicolor. Chemosphere. 2008;70(3):445–52.

    Article  CAS  Google Scholar 

  99. Wang J, Majima N, Hirai H, Kawagishi H. Effective removal of endocrine-disrupting compounds by lignin peroxidase from the white-rot fungus Phanerochaete sordida YK-624. Curr Microbiol. 2012;64(3):300–3.

    Article  CAS  Google Scholar 

  100. Hirai H, Nakanishi S, Nishida T. Oxidative dechlorination of methoxychlor by ligninolytic enzymes from white-rot fungi. Chemosphere. 2004;55(4):641–5.

    Article  CAS  Google Scholar 

  101. Hirano T, Honda Y, Watanabe T, Kuwahara M. Degradation of bisphenol A by the lignin-degrading enzyme, manganese peroxidase, produced by the white-rot basidiomycete, Pleurotus ostreatus. Biosci Biotechnol Biochem. 2000;64(9):1958–62.

    Article  CAS  Google Scholar 

  102. Lloret L, Eibes G, Lú-Chau TA, Moreira MT, Feijoo G, Lema JM. Laccase-catalyzed degradation of anti-inflammatories and estrogens. Biochem Eng J. 2010;51(3):124–31.

    Article  CAS  Google Scholar 

  103. Margot J, Copin P-J, von Gunten U, Barry DA, Holliger C. Sulfamethoxazole and isoproturon degradation and detoxification by a laccase-mediator system: influence of treatment conditions and mechanistic aspects. Biochem Eng J. 2015;103:47–59.

    Article  CAS  Google Scholar 

  104. Margot J, Maillard J, Rossi L, Barry DA, Holliger C. Influence of treatment conditions on the oxidation of micropollutants by Trametes versicolor laccase. New Biotechnol. 2013;30(6):803–13.

    Article  CAS  Google Scholar 

  105. Lloret L, Eibes G, Feijoo G, Moreira MT, Lema JM. Application of response surface methodology to study the removal of estrogens in a laccase-mediated continuous membrane reactor. Biocatalysis Biotransformation. 2013;31(4):197–207.

    Article  CAS  Google Scholar 

  106. Becker D, Varela Della Giustina S, Rodriguez-Mozaz S, Schoevaart R, Barceló D, de Cazes M, et al. Removal of antibiotics in wastewater by enzymatic treatment with fungal laccase—degradation of compounds does not always eliminate toxicity. Bioresour Technol. 2016;219:500–9.

    Article  CAS  Google Scholar 

  107. Lloret L, Eibes G, Moreira MT, Feijoo G, Lema JM. Removal of estrogenic compounds from filtered secondary wastewater effluent in a continuous enzymatic membrane reactor. Identification of biotransformation products. Environ Sci Technol. 2013;47(9):4536–43.

    Article  CAS  Google Scholar 

  108. d’Acunzo F, Galli C, Gentili P, Sergi F. 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. 2006;30(4):583–91.

    Article  CAS  Google Scholar 

  109. Astolfi P, Brandi P, Galli C, Gentili P, Gerini MF, Greci L, et al. New mediators for the enzyme laccase: mechanistic features and selectivity in the oxidation of non-phenolic substrates. New J Chem. 2005;29(10):1308–17.

    Article  CAS  Google Scholar 

  110. Murugesan K, Chang Y-Y, Kim Y-M, Jeon J-R, Kim E-J, Chang Y-S. Enhanced transformation of triclosan by laccase in the presence of redox mediators. Water Res. 2010;44(1):298–308.

    Article  CAS  Google Scholar 

  111. Hata T, Shintate H, Kawai S, Okamura H, Nishida T. Elimination of carbamazepine by repeated treatment with laccase in the presence of 1-hydroxybenzotriazole. J Hazard Mater. 2010;181(1):1175–8.

    Article  CAS  Google Scholar 

  112. Purich DL. Enzyme kinetics: catalysis & control: a reference of theory and best-practice methods. Amsterdam: Elsevier; 2010 .ISBN: 9780123809247

    Google Scholar 

  113. Khlifi R, Belbahri L, Woodward S, Ellouz M, Dhouib A, Sayadi S, et al. Decolourization and detoxification of textile industry wastewater by the laccase-mediator system. J Hazard Mater. 2010;175(1):802–8.

    Article  CAS  Google Scholar 

  114. Mukhopadhyay A, Dasgupta AK, Chakrabarti K. Enhanced functionality and stabilization of a cold active laccase using nanotechnology based activation-immobilization. Bioresour Technol. 2015;179:573–84.

    Article  CAS  Google Scholar 

  115. Sampaio LM, Padrão J, Faria J, Silva JP, Silva CJ, Dourado F, et al. Laccase immobilization on bacterial nanocellulose membranes: antimicrobial, kinetic and stability properties. Carbohydr Polym. 2016;145:1–12.

    Article  CAS  Google Scholar 

  116. Zhang J, Liu X, Xu Z, Chen H, Yang Y. Degradation of chlorophenols catalyzed by laccase. Int Biodeterior Biodegrad. 2008;61(4):351–6.

    Article  CAS  Google Scholar 

  117. Ullah MA, Bedford CT, Evans CS. Reactions of pentachlorophenol with laccase from Coriolus versicolor. Appl Microbiol Biotechnol. 2000;53(2):230–4.

    Article  CAS  Google Scholar 

  118. Bosco F, Capolongo A, Ruggeri B. Effect of temperature, pH, ionic strength, and sodium nitrate on activity of LiPs: implications for bioremediation. Bioremediation J. 2002;6(1):65–76.

    Article  CAS  Google Scholar 

  119. Sondhi S, Sharma P, Saini S, Puri N, Gupta N. Purification and characterization of an extracellular, thermo-alkali-stable, metal tolerant laccase from Bacillus tequilensis SN4. PLoS One. 2014;9(5):e96951.

    Article  CAS  Google Scholar 

  120. Hu X, Wang C, Wang L, Zhang R, Chen H. Influence of temperature, pH and metal ions on guaiacol oxidation of purified laccase from Leptographium qinlingensis. World J Microbiol Biotechnol. 2014;30(4):1285–90.

    Article  CAS  Google Scholar 

  121. Bhattacharya S, Das A, Prashanthi K, Palaniswamy M, Angayarkanni J. Mycoremediation of Benzo [a] pyrene by Pleurotus ostreatus in the presence of heavy metals and mediators. 3. Biotech. 2014;4(2):205–11.

    Google Scholar 

  122. Sun K, Luo Q, Gao Y, Huang Q. Laccase-catalyzed reactions of 17β-estradiol in the presence of humic acid: resolved by high-resolution mass spectrometry in combination with 13 C labeling. Chemosphere. 2016;145:394–401.

    Article  CAS  Google Scholar 

  123. Sun J, Bostick BC, Mailloux BJ, Ross JM, Chillrud SN. Effect of oxalic acid treatment on sediment arsenic concentrations and lability under reducing conditions. J Hazard Mater. 2016;311:125–33.

    Article  CAS  Google Scholar 

  124. Schmidt G, Krings U, Nimtz M, Berger RG. A surfactant tolerant laccase of Meripilus giganteus. World J Microbiol Biotechnol. 2012;28(4):1623–32.

    Article  CAS  Google Scholar 

  125. Wan J, Zeng G, Huang D, Huang C, Lai C, Li N, et al. The oxidative stress of Phanerochaete chrysosporium against lead toxicity. Appl Biochem Biotechnol. 2015;175(4):1981–91.

    Article  CAS  Google Scholar 

  126. Zeng G, Li N, Huang D, Lai C, Zhao M, Huang C, et al. The stability of Pb species during the Pb removal process by growing cells of Phanerochaete chrysosporium. Appl Microbiol Biotechnol. 2015;99(8):3685–93.

    Article  CAS  Google Scholar 

  127. Murugesan K, Kim Y-M, Jeon J-R, Chang Y-S. Effect of metal ions on reactive dye decolorization by laccase from Ganoderma lucidum. J Hazard Mater. 2009;168(1):523–9.

    Article  CAS  Google Scholar 

  128. D’Souza-Ticlo D, Sharma D, Raghukumar C. A thermostable metal-tolerant laccase with bioremediation potential from a marine-derived fungus. Mar Biotechnol. 2009;11(6):725–37.

    Article  CAS  Google Scholar 

  129. Zhang J, Kjonaas R, Flurkey WH. Does N-hydroxyglycine inhibit plant and fungal laccases? Phytochemistry. 1999;52(5):775–83.

    Article  CAS  Google Scholar 

  130. Gianfreda L, Sannino F, Filazzola M, Leonowicz A. Catalytic behavior and detoxifying ability of a laccase from the fungal strain Cerrena unicolor. J Mol Catal B Enzym. 1998;4(1):13–23.

    Article  CAS  Google Scholar 

  131. Kreuter T, Steudel A, Pickert H. On the inhibition of laccase by lower fatty acids. Acta Biotechnol. 1991;11(1):81–3.

    Article  CAS  Google Scholar 

  132. Xu F. Dioxygen reactivity of laccase. Appl Biochem Biotechnol. 2001;95(2):125–33.

    Article  CAS  Google Scholar 

  133. Naqui A, Varfolomeev S. Inhibition mechanism of Polyporus laccase by fluoride ion. FEBS Lett. 1980;113(2):157–60.

    Article  CAS  Google Scholar 

  134. Blanford CF, Foster CE, Heath RS, Armstrong FA. Efficient electrocatalytic oxygen reduction by the ‘blue’copper oxidase, laccase, directly attached to chemically modified carbons. Faraday Discuss. 2009;140:319–35.

    Article  Google Scholar 

  135. Bento I, Martins LO, Lopes GG, Carrondo MA, Lindley PF. Dioxygen reduction by multi-copper oxidases: a structural perspective. Dalton Trans. 2005;21:3507–13.

    Article  CAS  Google Scholar 

  136. Xu F. Oxidation of phenols, anilines, and benzenethiols by fungal laccases: correlation between activity and redox potentials as well as halide inhibition. Biochemistry. 1996;35(23):7608–14.

    Article  CAS  Google Scholar 

  137. Hata T, Kawai S, Okamura H, Nishida T. Removal of diclofenac and mefenamic acid by the white rot fungus Phanerochaete sordida YK-624 and identification of their metabolites after fungal transformation. Biodegradation. 2010;21(5):681–9.

    Article  CAS  Google Scholar 

  138. Marco-Urrea E, Pérez-Trujillo M, Cruz-Morató C, Caminal G, Vicent T. Degradation of the drug sodium diclofenac by Trametes versicolor pellets and identification of some intermediates by NMR. J Hazard Mater. 2010;176(1):836–42.

    Article  CAS  Google Scholar 

  139. Marco-Urrea E, Pérez-Trujillo M, Vicent T, Caminal G. Ability of white-rot fungi to remove selected pharmaceuticals and identification of degradation products of ibuprofen by Trametes versicolor. Chemosphere. 2009;74(6):765–72.

    Article  CAS  Google Scholar 

  140. Cabana H, Jones J, Agathos SN. Elimination of endocrine disrupting chemicals using white rot fungi and their lignin modifying enzymes: a review. Eng Life Sci. 2007;7(5):429–56.

    Article  CAS  Google Scholar 

  141. Hundt K, Martin D, Hammer E, Jonas U, Kindermann MK, Schauer F. Transformation of triclosan by Trametes versicolor and Pycnoporus cinnabarinus. Appl Environ Microbiol. 2000;66(9):4157–60.

    Article  CAS  Google Scholar 

  142. Nair RR, Demarche P, Agathos SN. Formulation and characterization of an immobilized laccase biocatalyst and its application to eliminate organic micropollutants in wastewater. New Biotechnol. 2013;30(6):814–23.

    Article  CAS  Google Scholar 

  143. Ansari SA, Husain Q. Potential applications of enzymes immobilized on/in nano materials: a review. Biotechnol Adv. 2012;30(3):512–23.

    Article  CAS  Google Scholar 

  144. Lloret L, Eibes G, Feijoo G, Moreira M, Lema J. Degradation of estrogens by laccase from Myceliophthora thermophila in fed-batch and enzymatic membrane reactors. J Hazard Mater. 2012;213:175–83.

    Article  CAS  Google Scholar 

  145. Hou J, Dong G, Luu B, Sengpiel RG, Ye Y, Wessling M, et al. Hybrid membrane with TiO 2 based bio-catalytic nanoparticle suspension system for the degradation of bisphenol-A. Bioresour Technol. 2014;169:475–83.

    Article  CAS  Google Scholar 

  146. Hou J, Dong G, Ye Y, Chen V. Laccase immobilization on titania nanoparticles and titania-functionalized membranes. J Membr Sci. 2014;452:229–40.

    Article  CAS  Google Scholar 

  147. Nguyen LN, Hai FI, Dosseto A, Richardson C, Price WE, Nghiem LD. Continuous adsorption and biotransformation of micropollutants by granular activated carbon-bound laccase in a packed-bed enzyme reactor. Bioresour Technol. 2016;210:108–16.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work has been partially funded by the GeoQuEST research centre of the University of Wollongong. A PhD scholarship to Muhammad B. Asif from the University of Wollongong is greatly appreciated.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Faisal I. Hai.

Ethics declarations

Conflict of Interest

The authors declare no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

This article is part of the Topical Collection on Water Pollution

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Asif, M.B., Hai, F.I., Singh, L. et al. Degradation of Pharmaceuticals and Personal Care Products by White-Rot Fungi—a Critical Review. Curr Pollution Rep 3, 88–103 (2017). https://doi.org/10.1007/s40726-017-0049-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40726-017-0049-5

Keywords

Navigation