Bisphenol A (BPA) and triclosan (TCS) are known or suspected potential endocrine disrupting chemicals (EDCs) which may pose a risk to human health and have an environmental impact. Enzyme preparations containing mainly laccases, obtained from Ganoderma stipitatum and Lentinus swartzii, two autochthonous Colombian forest white rot fungi (WRF), previously identified as high enzyme producers, were used to remove BPA and TCS from aqueous solutions. A Box-Behnken factorial design showed that pH, temperature, and duration of treatment were significant model terms for the elimination of BPA and TCS. Our results demonstrated that these EDCs were extensively removed from 5？mg？L？1 solutions after a contact time of 6 hours. Ninety-four percent of TCS and 97.8% of BPA were removed with the enzyme solution from G. stipitatum; 83.2% of TCS and 88.2% of BPA were removed with the L. swartzii enzyme solution. After a 6-hour treatment with enzymes from G. stipitatum and L. swartzii, up to 90% of the estrogenic activity of BPA was lost, as shown by the yeast estrogen screen assay. 2,2-Azino-bis-(3-ethylthiazoline-6-sulfonate) (ABTS) was used as a mediator (laccase/mediator system) and significantly improved the laccase catalyzed elimination of BPA and TCS. The elimination of BPA in the absence of a mediator resulted in production of oligomers of molecular weights of 454, 680, and 906 amu as determined by mass spectra analysis. The elimination of TCS in the same conditions produced dimers, trimers, and tetramers of molecular weights of 574, 859, and 1146？amu. Ecotoxicological studies using Daphnia pulex to determine lethal concentration (LC50) showed an important reduction of the toxicity of BPA and TCS solutions after enzymatic treatments. Use of laccases emerges thus as a key alternative in the development of innovative wastewater treatment technologies. Moreover, the exploitation of local biodiversity appears as a potentially promising approach for identifying new efficient strains for biotechnological applications. 1. Introduction Bisphenol A (BPA) and triclosan (TCS) are present in a great number of products of daily use. Residues of these products are found in many environmental matrices such as rivers and wastewater treatment plant effluents [1, 2]. BPA is a monomer or plasticizer in various polymeric materials [3], and residues of this compound in water appear to be due to incomplete polymerization [4, 5]. Triclosan (TCS) is used as a broad spectrum antibacterial agent and a preservative used in products of domestic use. It is found in cosmetics and personal care
References
[1]
G. R. Boyd, J. M. Palmeri, S. Zhang, and D. A. Grimm, “Pharmaceuticals and personal care products (PPCPs) and endocrine disrupting chemicals (EDCs) in stormwater canals and Bayou St. John in New Orleans, Louisiana, USA,” Science of the Total Environment, vol. 333, no. 1–3, pp. 137–148, 2004.
[2]
J. A. Brotons, M. F. Olea-Serrano, M. Villalobos, V. Pedraza, and N. Olea, “Xenoestrogens released from lacquer coatings in food cans,” Environmental Health Perspectives, vol. 103, no. 6, pp. 608–612, 1995.
[3]
C. A. Staples, P. B. Dorn, G. M. Klecka, S. T. O'Block, and L. R. Harris, “A review of the environmental fate, effects, and exposures of bisphenol A,” Chemosphere, vol. 36, no. 10, pp. 2149–2173, 1998.
[4]
B. Crathorne, C. P. Palmer, and J. A. Stanley, “High-performance liquid chromatographie determination of bisphenol a diglycidyl ether and bisphenol F diglycidyl ether in water,” Journal of Chromatography A, vol. 360, pp. 266–270, 1986.
[5]
G. Matsumoto, “Comparative study on organic constituents in polluted and unpolluted inland aquatic environments. III. Phenols and aromatic acids in polluted and unpolluted waters,” Water Research, vol. 16, no. 5, pp. 551–557, 1982.
[6]
M. Mezcua, M. J. Gómez, I. Ferrer, A. Aguera, M. D. Hernando, and A. R. Fernández-Alba, “Evidence of 2,7/2,8-dibenzodichloro-p-dioxin as a photodegradation product of triclosan in water and wastewater samples,” Analytica Chimica Acta, vol. 524, no. 1-2, pp. 241–247, 2004.
[7]
H. Ishibashi, N. Matsumura, M. Hirano et al., “Effects of triclosan on the early life stages and reproduction of medaka Oryzias latipes and induction of hepatic vitellogenin,” Aquatic Toxicology, vol. 67, no. 2, pp. 167–179, 2004.
[8]
S. Takeda, A. Omura, K. Chayama et al., “Separation and on-line concentration of bisphenol A and alkylphenols by micellar electrokinetic chromatography with anionic surfactant,” Journal of Chromatography A, vol. 1014, no. 1-2, pp. 103–107, 2003.
[9]
A. Soares, K. Jonasson, E. Terrazas, B. Guieysse, and B. Mattiasson, “The ability of white-rot fungi to degrade the endocrine-disrupting compound nonylphenol,” Applied Microbiology and Biotechnology, vol. 66, no. 6, pp. 719–725, 2005.
[10]
S. Jobling, D. Casey, T. Rodgers-Gray et al., “Comparative responses of molluscs and fish to environmental estrogens and an estrogenic effluent,” Aquatic Toxicology, vol. 66, no. 2, pp. 207–222, 2003.
[11]
H. Uchida, T. Fukuda, H. Miyamoto, T. Kawabata, M. Suzuki, and T. Uwajima, “Polymerization of bisphenol A by purified laccase from Trametes villosa,” Biochemical and Biophysical Research Communications, vol. 287, no. 2, pp. 355–358, 2001.
[12]
U.S. Environmental Protection Agency, “Special report on environmental endocrine disruption: An effects assessment and analysis,” EPA/630/R-96/012, Washington, DC, USA, 1997.
[13]
I. A. Lang, T. S. Galloway, A. Scarlett et al., “Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults,” Journal of the American Medical Association, vol. 300, no. 11, pp. 1303–1310, 2008.
[14]
H. Fang, W. Tong, L. M. Shi et al., “Structure-activity relationships for a large diverse set of natural, synthetic, and environmental estrogens,” Chemical Research in Toxicology, vol. 14, no. 3, pp. 280–294, 2001.
[15]
C. M. Foran, E. R. Bennett, and W. H. Benson, “Developmental evaluation of a potential non-steroidal estrogen: triclosan,” Marine Environmental Research, vol. 50, no. 1–5, pp. 153–156, 2000.
[16]
N. Veldhoen, R. C. Skirrow, H. Osachoff et al., “The bactericidal agent triclosan modulates thyroid hormone-associated gene expression and disrupts postembryonic anuran development,” Aquatic Toxicology, vol. 80, pp. 217–227, 2006.
[17]
N. Durán and E. Esposito, “Potential applications of oxidative enzymes and phenoloxidase-like compounds in wastewater and soil treatment: a review,” Applied Catalysis B, vol. 28, no. 2, pp. 83–99, 2000.
[18]
E. Torres, I. Bustos-Jaimes, and S. Le Borgne, “Potential use of oxidative enzymes for the detoxification of organic pollutants,” Applied Catalysis B, vol. 46, no. 1, pp. 1–15, 2003.
[19]
H. Cabana, J. L. Jiwan, R. Rozenberg et al., “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, vol. 67, no. 4, pp. 770–778, 2007.
[20]
H. Cabana, J. P. Jones, and S. N. Agathos, “Elimination of endocrine disrupting chemicals using white rot fungi and their lignin modifying enzymes: a review,” Engineering in Life Sciences, vol. 7, no. 5, pp. 429–456, 2007.
[21]
D. Wesenberg, I. Kyriakides, and S. N. Agathos, “White-rot fungi and their enzymes for the treatment of industrial dye effluents,” Biotechnology Advances, vol. 22, no. 1-2, pp. 161–187, 2003.
[22]
K. Murugesan, Y.-Y. Chang, Y.-M. Kim, J.-R. Jeon, E.-J. Kim, and Y.-S. Chang, “Enhanced transformation of triclosan by laccase in the presence of redox mediators,” Water Research, vol. 44, no. 1, pp. 298–308, 2010.
[23]
Y. S. Keum and Q. X. Li, “Fungal laccase-catalyzed degradation of hydroxy polychlorinated biphenyls,” Chemosphere, vol. 56, no. 1, pp. 23–30, 2004.
[24]
H. Cabana, J. P. Jones, and S. N. Agathos, “Preparation and characterization of cross-linked laccase aggregates and their application to the elimination of endocrine disrupting chemicals,” Journal of Biotechnology, vol. 132, no. 1, pp. 23–31, 2007.
[25]
Y. J. Kim and J. A. Nicell, “Impact of reaction conditions on the laccase-catalyzed conversion of bisphenol A,” Bioresource Technology, vol. 97, no. 12, pp. 1431–1442, 2006.
[26]
Y. J. Kim and J. A. Nicell, “Laccase-catalysed oxidation of aqueous triclosan,” Journal of Chemical Technology and Biotechnology, vol. 81, no. 8, pp. 1344–1352, 2006.
[27]
T. Saito, K. Kato, Y. Yokogawa, M. Nishida, and N. Yamashita, “Detoxification of bisphenol A and nonylphenol by purified extracellular laccase from a fungus isolated from soil,” Journal of Bioscience and Bioengineering, vol. 98, no. 1, pp. 64–66, 2004.
[28]
Y. Tsutsumi, T. Haneda, and T. Nishida, “Removal of estrogenic activities of bisphenol A and nonylphenol by oxidative enzymes from lignin-degrading basidiomycetes,” Chemosphere, vol. 42, no. 3, pp. 271–276, 2001.
[29]
C. Arboleda, A. I. Mejía, A. E. Franco-Molano, G. A. Jiménez, and M. J. Penninckx, “Autochthonous white rot fungi from the tropical forest of Colombia for dye decolourisation and ligninolytic enzymes production,” Sydowia, vol. 60, no. 2, pp. 165–180, 2008.
[30]
J. S. Knapp, E. J. Vantoch-Wood, and F. Zhang, “Use of wood-rotting fungi for the decolorization of dyes and industrial effluents,” in Fungi in Bioremediation, G. M. Gadd, Ed., pp. 242–304, Cambridge University Press, 2001.
[31]
S. B. Pointing, “Feasibility of bioremediation by white-rot fungi,” Applied Microbiology and Biotechnology, vol. 57, no. 1-2, pp. 20–33, 2001.
[32]
R. Bourbonnais and M. G. Paice, “Demethylation and delignification of kraft pulp by Trametes versicolor laccase in the presence of 2,2′-azinobis-(3-ethylbenzthiazoline-6-sulphonate),” Applied Microbiology and Biotechnology, vol. 36, no. 6, pp. 823–827, 1992.
[33]
E. J. Routledge and J. P. Sumpter, “Estrogenic activity of surfactants and some of their degradation products using a recombinant yeast screen,” Environmental Toxicology and Chemistry, vol. 15, pp. 241–248, 1996.
[34]
T. Schultis and J. W. Metzger, “Determination of estrogenic activity by LYES-assay (yeast estrogen screen-assay assisted by enzymatic digestion with lyticase),” Chemosphere, vol. 57, no. 11, pp. 1649–1655, 2004.
[35]
G. A. Harkey, P. F. Landrum, and S. J. Klaine, “Comparison of whole-sediment, elutriate and pore-water exposures for use in assessing sediment-associated organic contaminants in bioassays,” Environmental Toxicology and Chemistry, vol. 13, no. 8, pp. 1315–1329, 1994.
[36]
G. E. P. Box and D. W. Behnken, “Some new three level designs for the study of quantitative variables,” Technometrics, vol. 2, pp. 455–475, 1960.
[37]
D. C. Montgomery, Design and Analysis of Experiments, John Wiley & Sons, New York, NY, USA, 2005.
[38]
S. Y. Okazaki, J. Michizoe, M. Goto, S. Furusaki, H. Wariishi, and H. Tanaka, “Oxidation of bisphenol A catalyzed by laccase hosted in reversed micelles in organic media,” Enzyme and Microbial Technology, vol. 31, no. 3, pp. 227–232, 2002.
[39]
M. Fabbrini, C. Galli, and P. Gentili, “Radical or electron-transfer mechanism of oxidation with some laccase/mediator systems,” Journal of Molecular Catalysis B, vol. 18, no. 1–3, pp. 169–171, 2002.
[40]
R. Bourbonnais and M. G. Paice, “Oxidation of non-phenolic substrates—an expended role for laccase in lignin biodegradation,” FEBS Letters, vol. 267, no. 1, pp. 99–102, 1990.
[41]
R. S. Wolfenden and R. L. Willson, “Radical cations as reference chromogens in kinetic studies of one-electron transfer reactions: pulse radiolysis studies of 2,2′-azinobis-(3-ethylbenzothiazoline-6-sulphonate),” Journal of the Chemical Society, Perkin Transactions 2, pp. 805–812, 1982.
[42]
H. M. Hou, J. T. Zhou, J. Wang, C. H. Du, and B. Yan, “Enhancement of laccase production by Pleurotus ostreatus and its use for the decolorization of anthraquinone dye,” Process Biochemistry, vol. 39, no. 11, pp. 1415–1419, 2004.
[43]
C. Johannes, A. Majcherczyk, and A. Hüttermann, “Degradation of anthracene by laccase of Trametes versicolor in the presence of different mediator compounds,” Applied Microbiology and Biotechnology, vol. 46, no. 3, pp. 313–317, 1996.
[44]
A. M. Campos and E. A. Lissi, “Kinetics of the reaction between 2,2′-azinobis(3-ethylbenzothiazoline-6-sulfonic acid) (ABTS) derived radical cations and phenols,” International Journal of Chemical Kinetics, vol. 29, no. 3, pp. 219–224, 1997.
[45]
C. Henriquez, C. Aliaga, and E. Lissi, “Kinetics profiles in the reaction of abts derived radicals with simple phenols and polyphenols,” Journal of the Chilean Chemical Society, vol. 49, no. 1, pp. 65–67, 2004.
[46]
Q. Huang and W. J. Weber Jr., “Transformation and removal of bisphenol A from aqueous phase via peroxidase-mediated oxidative coupling reactions: efficacy, products, and pathways,” Environmental Science and Technology, vol. 39, no. 16, pp. 6029–6036, 2005.
[47]
H. Cabana, A. Ahamed, and R. Leduc, “Conjugation of laccase from the white rot fungus Trametes versicolor to chitosan and its utilization for the elimination of triclosan,” Bioresource Technology, vol. 102, no. 2, pp. 1656–1662, 2011.
[48]
H.-L. Ma, S. Kermasha, J.-M. Gao, R. M. Borges, and X.-Z. Yu, “Laccase-catalyzed oxidation of phenolic compounds in organic media,” Journal of Molecular Catalysis B, vol. 57, no. 1–4, pp. 89–95, 2009.
