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Technical Papers
Jun 18, 2020

Identification of Transformation Products for Benzotriazole, Triclosan, and Trimethoprim by Aerobic and Anoxic-Activated Sludge

Publication: Journal of Environmental Engineering
Volume 146, Issue 9

Abstract

This study identified biotransformation products formed from three anthropogenic trace organic compounds (TOrCs) (benzotriazole, triclosan, and trimethoprim) in aerobic and anoxic sludge from a biological nutrient removal (BNR) wastewater treatment system. Liquid chromatography coupled to quadrupole time-of-flight mass spectrometry (LC-QTOF) was used to identify intermediate transformation products. A user-defined compound library was used to target unknowns in samples with a mix of TOrCs without requiring chemical standards and developed using EAWAG-BDD predictive software, which included 37 potential transformation products. Biotransformation batch experiments were conducted using activated sludge from anoxic and aerobic redox regimes of a BNR treatment plant located in Southern Nevada, United States. Four intermediates were observed for benzotriazole in both aerobic and anoxic activated sludge, which consisted of two isomers of hydroxy benzotriazole and two isomers of methoxy benzotriazole. Four intermediates were observed for trimethoprim under aerobic conditions, which formed 2,4-diaminopyrimidin-5-yl)(3,4,5-trimethoxyphenyl)methanol (TMP 306) and 2,6-diamino-5-hydroxy-5-(3,4,5-trimethoxybenzyl)-5,6-dihydropyrimidin-4(1H)-one (TMP 324) and two demethylation isomers of desmethyl trimethoprim. Triclosan had one confirmed transformation product, triclosan-o-sulfate, formed in both conditions. The identification of these transformation products will allow for more thorough risk assessments to be performed for the target TOrCs.

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Data Availability Statement

All data, models, and code generated or used during the study appear in the published article.

Acknowledgments

The Southern Nevada Water Authority (SNWA) acknowledges the Water Research Foundation (Project No. U2R13/4874) are funders of certain technical information upon which this publication is based. SNWA thanks the Water Research Foundation, for their financial, technical, and administrative assistance in funding the project through which this information was discovered. The authors would like to acknowledge support from the SNWA: Janie Zeigler-Holady and Brittney Hornbeck for their assistance with the analysis of TOrCs and David Rexing and Jennifer Fuel for administrative support.

References

Abegglen, C., A. Joss, C. S. McArdell, G. Fink, M. P. Schlüsener, T. A. Ternes, and H. Siegrist. 2009. “The fate of selected micropollutants in a single-house MBR.” Water Res. 43 (7): 2036–2046. https://doi.org/10.1016/j.watres.2009.02.005.
Behera, S. K., H. W. Kim, J. Oh, and H. Park. 2011. “Occurrence and removal of antibiotics, hormones and several other pharmaceuticals in wastewater treatment plants of the largest industrial city of Korea.” Sci. Total Environ. 409 (20): 4351–4360. https://doi.org/10.1016/j.scitotenv.2011.07.015.
Bletsou, A. A., J. Jeon, J. Hollender, E. Archontaki, and N. S. Thomaidis. 2015. “Targeted and non-targeted liquid chromatography-mass spectrometric workflows for identification of transformation products of emerging pollutants in the aquatic environment.” Trends Anal. Chem. 66 (Mar): 32–44. https://doi.org/10.1016/j.trac.2014.11.009.
Cancilla, D. A., A. Holtkamp, L. Matassa, and X. Fang. 1997. “Isolation and characterization of Microtox®-active components from aircraft de-icing/anti-icing fluids.” Environ. Toxcol. Chem. 16 (3): 430–434. https://doi.org/10.1002/etc.5620160306.
Capdevielle, M., R. Van Egmond, M. Versteeg Whelan, M. D. Hofmann-Kamensky, J. Inauen, V. Cunningham, and D. Woltering. 2008. “Consideration of exposure and species sensitivity of triclosan in the freshwater environment.” Integr. Environ. Assess. Manage. 4 (1): 15–23. https://doi.org/10.1897/IEAM_2007-022.1.
Chen, X., M. E. Casas, J. L. Nielsen, R. Wimmer, and K. Bester. 2015. “Identification of triclosan-o-sulfate and other transformation products of triclosan formed by activated sludge.” Sci. Total Environ. 505 (Feb): 39–46. https://doi.org/10.1016/j.scitotenv.2014.09.077.
Chen, X., J. L. Nielsen, K. Furgal, Y. Liu, I. B. Lolas, and K. Bester. 2011. “Biodegradation of triclosan and formation of methyl-triclosan in activated sludge under aerobic conditions.” Chemosphere 84 (4): 452–456. https://doi.org/10.1016/j.chemosphere.2011.03.042.
Dickenson, E., S. Snyder, D. Sedlak, and J. Drewes. 2011. “Indicator compounds for assessment of wastewater effluent contributions to flow and water quality.” Water Res. 45 (3): 1199–1212. https://doi.org/10.1016/j.watres.2010.11.012.
EAWAG-BBD (Eidgenössische Anstalt für Wasserversorgung, Abwasserreinigung und Gewässerschutz-Biocatalysis/Biodegradation Database). 2018. “Biocatalysis/biodegradation database.” Accessed May 1, 2018. http://eawag-bbd.ethz.ch.
Eggen, R. I. L., J. Hollender, A. Joss, M. Schärer, and C. Stamm. 2014. “Reducing the discharge of micropollutants in the aquatic environment: The benefits of upgrading wastewater treatment plants.” Environ. Sci. Technol. 48 (14): 7683–7689. https://doi.org/10.1021/es500907n.
Eichhorn, P., P. L. Ferguson, S. Pérez, and D. S. Aga. 2005. “Application of ion trap-MS with H/D exchange and QqTOF-MS in the identification of microbial degradates of trimethoprim in nitrifying activated sludge.” Anal. Chem. 77 (13): 4176–4184. https://doi.org/10.1021/ac050141p.
Fekadu, S., E. Alemayehu, R. Dewil, and B. Van der Bruggen. 2019. “Pharmaceuticals in freshwater aquatic environments: A comparison of the African and European challenge.” Sci. Total Environ. 654 (Mar): 324–337. https://doi.org/10.1016/j.scitotenv.2018.11.072.
Fernandez-Fontaina, E., I. Pinho, M. Carballa, F. Omil, and J. M. Lema. 2013. “Biodegradation kinetic constants and sorption coefficients of micropollutants in membrane bioreactors.” Biodegradation 24 (2): 165–177. https://doi.org/10.1007/s10532-012-9568-3.
Gauthier, H., V. Yargeau, and D. G. Cooper. 2010. “Biodegradation of pharmaceuticals by Rhodococcus rhodochrous and Aspergillus niger by co-metabolism.” Sci. Total Environ. 408 (7): 1701–1706. https://doi.org/10.1016/j.scitotenv.2009.12.012.
Ghattas, A. K., F. Fischer, A. Wick, and T. Ternes. 2017. “Anaerobic biodegradation of (emerging) organic contaminants in the aquatic environment.” Water Res. 116 (Jun): 268–295. https://doi.org/10.1016/j.watres.2017.02.001.
Harris, C. A., E. J. Routledge, C. Schaffner, J. V. Brian, W. Giger, and J. P. Sumpter. 2007. “Benzotriazole is antiestrogenic in vitro but not in vivo.” Environ. Toxcol. Chem. 26 (11): 2367–2372. https://doi.org/10.1897/06-587R.1.
Helbling, D. E., J. Hollender, H. P. Kohler, and K. S. Fenner. 2010a. “Structure-based interpretation of biotransformation pathways of amide-containing compounds in sludge-seeded bioreactors.” Environ. Sci. Technol. 44 (17): 6628–6635. https://doi.org/10.1021/es101035b.
Helbling, D. E., J. Hollender, H. P. Kohler, H. Singer, and K. Fenner. 2010b. “High-throughput identification of microbial transformation products of organic micropollutants.” Environ. Sci. Technol. 44 (17): 6621–6627. https://doi.org/10.1021/es100970m.
Huntscha, S., T. B. Hofstetter, E. L. Schymanski, S. Spah, and J. Hollender. 2014. “Biotransformation of benzotriazoles: Insights from transformation identification and compound-specific isotope analysis.” Environ. Sci. Technol. 48 (8): 4435–4443. https://doi.org/10.1021/es405694z.
Inyang, M., R. Flowers, D. McAvoy, and E. Dickenson. 2016. “Biotransformation of trace organic compounds by activated sludge from a biological nutrient removal treatment system.” Bioresour. Technol. 216 (Sep): 778–784. https://doi.org/10.1016/j.biortech.2016.05.124.
Jewell, K. S., S. Castronovo, A. Wick, P. Falas, A. Joss, and T. A. Ternes. 2016. “New insights into the transformation of trimethoprim during biological wastewater treatment.” Water Res. 88 (Jan): 550–557. https://doi.org/10.1016/j.watres.2015.10.026.
Kim, Y., K. Murugesan, S. Schmidt, V. Bokare, J. Jeon, E. Kim, and Y. Chang. 2011. “Triclosan susceptibility and co-metabolism: A comparison for three aerobic pollutant-degrading bacteria.” Bioresour. Technol. 102 (3): 2206–2212. https://doi.org/10.1016/j.biortech.2010.10.009.
Lakshminarasimman, N., O. Quinones, B. Vanderford, P. Moreno-Campo, E. Dickenson, and D. McAvoy. 2018. “Biotransformation and sorption of trace organic compounds in biological nutrient removal treatment systems.” Sci. Total Environ. 640–641 (Nov): 62–72. https://doi.org/10.1016/j.scitotenv.2018.05.145.
Larcher, S., and V. Yargeau. 2011. “Biodegradation of sulfamethoxazole by individual and mixed bacteria.” Appl. Microbiol. Biotechnol. 91 (1): 211–218. https://doi.org/10.1007/s00253-011-3257-8.
Lee, D. G., F. Zhao, Y. H. Rezenom, D. H. Russell, and K. Chu. 2012. “Biodegradation of triclosan by a wastewater microorganism.” Water Res. 46 (13): 4226–4234. https://doi.org/10.1016/j.watres.2012.05.025.
Li, Z., S. L. Kaserzon, M. M. Plassmann, A. Sobek, M. J. G. Ramos, and M. Radke. 2017. “A strategic screening approach to identify transformation products of organic micropollutants formed in natural waters.” Environ. Sci. Processes Impacts 19 (4): 488–498. https://doi.org/10.1039/C6EM00635C.
Liu, Y. S., G. G. Ying, A. Shareef, and R. S. Kookana. 2011. “Biodegradation of three selected benzotriazoles under aerobic and anaerobic conditions.” Water Res. 45 (16): 5005–5014. https://doi.org/10.1016/j.watres.2011.07.001.
Loos, R., et al. 2013. “EU-wide monitoring survey on emerging polar organic contaminants in wastewater treatment plant effluents.” Water Res. 47 (17): 6475–6487. https://doi.org/10.1016/j.watres.2013.08.024.
Mazioti, A. A., A. S. Stasinakis, G. Gatidou, N. S. Thomaidis, and H. R. Andersen. 2015. “Sorption and biodegradation of selected benzotriazoles and hydroxybenzotriazole in activated sludge and estimation of their fate during wastewater treatment.” Chemosphere 131 (July): 117–123. https://doi.org/10.1016/j.chemosphere.2015.03.029.
Müller, E., W. Schüssler, H. Horn, and H. Lemmer. 2013. “Aerobic biodegradation of the sulfonamide antibiotic sulfamethoxazole by activated sludge applied as co-substrate and sole carbon and nitrogen source.” Chemosphere 92 (8): 969–978. https://doi.org/10.1016/j.chemosphere.2013.02.070.
Parker, W. J., V. Pileggi, P. Seto, X. Chen, M. Ogunlaja, G. Van Der Kraak, and J. Parrott. 2014. “Impact of activated sludge configuration and operating conditions on in vitro and in vivo responses and trace organic compound removal.” Sci. Total Environ. 490 (Aug): 360–369. https://doi.org/10.1016/j.scitotenv.2014.05.023.
Phan, H. V., F. I. Hai, J. Kang, H. K. Dam, R. Zhang, W. E. Price, A. Broechmann, and L. D. Nghiem. 2014. “Simultaneous nitrification/denitrification and trace organic contaminant (TrOC) removal by an anoxic-aerobic membrane bioreactor.” Bioresour. Technol. 165 (Aug): 96–104. https://doi.org/10.1016/j.biortech.2014.03.094.
Plósz, B. G., H. Leknes, and K. V. Thomas. 2010. “Impacts of competitive inhibition, parent compound formation and partitioning behavior on the removal of antibiotics in municipal wastewater treatment.” Environ. Sci. Technol. 44 (2): 734–742. https://doi.org/10.1021/es902264w.
Radjenović, J., S. Pérez, M. Petrović, and D. Barceló. 2008. “Identification and structural characterization of biodegradation products of atenolol and glibenclamide by liquid chromatography coupled to hybrid quadrupole time-of-flight and quadrupole ion trap mass spectrometry.” J. Chromotogr. A 1210 (2): 142–153. https://doi.org/10.1016/j.chroma.2008.09.060.
Rauch-Williams, T., E. Dickenson, J. Drewes, S. Synder, T. Letzel, S. Bieber, C. Glover, G. Woods, S. Deslaurier, and S. Dagnino. 2018. A framework for assessing the costs and benefits of managing compounds of emerging concern in surface water. Alexandria, VA: Water Research Foundation, United Kingdom Water Industry Research.
Rivera-Cancel, G., D. Bocioaga, and A. G. Hay. 2007. “Bacterial degradation of N, N-diethyl-m-toluamide (DEET): Cloning and heterologous expression of DEET hydrolase.” Appl. Environ. Microbiol. 73 (9): 3105–3108. https://doi.org/10.1128/AEM.02765-06.
Rosal, R., A. Rodríguez, J. A. Perdigón-Melón, A. Petre, E. García-Calvo, M. J. Gómez, A. Agüera, and A. R. Fernández-Alba. 2010. “Occurrence of emerging pollutants in urban wastewater and their removal through biological treatment followed by ozonation.” Water Res. 44 (2): 578–588. https://doi.org/10.1016/j.watres.2009.07.004.
Salveson, A., T. Rauch-Williams, E. R. V. Dickenson, J. E. Drewes, D. Drury, D. C. McAvoy, and S. Snyder. 2012. Trace organic compound removal during wastewater treatment: Categorizing wastewater treatment processes by their efficacy in reduction of a suite of indicator TOrC. CEC4R08. Alexandria, VA: Water Environment Research Foundation.
Santos, J. L., I. Aparicio, and E. Alonso. 2007. “Occurrence and risk assessment of pharmaceutically active compounds in wastewater treatment plants. A case study: Seville city (Spain).” Environ. Int. 33 (4): 596–601. https://doi.org/10.1016/j.envint.2006.09.014.
Suarez, S., J. M. Lema, and F. Omil. 2010. “Removal of Pharmaceutical and Personal Care Products (PPCPs) under nitrifying and denitrifying conditions.” Water Res. 44 (10): 3214–3224. https://doi.org/10.1016/j.watres.2010.02.040.
Tatarazako, N., H. Ishibashi, K. Teshima, K. Kishi, and K. Arizono. 2004. “Effects of triclosan on various organisms.” Environ. Sci. 11 (2): 133–140.
Terechovs, A., A. Ansari, J. McDonald, S. Khan, F. Hai, N. Knott, J. Zhou, and L. Nghiem. 2019. “Occurrence and bioconcentration of micropollutants in Silver Perch (Bidyanus bidyanus) in a reclaimed water reservoir.” Sci. Total Environ. 650 (Feb): 585–593. https://doi.org/10.1016/j.scitotenv.2018.08.431.
Veldhoen, N., R. Skirrow, H. Osachoff, H. Wigmore, D. Clapson, P. Gunderson, G. Van Aggelen, and C. Helbing. 2006. “The bactericidal agent triclosan modulates thyroid hormone-associated gene expression and disrupts postembryonic anuran development.” Aquat. Toxicol. 80 (3): 217–227. https://doi.org/10.1016/j.aquatox.2006.08.010.
Wick, A., G. Fink, A. Joss, H. Siegrist, and T. A. Ternes. 2009. “Fate of beta blockers and psycho-active drugs in conventional wastewater treatment.” Water Res. 43 (4): 1060–1074. https://doi.org/10.1016/j.watres.2008.11.031.
Xue, W., C. Wu, K. Xiao, X. Huang, H. Zhou, H. Tsuno, and H. Tanaka. 2010. “Elimination and fate of selected micro-organic pollutants in a full-scale anaerobic/anoxic/aerobic process combined with membrane bioreactor for municipal wastewater reclamation.” Water Res. 44 (20): 5999–6010. https://doi.org/10.1016/j.watres.2010.07.052.
Yang, L., G. Ying, H. Su, J. Stauber, M. Adams, and M. Binet. 2008. “Growth inhibiting effects of 12 antibacterial agents and their mixtures on the freshwater microalga Pseudokirchneriella subcapitata.” Environ. Toxicol. Chem. 27 (5): 1201–1208. https://doi.org/10.1897/07-471.1.

Information & Authors

Information

Published In

Go to Journal of Environmental Engineering
Journal of Environmental Engineering
Volume 146Issue 9September 2020

History

Received: Jul 30, 2019
Accepted: Oct 22, 2019
Published online: Jun 18, 2020
Published in print: Sep 1, 2020
Discussion open until: Nov 18, 2020

Authors

Affiliations

Rebecca A. Trenholm [email protected]
Research Chemist, Water Quality Research and Development Div., Southern Nevada Water Authority, Henderson, NV 89015. Email: [email protected]
Brett J. Vanderford [email protected]
Principal Research Laboratory Scientist, Water Quality Research and Development Div., Southern Nevada Water Authority, Henderson, NV 89015. Email: [email protected]
Narasimman Lakshminarasimman [email protected]
Graduate Student, Dept. of Chemical and Environmental Engineering, Univ. of Cincinnati, Cincinnati, OH 45221. Email: [email protected]
Drew C. McAvoy, Ph.D., M.ASCE [email protected]
P.E.
Professor, Dept. of Chemical and Environmental Engineering, Univ. of Cincinnati, Cincinnati, OH 45221. Email: [email protected]
Research and Development Project Manager, Water Quality Research and Development Div., Southern Nevada Water Authority, Henderson, NV 89015. (corresponding author) ORCID: https://orcid.org/0000-0003-2341-4997. Email: [email protected]

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