Technical Papers
Feb 10, 2018

Biodegradation of Chlortetracycline by Trametes versicolor–Produced Laccase: By-Product Identification

Publication: Journal of Environmental Engineering
Volume 144, Issue 4

Abstract

Chlortetracycline (CTC) is one of the widely used antibiotics in animal farms commonly found in wastewater and surface water and therefore development of new treatment technologies is necessary to avoid adverse effects on humans and the environment. White-rot fungi laccase is an attractive candidate for safe treatment of water and wastewater contaminated with micropollutants. In this work, Trametes versicolor laccase was produced and response surface methodology with a central composite design was employed to investigate the effects of different parameters including pH, temperature, mediator concentration, and enzyme concentration on biodegradation of CTC in the aqueous phase. A quadratic model was fitted to express the effects of each parameter including quadratic, linear, and interaction terms. The values for R2 and adjusted R2 were 0.85 and 0.70, respectively, indicating a reasonably good model for practical applications. Among the examined parameters, linear terms of temperature and pH had the largest effects. It was observed that the maximum degradation efficiency of approximately 95% can be achieved at pH, temperature, enzyme concentration, and mediator concentration of 5.2, 35.5°C, 62.3  units/L, and 10.9 μM, respectively. Also, three structures were proposed for the by-products of CTC biodegradation using mass spectroscopy data, and the yeast estrogen screen test showed that these by-products are not toxic.

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Acknowledgments

The authors are sincerely thankful to the Natural Sciences and Engineering Research Council of Canada (Discovery Grant 355254 and Strategic Grants), and Ministère des Relations internationales du Québec (122523) (Coopération Québec-Catalanya 2012-2014) for financial support. INRS-ETE is thanked for providing Mr. Mehrdad Taheran “Bourse d’excellence” scholarship for his Ph.D. studies. The views or opinions expressed in this article are those of the authors.

References

Andreu, G., and Vidal, T. (2011). “Effects of laccase-natural mediator systems on kenaf pulp.” Bioresour. Technol., 102(10), 5932–5937.
Bistan, M., Podgorelec, M., Marinšek Logar, R., and Tišler, T. (2012). “Yeast estrogen screen assay as a tool for detecting estrogenic activity in water bodies.” Food Technol. Biotechnol., 50(4), 427–433.
Borghi, A. A., and Palma, M. S. A. (2014). “Tetracycline: Production, waste treatment and environmental impact assessment.” Braz. J. Pharm. Sci., 50(1), 25–40.
Chang, P. H., Li, Z., Jean, J. S., Jiang, W. T., Wang, C. J., and Lin, K. H. (2012). “Adsorption of tetracycline on 2:1 layered non-swelling clay mineral illite.” Appl. Clay Sci., 67–68, 158–163.
Claus, H., Faber, G., and König, H. (2002). “Redox-mediated decolorization of synthetic dyes by fungal laccases.” Appl. Microbiol. Biotechnol., 59(6), 672–678.
Davis, J., Truman, C., Kim, S., Ascough, J., and Carlson, K. (2006). “Antibiotic transport via runoff and soil loss.” J. Environ. Qual., 35(6), 2250–2260.
de Cazes, M., et al. (2014). “Design and optimization of an enzymatic membrane reactor for tetracycline degradation.” Catal. Today, 236, 146–152.
de Godos, I., Muñoz, R., and Guieysse, B. (2012). “Tetracycline removal during wastewater treatment in high-rate algal ponds.” J. Hazard. Mater., 229–230, 446–449.
Design-Expert version 7 [Computer software]. Stat-Ease, Inc., Minneapolis.
Ding, H., et al. (2016). “Simultaneous removal and degradation characteristics of sulfonamide, tetracycline, and quinolone antibiotics by laccase-mediated oxidation coupled with soil adsorption.” J. Hazard. Mater., 307, 350–358.
Eibes, G., Debernardi, G., Feijoo, G., Moreira, M. T., and Lema, J. M. (2011). “Oxidation of pharmaceutically active compounds by a ligninolytic fungal peroxidase.” Biodegradation, 22(3), 539–550.
Faramarzi, M. A., and Forootanfar, H. (2011). “Biosynthesis and characterization of gold nanoparticles produced by laccase from Paraconiothyrium variabile.” Colloids Surf. B, 87(1), 23–27.
García-Galán, M. J., Rodríguez-Rodríguez, C. E., Vicent, T., Caminal, G., Díaz-Cruz, M. S., and Barceló, D. (2011). “Biodegradation of sulfamethazine by Trametes versicolor: Removal from sewage sludge and identification of intermediate products by UPLC-QqTOF-MS.” Sci. Total Environ., 409(24), 5505–5512.
Gómez-Pacheco, C. V., Sánchez-Polo, M., Rivera-Utrilla, J., and López-Peñalver, J. (2011). “Tetracycline removal from waters by integrated technologies based on ozonation and biodegradation.” Biochem. Eng. J., 178, 115–121.
Hao, R., Xiao, X., Zuo, X., Nan, J., and Zhang, W. (2012). “Efficient adsorption and visible-light photocatalytic degradation of tetracycline hydrochloride using mesoporous BiOI microspheres.” J. Hazard. Mater., 209–210, 137–145.
Hassan, S. S. M., Abdel-Shafy, H. I., and Mansour, M. S. M. (2017). “Removal of pharmaceutical compounds from urine via chemical coagulation by green synthesized ZnO-nanoparticles followed by microfiltration for safe reuse.” Arab. J. Chem., in press.
Hata, T., Shintate, H., Kawai, S., Okamura, H., and Nishida, T. (2010). “Elimination of carbamazepine by repeated treatment with laccase in the presence of 1-hydroxybenzotriazole.” J. Hazard. Mater., 181(1–3), 1175–1178.
Hoese, A., et al. (2009). “Chlortetracycline and tylosin runoff from soils treated with antimicrobial containing manure.” J. Environ. Sci. Health. Part B, 44(4), 371–378.
Hou, J., Wang, C., Mao, D., and Luo, Y. (2016). “The occurrence and fate of tetracyclines in two pharmaceutical wastewater treatment plants of Northern China.” Environ. Sci. Pollut. Res., 23(2), 1722–1731.
Isidori, M., Bellotta, M., Cangiano, M., and Parrella, A. (2009). “Estrogenic activity of pharmaceuticals in the aquatic environment.” Environ. Int., 35(5), 826–829.
Kang, J., Liu, H., Zheng, Y. M., Qu, J., and Chen, J. P. (2010). “Systematic study of synergistic and antagonistic effects on adsorption of tetracycline and copper onto a chitosan.” J. Colloid Interface Sci., 344(1), 117–125.
Karthikeyan, K. G., and Meyer, M. T. (2006). “Occurrence of antibiotics in wastewater treatment facilities in Wisconsin, USA.” Sci. Total Environ., 361(1–3), 196–207.
Khan, M. H., and Jung, J.-Y. (2016). “Ozonation of chlortetracycline in the aqueous phase: Degradation intermediates and pathway confirmed by NMR.” Chemosphere, 152, 31–38.
Khouni, I., Marrot, B., and Ben Amar, R. (2010). “Decolourization of the reconstituted dye bath effluent by commercial laccase treatment: Optimization through response surface methodology.” Chem. Eng. J., 156(1), 121–133.
Kim, S., Eichhorn, P., Jensen, J. N., Weber, A. S., and Aga, D. S. (2005). “Removal of antibiotics in wastewater: Effect of hydraulic and solid retention times on the fate of tetracycline in the activated sludge process.” Environ. Sci. Technol., 39(15), 5816–5823.
Li, D., Yang, J., Zhou, J., Wei, Q., and Huang, F. (2014). “Direct electrochemistry of laccase and a hydroquinone biosensing application employing ZnO loaded carbon nanofibers.” RSC Adv., 4(106), 61831–61840.
Liao, X., Zou, R., Li, B., Tong, T., Xie, S., and Yuan, B. (2017). “Biodegradation of chlortetracycline by acclimated microbiota.” Process Saf. Environ. Protection, 109, 11–17.
Llorca, M., et al. (2015). “Identification of new transformation products during enzymatic treatment of tetracycline and erythromycin antibiotics at laboratory scale by an on-line turbulent flow liquid-chromatography coupled to a high resolution mass spectrometer LTQ-Orbitrap.” Chemosphere, 119, 90–98.
Lloret, L., Eibes, G., Lú-Chau, T. A., Moreira, M. T., Feijoo, G., and Lema, J. M. (2010). “Laccase-catalyzed degradation of anti-inflammatories and estrogens.” Biochem. Eng. J., 51(3), 124–131.
Madhavi, V., and Lele, S. (2009). “Laccase: Properties and applications.” BioResources, 4(4), 1694–1717.
Marco-Urrea, E., Pérez-Trujillo, M., Blánquez, P., Vicent, T., and Caminal, G. (2010a). “Biodegradation of the analgesic naproxen by Trametes versicolor and identification of intermediates using HPLC-DAD-MS and NMR.” Bioresour. Technol., 101(7), 2159–2166.
Marco-Urrea, E., Pérez-Trujillo, M., Cruz-Morató, C., Caminal, G., and Vicent, T. (2010b). “Degradation of the drug sodium diclofenac by Trametes versicolor pellets and identification of some intermediates by NMR.” J. Hazard. Mater., 176(1–3), 836–842.
Marco-Urrea, E., Pérez-Trujillo, M., Vicent, T., and Caminal, G. (2009). “Ability of white-rot fungi to remove selected pharmaceuticals and identification of degradation products of ibuprofen by Trametes versicolor.” Chemosphere, 74(6), 765–772.
Margot, J., Maillard, J., Rossi, L., Barry, D. A., and Holliger, C. (2013). “Influence of treatment conditions on the oxidation of micropollutants by Trametes versicolor laccase.” New Biotechnol., 30(6), 803–813.
Maruyama, T., et al. (2003). “Enzymatic degradation of p-chlorophenol in a two-phase flow microchannel system.” Lab Chip, 3(4), 308–312.
Michniewicz, A., Ledakowicz, S., Ullrich, R., and Hofrichter, M. (2008). “Kinetics of the enzymatic decolorization of textile dyes by laccase from Cerrena unicolor.” Dyes Pigm., 77(2), 295–302.
Naghdi, M., et al. (2017). “Pine-wood derived nanobiochar for removal of carbamazepine from aqueous media: Adsorption behavior and influential parameters.” Arab. J. Chem., in press.
Parolo, M. E., Savini, M. C., Vallés, J. M., Baschini, M. T., and Avena, M. J. (2008). “Tetracycline adsorption on montmorillonite: pH and ionic strength effects.” Appl. Clay Sci., 40(1–4), 179–186.
Puicharla, R., Mohapatra, D. P., Brar, S. K., Drogui, P., Auger, S., and Surampalli, R. Y. (2014). “A persistent antibiotic partitioning and co-relation with metals in wastewater treatment plant—Chlortetracycline.” J. Environ. Chem. Eng., 2(3), 1596–1603.
Pulicharla, R., et al. (2015). “Toxicity of chlortetracycline and its metal complexes to model microorganisms in wastewater sludge.” Sci. Total Environ., 532, 669–675.
Routledge, E. J., and Sumpter, J. P. (1996). “Estrogenic activity of surfactants and some of their degradation products assessed using a recombinant yeast screen.” Environ. Toxicol. Chem., 15(3), 241–248.
Sigoillot, C., et al. (2004). “Natural and recombinant fungal laccases for paper pulp bleaching.” Appl. Microbiol. Biotechnol., 64(3), 346–352.
Søeborg, T., Ingerslev, F., and Halling-Sørensen, B. (2004). “Chemical stability of chlortetracycline and chlortetracycline degradation products and epimers in soil interstitial water.” Chemosphere, 57(10), 1515–1524.
Spengler, P., Körner, W., and Metzger, J. W. (2001). “Substances with estrogenic activity in effluents of sewage treatment plants in southwestern Germany. I: Chemical analysis.” Environ. Toxicol. Chem., 20(10), 2133–2141.
Suda, T., Hata, T., Kawai, S., Okamura, H., and Nishida, T. (2012). “Treatment of tetracycline antibiotics by laccase in the presence of 1-hydroxybenzotriazole.” Bioresour. Technol., 103(1), 498–501.
Taheran, M., Brar, S. K., Verma, M., Surampalli, R. Y., Zhang, T. C., and Valero, J. R. (2016). “Membrane processes for removal of pharmaceutically active compounds (PhACs) from water and wastewaters.” Sci. Total Environ., 547, 60–77.
Taheran, M., Naghdi, M., Brar, S. K., Knystautas, E. J., Verma, M., and Surampalli, R. Y. (2017). “Degradation of chlortetracycline using immobilized laccase on Polyacrylonitrile-biochar composite nanofibrous membrane.” Sci. Total Environ., 605, 315–321.
Tavares, A. P. M., Cristóvão, R. O., Loureiro, J. M., Boaventura, R. A. R., and Macedo, E. A. (2008). “Optimisation of reactive textile dyes degradation by laccase-mediator system.” J. Chem. Technol. Biotechnol., 83(12), 1609–1615.
Tavares, A. P. M., Cristóvão, R. O., Loureiro, J. M., Boaventura, R. A. R., and Macedo, E. A. (2009). “Application of statistical experimental methodology to optimize reactive dye decolourization by commercial laccase.” J. Hazard. Mater., 162(2–3), 1255–1260.
Tran, N. H., Urase, T., and Kusakabe, O. (2010). “Biodegradation characteristics of pharmaceutical substances by whole fungal culture Trametes versicolor and its laccase.” J. Water Environ. Technol., 8(2), 125–140.
Weng, S.-S., Liu, S.-M., and Lai, H.-T. (2013). “Application parameters of laccase-mediator systems for treatment of sulfonamide antibiotics.” Bioresour. Technol., 141, 152–159.

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Go to Journal of Environmental Engineering
Journal of Environmental Engineering
Volume 144Issue 4April 2018

History

Received: Feb 22, 2017
Accepted: Oct 20, 2017
Published online: Feb 10, 2018
Published in print: Apr 1, 2018
Discussion open until: Jul 10, 2018

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Authors

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M. Taheran
Ph.D. Student, Dept. of Water, Earth, and Environment, Institut national de la recherche scientifique-Centre Eau Terre Environnement, Université du Québec, 490, Rue de la Couronne, Québec, QC, Canada G1K 9A9.
M. Naghdi
Ph.D. Student, Dept. of Water, Earth, and Environment, Institut national de la recherche scientifique-Centre Eau Terre Environnement, Université du Québec, 490, Rue de la Couronne, Québec, QC, Canada G1K 9A9.
Professor, Dept. of Water, Earth, and Environment, Institut national de la recherche scientifique-Centre Eau Terre Environnement, Université du Québec, 490, Rue de la Couronne, Québec, QC, Canada G1K 9A9 (corresponding author). E-mail: [email protected]
E. J. Knystautas
Professor, Département de Physique, Université Laval, Québec, QC, Canada G1K 7P4.
M. Verma
Process Engineer, CO2 Solutions, Inc., 2300, rue Jean-Perrin, Québec, QC, Canada G2C 1T9.
R. D. Tyagi
Professor, Dept. of Water, Earth, and Environment, Institut national de la recherche scientifique-Centre Eau Terre Environnement, Université du Québec, 490, Rue de la Couronne, Québec, QC, Canada G1K 9A9.
R. Y. Surampalli, Dist.M.ASCE
President, Global Institute for Energy, Environment and Sustainability, Oak St., P.O. Box 14354, Lenexa, KS 66285.

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