A promising laccase immobilization approach for Bisphenol A removal from aqueous solutions
Graphical abstract
Introduction
For some decades, endocrine disrupting compounds (EDCs) or xenoestrogens have been widely introduced into the environment mainly through the anthropogenic activities. Among these compounds, Bisphenol A (BPA) (2,2-bis (4-hydroxyphenyl) propane), which is mainly used in the production of polycarbonates and epoxy resins, is produced in large amounts worldwide with an annual production exceeding 3.8 million tons (Michałowicz, 2014). The US Environmental Protection Agency (EPA) identified BPA as a compound that may present an unreasonable risk of injury to the environment (Bisphenol A Action Plan, 2010). Recently, in June 2017, the European Chemical Agency (ECHA) has included BPA in the list of “substances of very high concern” (ECHA, 2017). More recently, BPA has been pointed as a potential risk factor in breast cancer development (Shafei et al., 2018). Hence, the presence of BPA in the aquatic environment poses a serious threat to the environment and public health (Arboleda et al., 2013).
Biological processes have been considered as a viable alternative as compared to the conventional physicochemical ones which present a high cost and lead to the formation of hazardous by-products (de Freitas et al., 2017). Instead of microorganisms, the use of enzymes separated from their cells presents several advantages such as no toxicity, high catalytic efficiency, high substrate specificity, shorter reaction time and mild reaction conditions (Sharma et al., 2018). White-rot basidiomycetes secret individual and multiple ligninolytic enzymes, such as laccases, lignin peroxidases (LiPs) and manganese-dependent peroxidases (MnPs), under suitable environmental conditions, with high BPA degrading ability (Bilal et al., 2017). Among the above-mentioned enzymes, laccases (p-diphenol oxygen oxidoreductases, EC 1.10.3.2) are the most frequently studied (Ba and Vinoth Kumar, 2017) due to, unlike peroxidases, laccases use molecular oxygen as the final electron acceptor which is usually available in the environment (Baldrian, 2006). However, the use of enzymes in their soluble form limits their practical application due to their non-reusability, sensitivity towards denaturing agents and low stability (Gasser et al., 2014, Songulashvili et al., 2012). To overcome these drawbacks, immobilization of enzymes is a suitable technique that can increase the stability, facilitate the efficient recovery and re-use of enzymes, thus, enabling their cost-effective use in continuous processes (Gasser et al., 2014, Sheldon and van Pelt, 2013).
Among the reported immobilization techniques (Barrios-Estrada et al., 2018, Gasser et al., 2014), enzyme entrapment in alginate beads is an eco-friendly, low-cost and easy immobilization technique (Chaudhari et al., 2015). Nevertheless, this technique is limited by the porosity of the gel which can lead to enzyme leakage (Brandi et al., 2006). Thus, in the present study, a new strategy consisting in crosslinking laccase enzymes prior to their entrapment into calcium alginate beads was investigated. Further, this approach was applied to BPA removal from aqueous solutions. To the best of our knowledge laccase from Trametes pubescens has not been used for BPA removal before this study.
Section snippets
Chemicals
ABTS (2,2-azino-bis-(3-ethylbenzothiazoline-6-sulfonic acid), sodium alginate, glutaraldehyde (50% v/v), succinic acid, potassium ferricyanide (K3Fe(CN)6), 4-amino-antipyrine and other standard laboratory grade solvents and chemicals were purchased from Sigma Aldrich (St. Louis, MO, USA). Bisphenol A (>97%) used for the degradation studies was provided by Alfa Aesar (Karlsruhe, Germany). All reagents were used as received without further purification.
Microorganism
The fungus Trametes pubescens MB89 was
Crude laccase production
Laccase activity peaked on the 18th day (17907 U L−1). No other ligninolytic enzymes were detected in the culture broth. The enzymatic activity and the specific activity of the crude laccase after ultrafiltration in Amicon were 40,446 U L−1 and 12.3 U mg−1, respectively. This crude laccase was used to perform the subsequent experiments.
Laccase immobilization and leakage
Laccase immobilized by crosslinking prior to entrapment showed a higher immobilization yield (>72%) than that of the laccase immobilized only by entrapment
Conclusion
Crude laccase from T. pubescens was successfully immobilized by entrapment and crosslinking prior to entrapment in alginate beads. In addition, the crosslinked-entrapped laccase reduced laccase leakage from the alginate beads by 7-fold and removed BPA (20 mg L−1) efficiently in 10 successive batches with a removal percentage higher than 70% at the end of the last batch. Also, FTIR results suggested BPA biotransformation by laccase enzymes. Moreover, laccase treated BPA solution showed no
Acknowledgements
We gratefully acknowledge the financial support by Ministry of Higher Education and Scientific Research (MESRS) of Algeria for funding provided under the PNE scholarship Program. Dr. Oihane Beldarrain from the BioMEMS group at Ceit-IK4 (Donostia-San Sebastian, Spain) is gratefully acknowledged for her assistance in the ATR-FTIR analyses.
References (47)
- et al.
Purification and immobilization of laccase from Trichoderma harzianum strain HZN10 and its application in dye decolorization
J. Genet. Eng. Biotechnol.
(2017) - et al.
Emergent contaminants: endocrine disruptors and their laccase-assisted degradation – a review
Sci. Total Environ.
(2018) - et al.
Immobilized ligninolytic enzymes: An innovative and environmental responsive technology to tackle dye-based industrial pollutants – a review
Sci. Total Environ.
(2017) - et al.
In search for practical advantages from the immobilisation of an enzyme: the case of laccase
J. Mol. Catal. B Enzym.
(2006) Chemically aggregated enzymes
Methods Enzymol. Elsevier
(1976)- et al.
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.
(2009) - et al.
Preparation and characterization of cross-linked laccase aggregates and their application to the elimination of endocrine disrupting chemicals
J. Biotechnol.
(2007) - et al.
Biodegradation of textile dyes by immobilized laccase from Coriolopsis gallica into Ca-alginate beads
Int. Biodeterior. Biodegrad.
(2014) - et al.
Removal of bisphenol A by laccases from Pleurotus ostreatus and Pleurotus pulmonarius and evaluation of ecotoxicity of degradation products
Chem. Eng. J.
(2017) - et al.
Direct immobilization of laccase on titania nanoparticles from crude enzyme extracts of P. ostreatus culture for micro-pollutant degradation
Sep. Purif. Technol.
(2017)
Improved enzyme properties upon glutaraldehyde cross-linking of alginate entrapped xylanase from Bacillus licheniformis
Int. J. Biol. Macromol.
Separation and characterization of two extracellular HZOZ-dependent oxidases from ligninolytic cultures of
FEBS Lett.
Reversible immobilization of laccase onto metal-ion-chelated magnetic microspheres for bisphenol A removal
Int. J. Biol. Macromol.
Bisphenol A – sources, toxicity and biotransformation
Environ. Toxicol. Pharmacol.
Formulation and characterization of an immobilized laccase biocatalyst and its application to eliminate organic micropollutants in wastewater
New Biotechnol.
Detection of white-rot fungi by a non-toxic stain
Mycol. Res.
Degradation of phenolic compounds by laccase immobilized on carbon nanomaterials: Diffusional limitation investigation
Talanta
Purification and characterization of two thermostable laccases from Pycnoporus sanguineus and potential role in degradation of endocrine disrupting chemicals
J. Mol. Catal. B Enzym.
Contemporary enzyme based technologies for bioremediation: a review
J. Environ. Manage.
Immobilized laccase of Cerrena unicolor for elimination of endocrine disruptor micropollutants
Fungal Biol.
Repeated batch for dye degradation in an airlift bioreactor by laccase entrapped in copper alginate
Int. Biodeterior. Biodegrad.
Effects of redox potential and hydroxide inhibition on the pH activity profile of fungal laccases
J. Biol. Chem.
Semi-interpenetrating polymer networks (semi-IPNs) for entrapment of laccase and their use in Acid Orange 52 decolorization
Process. Biochem.
Cited by (192)
Construction of copper-manganese based aminoclays with significant laccase-like activity and its prominent degradation performance towards bisphenol A
2024, Journal of Environmental Chemical EngineeringEdible bubbles: A delivery system for enhanced bioaccessibility of phenolic compounds in red fruits and edible flowers
2024, Innovative Food Science and Emerging TechnologiesEnhanced removal of dibutyl phthalate in a laccase-mediator system: Optimized process parameters, kinetics, and environmental impact
2023, Journal of Environmental ManagementResponse surface methodology mediated optimization of diclofenac and norfloxacin biodegradation using laccase immobilized on metal–organic frameworks
2023, Separation and Purification TechnologySpatial nanopores promote laccase degradation of bisphenol A and its analogs
2023, Science of the Total Environment