Abstract
The removal of emerging organic contaminants from municipal wastewater poses a major challenge unsatisfactorily addressed by present wastewater treatment processes. Enzyme-catalyzed transformation of emerging organic contaminants (EOC) has been proposed as a possible solution to this major environmental issue more than a decade ago. Especially, laccases gained interest in this context in recent years due to their broad substrate range and since they only need molecular oxygen as a cosubstrate. In order to ensure the stability of the enzymes and allow their retention and reuse, either immobilization or insolubilization of the biocatalysts seems to be the prerequisite for continuous wastewater treatment applications. The present review summarizes the research conducted on EOC transformation with laccases and presents an overview of the possible immobilization techniques. The goal is to assess the state of the art and identify the next necessary steps that have to be undertaken in order to implement laccases as a tertiary wastewater treatment process in sewage treatment plants.
Similar content being viewed by others
References
Ammann EM, Gasser CA, Hommes G, Corvini PFX (2014) Immobilization of defined laccase combinations for enhanced oxidation of phenolic contaminants. Appl Microbiol Biotechnol 98:1397–1406
Andreozzi R, Raffaele M, Paxéus N (2003) Pharmaceuticals in STP effluents and their solar photodegradation in aquatic environment. Chemosphere 50:1319–1330
Ashton D, Hilton M, Thomas KV (2004) Investigating the environmental transport of human pharmaceuticals to streams in the United Kingdom. Sci Total Environ 333:167–184
Auriol M, Filali-Meknassi Y, Tyagi RD, Adams CD, Surampalli RY (2006) Endocrine disrupting compounds removal from wastewater, a new challenge. Process Biochem 41:525–539
Auriol M, Filali-Meknassi Y, Tyagi RD, Adams CD (2007) Laccase-catalyzed conversion of natural and synthetic hormones from a municipal wastewater. Water Res 41:3281–3288
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 70:445–452
Aust SD, Benson JT (1993) The fungus among us—use of white rot fungi to biodegrade environmental pollutants. Environ Health Perspect 101:232–233
Ba S, Arsenault A, Hassani T, Jones JP, Cabana H (2013) Laccase immobilization and insolubilization: from fundamentals to applications for the elimination of emerging contaminants in wastewater treatment. Crit Rev Biotechnol 33:404–418
Baldrian P (2006) Fungal laccases—occurrence and properties. FEMS Microbiol Rev 30:215–242
Bankar SB, Bule MV, Singhal RS, Ananthanarayan L (2009) Glucose oxidase—an overview. Biotechnol Adv 27:489–501
Battistuzzi G, Di Rocco G, Leonardi A, Sola M (2003) 1H NMR of native and azide-inhibited laccase from Rhus vernicifera. J Inorg Biochem 96:503–506
Bolz U, Hagenmaier H, Körner W (2001) Phenolic xenoestrogens in surface water, sediments, and sewage sludge from Baden-Württemberg, south-west Germany. Environ Pollut 115:291–301
Boyd GR, Palmeri JM, Zhang S, Grimm DA (2004) Pharmaceuticals and personal care products (PPCPs) and endocrine disrupting chemicals (EDCs) in stormwater canals and Bayou St. John in New Orleans, Louisiana, USA. Sci Total Environ 333:137–148
Brady D, Jordaan J (2009) Advances in enzyme immobilisation. Biotechnol Lett 31:1639–1650
Breen A, Singleton FL (1999) Fungi in lignocellulose breakdown and biopulping. Curr Opin Biotechnol 10:252–258
Brun GL, Bernier M, Losier R, Doe K, Jackman P, Lee HB (2006) Pharmaceutically active compounds in Atlantic Canadian sewage treatment plant effluents and receiving waters, and potential for environmental effects as measured by acute and chronic aquatic toxicity. Environ Toxicol Chem 25:2163–2176
Cabana H, Jiwan JLH, Rozenberg R, Elisashvili V, Penninckx M, Agathos SN, Jones JP (2007a) 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 67:770–778
Cabana H, Jones JP, Agathos SN (2007b) Elimination of endocrine disrupting chemicals using white rot fungi and their lignin modifying enzymes: a review. Eng Life Sci 7:429–456
Cabana H, Jones JP, Agathos SN (2007c) Characterization of cross-linked laccase aggregates and their application to the elimination of endocrine disrupting chemicals. J Biotechnol 132:23–31
Cabana H, Alexandre C, Agathos SN, Jones JP (2009a) 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 100:3447–3458
Cabana H, Jones JP, Agathos SN (2009b) Utilization of cross-linked laccase aggregates in a perfusion basket reactor for the continuous elimination of endocrine-disrupting chemicals. Biotechnol Bioeng 102:1582–1592
Cabana H, Ahamed A, Leduc R (2011) Conjugation of laccase from the white rot fungus Trametes versicolor to chitosan and its utilization for the elimination of triclosan. Bioresour Technol 102:1656–1662
Camarero S, Sarkar S, Ruiz-Dueñas FJ, Martínez MJ, Martínez ÁT (1999) Description of a versatile peroxidase involved in the natural degradation of lignin that has both manganese peroxidase and lignin peroxidase substrate interaction sites. J Biol Chem 274:10324–10330
Cañas AI, Camarero S (2010) Laccases and their natural mediators: biotechnological tools for sustainable eco-friendly processes. Biotechnol Adv 28:694–705
Castellanos IJ, Cruz G, Crespo R, Griebenow K (2002) Encapsulation-induced aggregation and loss in activity of γ-chymotrypsin and their prevention. J Control Release 81:307–319
Catapane M, Nicolucci C, Menale C, Mita L, Rossi S, Mita DG, Diano N (2013) Enzymatic removal of estrogenic activity of nonylphenol and octylphenol aqueous solutions by immobilized laccase from Trametes versicolor. J Hazard Mater 248–249:337–346
Cecen F, Aktas Ö (2011) Activated carbon for water and wastewater treatment: integration of adsorption and biological treatment. Weinheim, Wiley VCH
Cirja M, Ivashechkin P, Schäffer A, Corvini PFX (2008) Factors affecting the removal of organic micropollutants from wastewater in conventional treatment plants (CTP) and membrane bioreactors (MBR). Rev Environ Sci Biotechnol 7:61–78
Claus H (2003) Laccases and their occurrence in prokaryotes. Arch Microbiol 179:145–150
Claus H (2004) Laccases: structure, reactions, distribution. Micron 35:93–96
Corvini PFX, Shahgaldian P (2010) LANCE: laccase-nanoparticle conjugates for the elimination of micropollutants (endocrine disrupting chemicals) from wastewater in bioreactors. Rev Environ Sci Biotechnol 9:23–27
De Maio A, El-Masry MM, Portaccio M, Diano N, Di Martino S, Mattei A, Bencivenga U, Mita DG (2003) Influence of the spacer length on the activity of enzymes immobilised on nylon/polyGMA membranes: part 1. Isothermal conditions. J Mol Catal B Enzym 21:239–252
Dec J, Haider K, Bollag JM (2003) Release of substituents from phenolic compounds during oxidative coupling reactions. Chemosphere 52:549–556
Demarche P, Junghanns C, Mazy N, Agathos SN (2012) Design-of-experiment strategy for the formulation of laccase biocatalysts and their application to degrade bisphenol A. New Biotechnol 30:96–103
Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for community action in the field of water policy. OJ L327:1–72
Directive 2008/105/EC of the European Parliament and of the Council of 16 December 2008 on environmental quality standards in the field of water policy, amending and subsequently repealing Council Directives 82/176/EEC, 83/513/EEC, 84/156/EEC, 84/491/EEC, 86/280/EEC and amending Directive 2000/60/EC of the European Parliament and of the Council. OJ L348:84–97
Durán N, Esposito E (2000) Potential applications of oxidative enzymes and phenoloxidase-like compounds in wastewater and soil treatment: a review. Appl Catal B Environ 28:83–99
Durán N, Rosa MA, D’Annibale A, Gianfreda L (2002) Applications of laccases and tyrosinases (phenoloxidases) immobilized on different supports: a review. Enzym Microb Technol 31:907–931
Escher BI, Baumgartner R, Koller M, Treyer K, Lienert J, McArdell CS (2011) Environmental toxicology and risk assessment of pharmaceuticals from hospital wastewater. Water Res 45:75–92
Fernandez MP, Ikonomou MG, Buchanan I (2007) An assessment of estrogenic organic contaminants in Canadian wastewaters. Sci Total Environ 373:250–269
Fukuda T, Uchida H, Takashima Y, Uwajima T, Kawabata T, Suzuki M (2001) Degradation of bisphenol A by purified laccase from Trametes villosa. Biochem Biophys Res Commun 284:704–706
Fukuda T, Uchida H, Suzuki M, Miyamoto H, Morinaga H, Nawata H, Uwajima T (2004) Transformation products of bisphenol A by a recombinant Trametes villosa laccase and their estrogenic activity. J Chem Technol Biotechnol 79:1212–1218
Galliker P, Hommes G, Schlosser D, Corvini PFX, Shahgaldian P (2010) Laccase-modified silica nanoparticles efficiently catalyze the transformation of phenolic compounds. J Colloid Interface Sci 349:98–105
Gasser CA, Hommes G, Schäffer A, Corvini PFX (2012) Multi-catalysis reactions: new prospects and challenges of biotechnology to valorize lignin. Appl Microbiol Biotechnol 95:1115–1134
Gasser CA, Yu L, Svojitka J, Wintgens T, Ammann EM, Shahgaldian P, Corvini PFX, Hommes G (2014) Advanced enzymatic elimination of phenolic contaminants in wastewater: a nano approach at field scale. Appl Microbiol Biotechnol 98:3305–3316
Georgieva S, Godjevargova T, Mita DG, Diano N, Menale C, Nicolucci C, Romano C, Mita L, Golovinsky E (2010) Non-isothermal bioremediation of waters polluted by phenol and some of its derivatives by laccase covalently immobilized on polypropylene membranes. J Mol Catal B Enzym 66:210–218
Giardina P, Faraco V, Pezzella C, Piscitelli A, Vanhulle S, Sannia G (2010) Laccases: a never-ending story. Cell Mol Life Sci 67:369–385
Gómez MJ, Petrovic M, Fernández-Alba AR, Barceló D (2006) Determination of pharmaceuticals of various therapeutic classes by solid-phase extraction and liquid chromatography-tandem mass spectrometry analysis in hospital effluent wastewaters. J Chromatogr A 1114:224–233
González Alonso S, Catalá M, Maroto RR, Gil JLR, de Miguel AG, Valcárcel Y (2010) Pollution by psychoactive pharmaceuticals in the rivers of Madrid metropolitan area (Spain). Environ Int 36:195–201
González S, Petrovic M, Barceló D (2007) Removal of a broad range of surfactants from municipal wastewater—comparison between membrane bioreactor and conventional activated sludge treatment. Chemosphere 67:335–343
Gracia-Lor E, Sancho JV, Serrano R, Hernández F (2012) Occurrence and removal of pharmaceuticals in wastewater treatment plants at the Spanish Mediterranean area of Valencia. Chemosphere 87:453–462
Greim HA (2004) The endocrine and reproductive system: adverse effects of hormonally active substances? Pediatrics 113:1070–1075
Hirsch R, Ternes T, Haberer K, Kratz KL (1999) Occurrence of antibiotics in the aquatic environment. Sci Total Environ 225:109–118
Hommes G, Gasser CA, Howald CBC, Goers R, Schlosser D, Shahgaldian P, Corvini PFX (2012) Production of a robust nanobiocatalyst for municipal wastewater treatment. Bioresour Technol 115:8–15
Hommes G, Gasser CA, Ammann EM, Corvini PFX (2013) Determination of oxidoreductase activity using a high-throughput microplate respiratory measurement. Anal Chem 85:283–291
Hu JY, Aizawa T, Ookubo S (2002) Products of aqueous chlorination of bisphenol A and their estrogenic activity. Environ Sci Technol 36:1980–1987
Husain Q, Qayyum S (2013) Biological and enzymatic treatment of bisphenol A and other endocrine disrupting compounds: a review. Crit Rev Biotechnol 33:260–292
Iimura Y, Hartikainen P, Tatsumi K (1996) Dechlorination of tetrachloroguaiacol by laccase of white-rot basidiomycete Coriolus versicolor. Appl Microbiol Biotechnol 45:434–439
Jager T (2011) Some good reasons to ban ECx and related concepts in ecotoxicology. Environ Sci Technol 45:8180–8181
Jarosz-Wilkołazka A, Luterek J, Olszewska A (2008) Catalytic activity of versatile peroxidase from Bjerkandera fumosa at different pH. Biocatal Biotransfor 26:280–287
Jin X, Jiang G, Huang G, Liu J, Zhou Q (2004) Determination of 4-tert-octylphenol, 4-nonylphenol and bisphenol A in surface waters from the Haihe River in Tianjin by gas chromatography-mass spectrometry with selected ion monitoring. Chemosphere 56:1113–1119
Jochems P, Satyawali Y, Diels L, Dejonghe W (2011) Enzyme immobilization on/in polymeric membranes: status, challenges and perspectives in biocatalytic membrane reactors (BMRs). Green Chem 13:1609–1623
Kandelbauer A, Maute O, Kessler RW, Erlacher A, Gubitz GM (2004) Study of dye decolorization in an immobilized laccase enzyme-reactor using online spectroscopy. Biotechnol Bioeng 87:552–563
Karthikeyan KG, Meyer MT (2006) Occurrence of antibiotics in wastewater treatment facilities in Wisconsin, USA. Sci Total Environ 361:196–207
Kasprzyk-Hordern B, Dinsdale RM, Guwy AJ (2009) The removal of pharmaceuticals, personal care products, endocrine disruptors and illicit drugs during wastewater treatment and its impact on the quality of receiving waters. Water Res 43:363–380
Kawai S, Umezawa T, Higuchi T (1988) Degradation mechanisms of phenolic β-1 lignin substructure model compounds by laccase of Coriolus versicolor. Arch Biochem Biophys 262:99–110
Kersten PJ, Kalyanaraman B, Hammel KE, Reinhammar B, Kirk TK (1990) Comparison of lignin peroxidase, horseradish peroxidase and laccase in the oxidation of methoxybenzenes. Biochem J 268:475–480
Kim YJ, Nicell JA (2006) Laccase-catalysed oxidation of aqueous triclosan. J Chem Technol Biotechnol 81:1344–1352
Kim SD, Cho J, Kim IS, Vanderford BJ, Snyder SA (2007) Occurrence and removal of pharmaceuticals and endocrine disruptors in South Korean surface, drinking, and waste waters. Water Res 41:1013–1021
Klibanov AM, Alberti ED, Morris ED, Felshin ZM (1980) Enzymatic removal of toxic phenols and anilines from waste waters. J Appl Biochem 2:414–421
Korshin GV, Kim J, Gan L (2006) Comparative study of reactions of endocrine disruptors bisphenol A and diethylstilbestrol in electrochemical treatment and chlorination. Water Res 40:1070–1078
Kudanga T, Nyanhongo GS, Guebitz GM, Burton S (2011) Potential applications of laccase-mediated coupling and grafting reactions: a review. Enzym Microb Technol 48:195–208
Kunamneni A, Ballesteros A, Plou FJ, Alcalde M (2007) Fungal laccase—a versatile enzyme for biotechnological applications. In: Méndez-Vilas A (ed) Communicating current research and educational topics and trends in applied microbiology. Formatex, Badajoz, pp 233–245
Kuster M, López de Alda MJ, Hernando MD, Petrovic M, Martín-Alonso J, Barceló D (2008) Analysis and occurrence of pharmaceuticals, estrogens, progestogens and polar pesticides in sewage treatment plant effluents, river water and drinking water in the Llobregat river basin (Barcelona, Spain). J Hydrol 358:112–123
Laganà A, Bacaloni A, De Leva I, Faberi A, Fago G, Marino A (2004) Analytical methodologies for determining the occurrence of endocrine disrupting chemicals in sewage treatment plants and natural waters. Anal Chim Acta 501:79–88
Lapworth DJ, Baran N, Stuart ME, Ward RS (2012) Emerging organic contaminants in groundwater: a review of sources, fate and occurrence. Environ Pollut 163:287–303
Laskowski R (1995) Some good reasons to ban the use of NOEC, LOEC and related concepts in ecotoxicology. Oikos 73:140–144
Lin AYC, Yu TH, Lin CF (2008) Pharmaceutical contamination in residential, industrial, and agricultural waste streams: risk to aqueous environments in Taiwan. Chemosphere 74:131–141
Lishman L, Smyth SA, Sarafin K, Kleywegt S, Toito J, Peart T, Lee B, Servos M, Beland M, Seto P (2006) Occurrence and reductions of pharmaceuticals and personal care products and estrogens by municipal wastewater treatment plants in Ontario, Canada. Sci Total Environ 367:544–558
Lloret L, Eibes G, Lú-Chau TA, Moreira MT, Feijoo G, Lema JM (2010) Laccase-catalyzed degradation of anti-inflammatories and estrogens. Biochem Eng J 51:124–131
Lloret L, Eibes G, Feijoo G, Moreira MT, Lema JM, Hollmann F (2011) Immobilization of laccase by encapsulation in a sol–gel matrix and its characterization and use for the removal of estrogens. Biotechnol Progress 27:1570–1579
Lloret L, Eibes G, Feijoo G, Moreira MT, Lema JM (2012a) Continuous operation of a fluidized bed reactor for the removal of estrogens by immobilized laccase on Eupergit supports. J Biotechnol 162:404–406
Lloret L, Eibes G, Feijoo G, Moreira MT, Lema JM (2012b) Degradation of estrogens by laccase from Myceliophthora thermophila in fed-batch and enzymatic membrane reactors. J Hazard Mater 213–214:175–183
Lloret L, Hollmann F, Eibes G, Feijoo G, Moreira MT, Lema JM (2012c) Immobilisation of laccase on Eupergit supports and its application for the removal of endocrine disrupting chemicals in a packed-bed reactor. Biodegradation 23:373–386
Lloret L, Eibes G, Feijoo G, Moreira MT, Lema JM (2013a) Application of response surface methodology to study the removal of estrogens in a laccase-mediated continuous membrane reactor. Biocatal Biotransfor 31:197–207
Lloret L, Eibes G, Moreira MT, Feijoo G, Lema JM (2013b) Removal of estrogenic compounds from filtered secondary wastewater effluent in a continuous enzymatic membrane reactor. Identification of biotransformation products. Environ Sci Technol 47:4536–4543
Lloret L, Eibes G, Moreira MT, Feijoo G, Lema JM (2013c) On the use of a high-redox potential laccase as an alternative for the transformation of non-steroidal anti-inflammatory drugs (NSAIDs). J Mol Catal B Enzym 97:233–242
Loos R, Hanke G, Umlauf G, Eisenreich SJ (2007) LC-MS-MS analysis and occurrence of octyl- and nonylphenol, their ethoxylates and their carboxylates in Belgian and Italian textile industry, waste water treatment plant effluents and surface waters. Chemosphere 66:690–699
Loos R, Carvalho R, António DC, Comero S, Locoro G, Tavazzi S, Paracchini B, Ghi-ani M, Lettieri T, Blaha L, Jarosova B, Voorspoels S, Servaes K, Haglund P, Fick J, Lindberg RH, Schwesig D, Gawlik BM (2013) EU-wide monitoring survey on emerging polar organic contaminants in wastewater treatment plant effluents. Water Res 47:6475–6487
Löwenberg J, Zenker A, Baggenstos M, Koch G, Kazner C, Wintgens T (2014) Comparison of two PAC/UF processes for the removal of micropollutants from wastewater treatment plant effluent: process performance and removal efficiency. Water Res 56:26–36
Majeau JA, Brar SK, Tyagi RD (2010) Laccases for removal of recalcitrant and emerging pollutants. Bioresour Technol 101:2331–2350
Maloney SW, Manem J, Mallevialle J, Fiessinge F (1986) Transformation of trace organic compounds in drinking water by enzymic oxidative coupling. Environ Sci Technol 20:249–253
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 176:836–842
Margot J, Kienle C, Magnet A, Weil M, Rossi L, de Alencastro LF, Abegglen C, Thonney D, Chèvre N, Schärer M, Barry DA (2013a) Treatment of micropollutants in municipal wastewater: ozone or powdered activated carbon? Sci Total Environ 461–462:480–498
Margot J, Maillard J, Rossi L, Barry DA, Holliger C (2013b) Influence of treatment conditions on the oxidation of micropollutants by Trametes versicolor laccase. New Biotechnol 30:803–813
Martín J, Camacho-Muñoz D, Santos JL, Aparicio I, Alonso E (2012) Occurrence of pharmaceutical compounds in wastewater and sludge from wastewater treatment plants: removal and ecotoxicological impact of wastewater discharges and sludge disposal. J Hazard Mater 239–240:40–47
Mayer AM, Staples RC (2002) Laccase: new functions for an old enzyme. Phytochemistry 60:551–565
Metcalfe CD, Miao XS, Koenig BG, Struger J (2003) Distribution of acidic and neutral drugs in surface waters near sewage treatment plants in the lower great lakes, Canada. Environ Toxicol Chem 22:2881–2889
Miao XS, Bishay F, Chen M, Metcalfe CD (2004) Occurrence of antimicrobials in the final effluents of wastewater treatment plants in Canada. Environ Sci Technol 38:3533–3541
Minuth W, Klischies M, Esser K (1978) The phenoloxidases of the ascomycete Podospora anserina. Structural differences between laccases of high and low molecular weight. Eur J Biochem 90:73–82
Mohapatra DP, Brar SK, Tyagi RD, Surampalli RY (2010a) Degradation of endocrine disrupting bisphenol A during pre-treatment and biotransformation of wastewater sludge. Chem Eng J 163:273–283
Mohapatra DP, Brar SK, Tyagi RD, Surampalli RY (2010b) Physico-chemical pre-treatment and biotransformation of wastewater and wastewater sludge—fate of bisphenol A. Chemosphere 78:923–941
Molitoris HP, Van Breemen JFL, Van Bruggen EFJ, Esser K (1972) The phenoloxidase of the ascomycete Podospora anserina X. Electron microscopic studies on the structure of laccases I, II, and III. Biochim Biophys Acta 271:286–291
Morozova O, Shumakovich G, Shleev S, Yaropolov Y (2007) Laccase-mediator systems and their applications: a review. Appl Biochem Microbiol 43:523–535
Murugesan K, Chang YY, Kim YM, Jeon JR, Kim EJ, Chang YS (2010) Enhanced transformation of triclosan by laccase in the presence of redox mediators. Water Res 44:298–308
Nair RR, Demarche P, Agathos SN (2013) Formulation and characterization of an immobilized laccase biocatalyst and its application to eliminate organic micropollutants in wastewater. New Biotechnol 30:814–823
Nguyen LN, Hai FI, Price WE, Leusch FDL, Roddick F, Ngo HH, Guo W, Magram SF, Nghiem LD (2014) The effects of mediator and granular activated carbon addition on degradation of trace organic contaminants by an enzymatic membrane reactor. Bioresour Technol 167:169–177
Ostadhadi-Dehkordi S, Tabatabaei-Sameni M, Forootanfar H, Kolahdouz S, Ghazi-Khansari M, Faramarzi MA (2012) Degradation of some benzodiazepines by a laccase-mediated system in aqueous solution. Bioresour Technol 125:344–347
Pal A, Gin KYH, Lin AYC, Reinhard M (2010) Impacts of emerging organic contaminants on freshwater resources: review of recent occurrences, sources, fate and effects. Sci Total Environ 408:6062–6069
Pierre AC (2004) The sol-gel encapsulation of enzymes. Biocatal Biotransform 22:145–170
Piontek K, Antorini M, Choinowski T (2002) Crystal structure of a laccase from the fungus Trametes versicolor at 1.90-Å resolution containing a full complement of coppers. J Biol Chem 277:37663–37669
Proia L, Osorio V, Soley S, Köck-Schulmeyer M, Pérez S, Barceló D, Romaní AM, Sabater S (2013) Effects of pesticides and pharmaceuticals on biofilms in a highly impacted river. Environ Pollut 178:220–228
Reinhammar BRM, Vänngåd TI (1971) The electron-accepting sites in Rhus vernicifera laccase as studied by anaerobic oxidation-reduction titrations. Eur J Biochem 18:463–468
Rosenstiel R, Ort C (2008) Massnahmen in ARA zur weitergehenden Elimination von Mikroverunreinigungen, Kostenstudie. BAFU, Winterthur
Sánchez-Avila J, Bonet J, Velasco G, Lacorte S (2009) Determination and occurrence of phthalates, alkylphenols, bisphenol A, PBDEs, PCBs and PAHs in an industrial sewage grid discharging to a municipal wastewater treatment plant. Sci Total Environ 407:4157–4167
Santos LHMLM, Gros M, Rodriguez-Mozaz S, Delerue-Matos C, Pena A, Barceló D, Montenegro MCBSM (2013) Contribution of hospital effluents to the load of pharmaceuticals in urban wastewaters: identification of ecologically relevant pharmaceuticals. Sci Total Environ 461–462:302–316
Schwarzenbach RP, Escher BI, Fenner K, Hofstetter TB, Johnson CA, von Gunten U, Wehrli B (2006) The challenge of micropollutants in aquatic systems. Science 313:1072–1077
Sheldon RA (2007) Enzyme immobilization: the quest for optimum performance. Adv Synth Catal 349:1289–1307
Silva BF, Jelic A, López-Serna R, Mozeto AA, Petrovic M, Barceló D (2011) Occurrence and distribution of pharmaceuticals in surface water, suspended solids and sediments of the Ebro river basin, Spain. Chemosphere 85:1331–1339
Snyder SA (2008) Occurrence, treatment, and toxicological relevance of EDCs and pharmaceuticals in water. Ozone Sci Eng 30:65–69
Snyder S, Adham S, Redding AM, Cannon FS, DeCarolis J, Oppenheimer J, Wert EC, Yoon Y (2007) Role of membranes and activated carbon in the removal of endocrine disruptors and pharmaceuticals. Desalination 202:156–181
Solomon EI, Chen P, Metz M, Lee SK, Palmer AE (2001) Oxygen binding, activation, and reduction to water by copper proteins. Angew Chem Int Ed 40:4570–4590
Songulashvili G, Jimenéz-Tobón GA, Jaspers C, Penninckx MJ (2012) Immobilized laccase of Cerrena unicolor for elimination of endocrine disruptor micropollutants. Fungal Biol 116:883–889
Srinivasan C, Dsouza TM, Boominathan K, Reddy CA (1995) Demonstration of laccase in the white rot basidiomycete Phanerochaete chrysosporium BKM-F1767. Appl Environ Microbiol 61:4274–4277
Stasinakis AS, Gatidou G, Mamais D, Thomaidis NS, Lekkas TD (2008) Occurrence and fate of endocrine disrupters in Greek sewage treatment plants. Water Res 42:1796–1804
Strong PJ, Claus H (2011) Laccase: a review of its past and its future in bioremediation. Crit Rev Environ Sci Technol 41:373–434
Ternes TA (1998) Occurrence of drugs in German sewage treatment plants and rivers. Water Res 32:3245–3260
Ternes TA, Stumpf M, Mueller J, Haberer K, Wilken RD, Servos M (1999) Behavior and occurrence of estrogens in municipal sewage treatment plants—I. Investigations in Germany, Canada and Brazil. Sci Total Environ 225:81–90
Thurston CF (1994) The structure and function of fungal laccases. Microbiology 140:19–26
Touahar IE, Haroune L, Ba S, Bellenger JP, 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
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 8:125–140
Tsutsumi Y, Haneda T, Nishida T (2001) Removal of estrogenic activities of bisphenol A and nonylphenol by oxidative enzymes from lignin-degrading basidiomycetes. Chemosphere 42:271–276
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 287:355–358
Vethaak AD, Lahr J, Schrap SM, Belfroid AC, Rijs GBJ, Gerritsen A, de Boer J, Bulder AS, Grinwis GCM, Kuiper RV, Legler J, Murk TAJ, Peijnenburg W, Verhaar HJM, de Voogt P (2005) An integrated assessment of estrogenic contamination and biological effects in the aquatic environment of The Netherlands. Chemosphere 59:511–524
Vidal-Dorsch DE, Bay SM, Maruya K, Snyder SA, Trenholm RA, Vanderford BJ (2012) Contaminants of emerging concern in municipal wastewater effluents and marine receiving water. Environ Toxicol Chem 31:2674–2682
Waltman EL, Venables BJ, Waller WT (2006) Triclosan in a north Texas wastewater treatment plant and the influent and effluent of an experimental constructed wetland. Environ Toxicol Chem 25:367–372
Weng SS, Ku KL, Lai HT (2012) The implication of mediators for enhancement of laccase oxidation of sulfonamide antibiotics. Bioresour Technol 113:259–264
Wick A, Fink G, Joss A, Siegrist H, Ternes TA (2009) Fate of beta blockers and psycho-active drugs in conventional wastewater treatment. Water Res 43:1060–1074
Wong D (2009) Structure and action mechanism of ligninolytic enzymes. Appl Biochem Biotechnol 157:174–209
Xu F, Shin W, Brown SH, Wahleithner JA, Sundaram UM, Solomon EI (1996) A study of a series of recombinant fungal laccases and bilirubin oxidase that exhibit significant differences in redox potential, substrate specificity, and stability. Biochim Biophys Acta 1292:303–311
Xu F, Damhus T, Danielsen S, Østergaard LH (2007) Catalytic applications of laccase. In: Schmid RD, Urlacher VB (eds) Modern biooxidation. Wiley VCH, Weinheim, pp 43–75
Ying GG, Kookana RS (2007) Triclosan in wastewaters and biosolids from Australian wastewater treatment plants. Environ Int 33:199–205
Ying GG, Kookana RS, Kumar A, Mortimer M (2009) Occurrence and implications of estrogens and xenoestrogens in sewage effluents and receiving waters from South East Queensland. Sci Total Environ 407:5147–5155
Yuan S, Jiang X, Xia X, Zhang H, Zheng S (2013) Detection, occurrence and fate of 22 psychiatric pharmaceuticals in psychiatric hospital and municipal wastewater treatment plants in Beijing, China. Chemosphere 90:2520–2525
Zhang Z, Feng Y, Gao P, Wang C, Ren N (2011) Occurrence and removal efficiencies of eight EDCs and estrogenicity in a STP. J Environ Monit 13:1366–1373
Zhao JL, Ying GG, Liu YS, Chen F, Yang JF, Wang L (2010a) Occurrence and risks of triclosan and triclocarban in the Pearl River system, South China: from source to the receiving environment. J Hazard Mater 179:215–222
Zhao JL, Ying GG, Liu YS, Chen F, Yang JF, Wang L, Yang XB, Stauber JL, Warne MSJ (2010b) Occurrence and a screening-level risk assessment of human pharmaceuticals in the Pearl River system, South China. Environ Toxicol Chem 29:1377–1384
Zhou Z, Hartmann M (2012) Recent progress in biocatalysis with enzymes immobilized on mesoporous hosts. Top Catal 55:1081–1100
Zimmermann YS, Shahgaldian P, Corvini PFX, Hommes G (2011) Sorption-assisted surface conjugation: a way to stabilize laccase enzyme. Appl Microbiol Biotechnol 92:169–178
Acknowledgments
The support of the European Commission within the 7th framework program under grant agreement 265946 (MINOTAURUS) and FP7-KBBE-2012-6-311933 (Water4Crops), the Swiss National Science Foundation, National Research Program 66 (Project 4066-136686), and the Commission for Technology and Innovation of the Swiss Federal Office for Professional Education and Technology (Grant PFNM-NM 12608.1) is gratefully acknowledged. Special thanks are due to Yannick-Serge Zimmermann (Institute for Ecopreneurship, University of Applied Sciences and Arts Northwestern Switzerland) for the valuable advice.
Conflict of interest
The authors confirm that they have no conflict of interests.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gasser, C.A., Ammann, E.M., Shahgaldian, P. et al. Laccases to take on the challenge of emerging organic contaminants in wastewater. Appl Microbiol Biotechnol 98, 9931–9952 (2014). https://doi.org/10.1007/s00253-014-6177-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-014-6177-6