Skip to main content
Log in

Potentiality of a ceramic membrane reactor for the laccase-catalyzed removal of bisphenol A from secondary effluents

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

In this study, the removal of bisphenol A (BPA) by laccase in a continuous enzymatic membrane reactor (EMR) was investigated. The effects of key parameters, namely, type of laccase, pH, and enzyme activity, were initially evaluated. Once optimal conditions were determined, the continuous removal of the pollutant in an EMR was assessed in synthetic and real biologically treated wastewaters. The reactor configuration consisted of a stirred tank reactor coupled to a ceramic membrane, which prevented the sorption of the pollutant and allowed the recovery and recycling of laccase. Nearly complete removal of BPA was attained under both operation regimes with removal yields above 94.5 %. In experiments with real wastewater, the removal of BPA remained high while the presence of colloids and certain ions and the formation of precipitates on the membrane potentially affected enzyme stability and made necessary the periodic addition of laccase. Polymerization and degradation were observed as probable mechanisms of BPA transformation by laccase.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Acero JL, Benitez FJ, Leal AI, Real FJ, Teva F (2010) Membrane filtration technologies applied to municipal secondary effluents for potential reuse. J Hazard Mater 177(1–3):390–398

    Article  CAS  PubMed  Google Scholar 

  • Agenson KO, Oh J-I, Urase T (2003) Retention of a wide variety of organic pollutants by different nanofiltration/reverse osmosis membranes: controlling parameters of process. J Membr Sci 225(1–2):91–103

    Article  CAS  Google Scholar 

  • Ammann EM, Gasser CA, Hommes G, Corvini PFX (2014) Immobilization of defined laccase combinations for enhanced oxidation of phenolic contaminants. Appl Microbiol Biotechnol 98(3):1397–1406

    Article  CAS  PubMed  Google Scholar 

  • Arca-Ramos A, Eibes G, Moreira MT, Feijoo G, Lema JM (2012) Surfactant-assisted two phase partitioning bioreactors for laccase-catalyzed degradation of anthracene. Process Biochem 47(7):1115–1121

    Article  CAS  Google Scholar 

  • Arca-Ramos A, Eibes G, Moreira MT, Feijoo G, Lema JM (2014) Vegetable oils as NAPLs in two phase partitioning bioreactors for the degradation of anthracene by laccase. Chem Eng J 240:281–289

    Article  CAS  Google Scholar 

  • Babot ED, Rico A, Rencoret J, Kalum L, Lund H, Romero J, del Río JC, Martínez ÁT, Gutiérrez A (2011) Towards industrially-feasible delignification and pitch removal by treating paper pulp with Myceliophthora thermophila laccase and a phenolic mediator. Bioresour Technol 102(12):6717–6722

    Article  CAS  PubMed  Google Scholar 

  • Baldrian P (2006) Fungal laccases—occurrence and properties. FEMS Microbiol Rev 30(2):215–242

    Article  CAS  PubMed  Google Scholar 

  • 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(5):429–456

    Article  CAS  Google Scholar 

  • Ciora RJ, Liu PKT (2003) Ceramic membranes for environmental related applications. Fluid/Part Sep J 15:51–60

    CAS  Google Scholar 

  • 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 Biotransform 25(2–4):260–268

    Article  CAS  Google Scholar 

  • European Commission (2007) Commission staff working document on the implementation of the “community strategy for endocrine disrupters”—a range of substances suspected of interfering with the hormone systems of humans and wildlife. Commission of the european communities, Brussels

    Google Scholar 

  • Flint S, Markle T, Thompson S, Wallace E (2012) Bisphenol a exposure, effects, and policy: a wildlife perspective. J Environ Manag 104:19–34

    Article  CAS  Google Scholar 

  • 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(11):1212–1218

    Article  CAS  Google Scholar 

  • 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(1):98–105

    Article  CAS  PubMed  Google Scholar 

  • Gascón V, Díaz I, Márquez-Álvarez C, Blanco R (2014) Mesoporous silicas with tunable morphology for the immobilization of laccase. Molecules 19(6):7057–7071

    Article  PubMed  Google Scholar 

  • Gasser C, Ammann EM, Shahgaldian P, Corvini PFX (2014) Laccases to take on the challenge of emerging organic contaminants in wastewater. Appl Microbiol Biotechnol 98(24):9931–9952

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Huang Q, Weber WJ (2005) Transformation and removal of bisphenol a from aqueous phase via peroxidase-mediated oxidative coupling reactions: efficacy, products, and pathways. Environ Sci Technol 39(16):6029–6036

    Article  CAS  PubMed  Google Scholar 

  • Keum YS, Li QX (2004) Copper dissociation as a mechanism of fungal laccase denaturation by humic acid. Appl Microbiol Biotechnol 64(4):588–592

    Article  CAS  PubMed  Google Scholar 

  • Kim Y-J, Nicell JA (2006a) Impact of reaction conditions on the laccase-catalyzed conversion of bisphenol A. Bioresour Technol 97(12):1431–1442

    Article  CAS  PubMed  Google Scholar 

  • Kim Y-J, Nicell JA (2006b) Laccase-catalyzed oxidation of aqueous triclosan. J Chem Technol Biotechnol 81(8):1344–1352

    Article  CAS  Google Scholar 

  • Kunamneni A, Camarero S, Garcia-Burgos C, Plou F, Ballesteros A, Alcalde M (2008) Engineering and applications of fungal laccases for organic synthesis. Microb Cell Factories 7(1):32

    Article  Google Scholar 

  • Li K, Xu F, Eriksson K-EL (1999) Comparison of fungal laccases and redox mediators in oxidation of a nonphenolic lignin model compound. Appl Environ Microbiol 65(6):2654–2660

    PubMed Central  CAS  PubMed  Google Scholar 

  • López C, Moreira MT, Feijoo G, Lema JM (2004) Dye decolorization by manganese peroxidase in an enzymatic membrane bioreactor. Biotechnol Prog 20(1):74–81

    Article  PubMed  Google Scholar 

  • 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(3):124–131

    Article  CAS  Google Scholar 

  • Lloret L, Eibes G, Feijoo G, Moreira MT, Lema JM (2012a) Degradation of estrogens by laccase from Myceliophthora thermophila in fed-batch and enzymatic membrane reactors. J Hazard Mater 213–214:175–183

    Article  PubMed  Google Scholar 

  • Lloret L, Hollmann F, Eibes G, Feijoo G, Moreira MT, Lema JM (2012b) Immobilization of laccase on eupergit supports and its application for the removal of endocrine disrupting chemicals in a packed-bed reactor. Biodegradation 23(3):373–386

    Article  CAS  PubMed  Google Scholar 

  • Lloret L, Eibes G, Moreira MT, Feijoo G, Lema JM (2013a) 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

    Article  CAS  Google Scholar 

  • 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(9):4536–4543

    Article  CAS  PubMed  Google Scholar 

  • Margot J, Bennati-Granier C, Maillard J, Blanquez P, Barry D, Holliger C (2013a) Bacterial versus fungal laccase: potential for micropollutant degradation. AMB Express 3(1):63

    Article  PubMed Central  PubMed  Google Scholar 

  • Margot J, Maillard J, Rossi L, Barry D, Holliger C (2013b) Influence of treatment conditions on the oxidation of micropollutants by Trametes versicolor laccase. New Biotechnol 30(6):803–813

    Article  CAS  Google Scholar 

  • Michizoe J, Ichinose H, Kamiya N, Maruyama T, Goto M (2005) Biodegradation of phenolic environmental pollutants by a surfactant–laccase complex in organic media. J Biosci Bioeng 99(6):642–647

    Article  CAS  PubMed  Google Scholar 

  • Nghiem LD, Vogel D, Khan S (2008) Characterizing humic acid fouling of nanofiltration membranes using bisphenol A as a molecular indicator. Water Res 42(15):4049–4058

    Article  CAS  PubMed  Google Scholar 

  • Nguyen LN, Hai FI, Price WE, Leusch FDL, Roddick F, McAdam EJ, Magram SF, Nghiem LD (2014) Continuous biotransformation of bisphenol A and diclofenac by laccase in an enzymatic membrane reactor. Int Biodeterior Biodegrad 95(Part A):25–32

    Article  CAS  Google Scholar 

  • Pang R, Li M, Zhang C (2015) Degradation of phenolic compounds by laccase immobilized on carbon nanomaterials: diffusional limitation investigation. Talanta 131:38–45

    Article  CAS  PubMed  Google Scholar 

  • Staples CA, Tilghman Hall A, Friederich U, Caspers N, Klecka GM (2011) Early life-stage and multigeneration toxicity study with bisphenol A and fathead minnows (Pimephales promelas). Ecotoxicol Environ Saf 74(6):1548–1557

    Article  CAS  PubMed  Google Scholar 

  • Su-Hua W, Bing-zhi D, Yu H (2010) Adsorption of bisphenol A by polysulphone membrane. Desalination 253(1–3):22–29

    Article  Google Scholar 

  • Torres-Duarte C, Viana M, Vazquez-Duhalt R (2012) Laccase-mediated transformations of endocrine disrupting chemicals abolish binding affinities to estrogen receptors and their estrogenic activity in zebrafish. Appl Biochem Biotechnol 168(4):864–876

    Article  CAS  PubMed  Google Scholar 

  • Uchida H, Fukuda T, Miyamoto H, Kawabata T, Suzuki M, Uwajima T (2001) Polymerization of bisphenol a by purified laccase from Trametes villosa. Biochem Biophys Res Commun 287(2):355–358

    Article  CAS  PubMed  Google Scholar 

  • Westgate PJ, Park C (2010) Evaluation of proteins and organic nitrogen in wastewater treatment effluents. Environ Sci Technol 44(14):5352–5357

    Article  CAS  PubMed  Google Scholar 

  • Wu G, Gan S, Cui L, Xu Y (2008) Preparation and characterization of PES/TiO2 composite membranes. Appl Surf Sci 254(21):7080–7086

    Article  CAS  Google Scholar 

  • Zhang Y, Causserand C, Aimar P, Cravedi JP (2006) Removal of bisphenol A by a nanofiltration membrane in view of drinking water production. Water Res 40(20):3793–3799

    Article  CAS  PubMed  Google Scholar 

  • Zimmermann Y-S, Shahgaldian P, Corvini PFX, Hommes G (2011) Sorption-assisted surface conjugation: a way to stabilize laccase enzyme. Appl Microbiol Biotechnol 92(1):169–178

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was funded by the Spanish Ministry of Science and Innovation (MICINN, CTQ2013-44762-R). The authors belong to the Galician Competitive Research Group GRC 2013-032, program co-funded by FEDER. Adriana Arca thanks the Spanish Ministry of Education for the FPU grant AP2010-2086. Gemma Eibes thanks the Xunta de Galicia for her postdoctoral grant (I2C Program).

Conflict of interest

The authors declare that they have no competing interests.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Arca-Ramos.

Electronic supplementary material

ESM 1

(PDF 299 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Arca-Ramos, A., Eibes, G., Feijoo, G. et al. Potentiality of a ceramic membrane reactor for the laccase-catalyzed removal of bisphenol A from secondary effluents. Appl Microbiol Biotechnol 99, 9299–9308 (2015). https://doi.org/10.1007/s00253-015-6826-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-015-6826-4

Keywords

Navigation