Abstract
Widespread occurrence of various heterocyclic aromatic compounds is reported in concentrations from 1 to 20 μg/L in surface and groundwater as well as influents and effluents of wastewater treatment plants around the world. These so-called emerging contaminants and their metabolites can cause adverse effects on the environment and humans, even at very low concentration, hence raised environmental concerns. In this study, feasibility of soybean peroxidase-catalyzed removal of three selected heterocyclic aromatics from water was investigated, including sensitivity to the most important operational conditions, pH (range 3.6–9.0), H2O2 concentration (range 0.10–1.50 mM), and enzyme activity (range 0.001–5.0 U/mL). 3-Hydroxycoumarin and 2-aminobenzoxaozle were found to be substrates for the enzyme, having ≥95% and 45% removal efficiency with most effective pHs of 7.0 and 6.0, respectively. Time course study was also conducted to determine the initial first-order rate constants and half-lives; half-lives normalized for enzyme activity (0.0257 and 452 min for the respective substrates) are compared with those of 21 other compounds reactive with soybean peroxidase. High-resolution mass spectrometry was employed to characterize the plausible oligomerization products of enzymatic treatment, which revealed formation of dimers and trimers of the two substrates.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alavi SJ, Sadeghian H, Seyedi SM, Salimi A, Eshghi H (2018) A novel class of human 15-LOX-1 inhibitors based on 3-hydroxycoumarin. Chem Biol Drug Des 91:1125–1132. https://doi.org/10.1111/cbdd.13174
Almaqdi KA, Morsi R, Alhayuti B, Alharthi F, Ashraf SS (2019) LC-MSMS based screening of emerging pollutant degradation by different peroxidases. BMC Biotechnol 19:1–16. https://doi.org/10.1186/s12896-019-0574-y
Altahir BM, Feng W, Jasim HH, Taylor KE, Biswas N, Bewtra JK, Jassim SAA (2016) Soybean peroxidase-catalysed removal of benzidines from water. J Environ Eng Sci 10:73–80. https://doi.org/10.1680/jenes.15.00018
Asthana S, Zucca P, Vargiu AV, Sanjust E, Ruggerone P, Rescigno A (2015) Structure − activity relationship study of hydroxycoumarins and mushroom tyrosinase. J Agric Food Chem 63:236–7244. https://doi.org/10.1021/acs.jafc.5b02636
Brack W, Schirmer K (2003) Effect-directed identification of oxygen and sulfur heterocycles as major polycyclic aromatic cytochrome P4501A-inducers in a contaminated sediment. Environ SciTechnol 37:3062–3070. https://doi.org/10.1021/es020248j
Bundy JG, Morriss AWJ, Durham DG, Campbell CD, Paton GI (2001) Development of QSARs to investigate the bacterial toxicity and biotransformation potential of aromatic heterocylic compounds. Chemosphere 42:885–892
Caza N, Bewtra JK, Biswas N, Taylo KE (1999) Removal of phenolic compounds from synthetic wastewater using soybean peroxidase. Water Res 33:3012–3018
Chang K, Chen H, Wang T, Chen I, Chen Y, Yang S, Chen Y, Chang H, Huang C, Chang J, Shih C, Kuo C, Tzeng C (2015) Novel oxime-bearing coumarin derivatives act as potent Nrf2/ARE activators in vitro and in mouse model. Eur J Med Chem 106:60–74. https://doi.org/10.1016/j.ejmech.2015.10.029
Ćirić-Marjanović G, Milojević-Rakić M, Janošević-Ležaić A, Luginbühl S, Walde P (2017) Enzymatic oligomerization and polymerization of arylamines: state of the art and perspectives. Chem Pap 71:199–242. https://doi.org/10.1007/s11696-016-0094-3
Cordova Villegas LG, Mashhadi N, Chen M, Mukherjee D, Taylor KE, Biswas N (2016) A Short review of techniques for phenol removal from wastewater. Curr Pollut Rep 2:157–167. https://doi.org/10.1007/s40726-016-0035-3
Cordova Villegas LG, Mazloum S, Taylor KE, Biswas N (2018) Soybean peroxidase-catalyzed treatment of azo dyes with or without Fe° pretreatment. Water Environ Res 90:675–684. https://doi.org/10.2175/106143017X15131012153149
Cordova Villegas LG, Cordova Villegas AY, Taylor KE, Biswas N (2019) Response surface methodology for optimization of enzyme-catalyzed azo dye decolorization. J Environ Eng 145:04019013. https://doi.org/10.1061/(ASCE)EE.1943-7870.0001513
Feng W, Taylor KE, Biswas N, Bewtra JK (2013) Soybean peroxidase trapped in product precipitate during phenol polymerization retains activity and may be recycled. J Chem Technol Biotechnol 88:1429–1435. https://doi.org/10.1002/jctb.4075
Gomori G (1955) Preparation of buffers for use in enzyme studies. In: Colowick SP, Kaplan NO (eds) Methods in Enzymology 1. Academic Press, New York, pp 138–146
Hohmann C, Schneider BC, Irran E, Nicholson G, Bull AT, Jones AL, Brown R, Stach JEM, Goodfellow M, Winfried B, Krämer M, Imhoff JF, Süssmuth RD, Fiedler H (2009) Caboxamycin, a new antibiotic of the benzoxazole family produced by the deep-sea strain Streptomyces sp. NTK 937. J Antibiot 62:99–104. https://doi.org/10.1038/ja.2008.24
Jun L, Yon L, Mubarak NM, Bing CH, Pan S, Danquah MK, Abdullah EC, Khalid M (2019) An overview of immobilized enzyme technologies for dye and phenolic removal from wastewater. J Environ Chem Eng 7:102961. https://doi.org/10.1016/j.jece.2019.102961
Kamal JKA, Behere DV (2003) Activity, stability and conformational flexibility of seed coat soybean peroxidase. J Inorg Biochem 94:236–242. https://doi.org/10.1016/S0162-0134(03)00004-7
Kaur A, Taylor KE, Biswas N (2021) Soybean peroxidase-catalyzed degradation of a sulfonated dye and its azo-cleavage product. J Chem Technol Biotechnol 96(2):423–430. https://doi.org/10.1002/jctb.6555
Kim HY, Kim T, Cha SM, Yu S (2017) Degradation of sulfamethoxazole by ionizing radiation: Identification and characterization of radiolytic products. Chem Eng J 313:556–566. https://doi.org/10.1016/j.cej.2016.12.080
Martini J, Orge CA, Faria JL, Pereira MFR (2018) Sulfamethoxazole degradation by combination of advanced oxidation processes. J Environ Chem Eng 6:4054–4060. https://doi.org/10.1016/j.jece.2018.05.047
Maruthamuthu S, Stella C, Dileepan B, Ranjith R (2016) The chemistry and biological significance of imidazole, benzimidazole, benzoxazole, tetrazole and quinazolinone nucleus. J Chem Pharm Res 8:505–526
Mashhadi N, Taylor KE, Biswas N, Meister P, Gaul JW (2019) Oligomerization of 3-substituted quinolines by catalytic activity of soybean peroxidase as a wastewater treatment. Product formation and computational studies. Chem Eng J 364:340–348. https://doi.org/10.1016/j.cej.2019.01.184
Mashhadi N, Taylor, KE, Biswas N, Meister P, Gauld JW (2021) Biocatalytic oligomerization of azoles, experimental and computational studies. Submitted to Environ Sci Water Res Technol (revision 27 Jan., 2021)
Morsi R, Bilal M, Iqbal MN, Ashraf SS (2020) Laccases and peroxidases: the smart, greener and futuristic biocatalytic tools to mitigate recalcitrant emerging pollutants. Sci Total Environ 714:136572. https://doi.org/10.1016/j.scitotenv.2020.136572
Mousa Al-Ansari M, Taylor KE, Bewtra JK, Biswas N (2009) Soybean peroxidase-catalyzed removal of phenylenediamines and benzenediols from water. Enzym Microb Technol 45:253–260. https://doi.org/10.1016/j.enzmictec.2009.07.004
Mousa Al-Ansari M, Steevensz A, Taylor KE, Bewtra JK, Biswas N (2010) Soybean peroxidase-catalyzed removal of an aromatic thiol, 2-mercaptobenzothiazole, from water. Water Environ Res 82:2285–2289. https://doi.org/10.2175/106143010X12681059116617
Mukherjee D, Bhattacharya S, Taylor KE, Biswas N (2019) Enzymatic treatment for removal of hazardous aqueous arylamines, 4,4′-methylenedianiline and 4,4′-thiodianiline. Chemosphere 235:365–372. https://doi.org/10.1016/j.chemosphere.2019.06.182
Mukherjee D, Taylor KE, Biswas N (2018) Soybean peroxidase-induced treatment of dye-derived arylamines in water. Water Air Soil Pollut 8:229–283. https://doi.org/10.1007/s11270-018-3936-5
Mukherjee D, Taylor KE, Biswas N (2020) Soybean peroxidase-catalyzed oligomerization of arylamines in water: optimization, kinetics, products and cost. J Environ Chem Eng 8:103871. https://doi.org/10.1016/j.jec.2020.103871
Mulla SI, Hu A, Sun Q, Li J, Ashfaq M, Yu C (2018) Biodegradation of sulfamethoxazole in bacteria from three different origins. J Environ Manag 206:93–102. https://doi.org/10.1016/j.jenvman.2017.10.029
Noguera-Oviedo K, Aga DS (2016) Lessons learned from more than two decades of research on emerging contaminants in the environment. J Hazard Mater 316:242–251. https://doi.org/10.1016/j.jhazmat.2016.04.058
Nowak PM, Wozniakiewicz M, Piwowarska M, Koscielniak P (2016) Determination of acid dissociation constant of 20 coumarin derivatives by capillary electrophoresis using the amine capillary and two different methodologies. J Chromatogr 1446:149–157. https://doi.org/10.1016/j.chroma.2016.03.084
Pandey VP, Awasthi M, Singh S, Tiwari S, Dwivedi UN (2017) A comprehensive review on function and application of plant peroxidases. Biochem Anal Biochem 6:1–16. https://doi.org/10.4172/2161-1009.1000308
Patapas J, Mousa Al-Ansari M, Taylor KE, Bewtra JK, Biswas N (2007) Removal of dinitrotoluenes from water via reduction with iron and peroxidase-catalyzed oxidative polymerization: a comparison between Arthromyces ramosus peroxidase and soybean peroxidase. Chemosphere 67:1485–1491. https://doi.org/10.1016/j.chemosphere.2006.12.040
Richardson SD, Kimura SY (2017) Emerging environmental contaminants: challenges facing our next generation and potential engineering solutions. Environ Technol Innov 8:40–56. https://doi.org/10.1016/j.eti.2017.04.002
Rivera-Utrilla J, Sánchez-Polo M, Ferro-García MÁ, Prados-Joya G, Ocampo-Pérez R (2013) Pharmaceuticals as emerging contaminants and their removal from water. A review. Chemosphere 93:1268–1287. https://doi.org/10.1016/j.chemosphere.2013.07.059
Singh S, Veeraswamy G, Bhattarai D, Goo J, Lee K (2015) Recent advances in the development of pharmacologically active compounds that contain a benzoxazole scaffold. Asian J Org Chem 4:1338–1361. https://doi.org/10.1002/ajoc.201500235
Slachtova V, Brulıková L (2018) Benzoxazole derivatives as promising antitubercular agents. ChemistrySelect 3:4653–4662. https://doi.org/10.1002/slct.201800631
Souza BM, Marinho BA, Moreira FC, Dezotti MWC, Boaventura RAR, Vilar VJP (2017) Photo-Fenton oxidation of 3-amino-5-methylisoxazole: a by-product from biological breakdown of some pharmaceutical compounds. Environ Sci Pollut Res 24:6195–6204. https://doi.org/10.1007/s11356-015-5690-1
Steevensz A, Madur S, Feng W, Taylor KE, Bewtra JK, Biswas N (2014) Crude soybean hull peroxidase treatment of phenol in synthetic and real wastewater: enzyme economy enhanced by Triton X-100. Enzym Microb Technol 55:65–71. https://doi.org/10.1016/j.enzmictec.2013.12.005
Urrea DAM, Haure PM, Einschlag FSG, Contreras EM (2018) Horseradish peroxidase-mediated decolourization of Orange II: modelling hydrogen peroxide utilization efficiency at different pH values. Environ Sci Pollut Res 25:19989–20002. https://doi.org/10.1007/s11356-018-2134-8
Valderrama B, Ayala M, Vazquez-Duhalt R (2002) Suicide inactivation of peroxidases and the challenge of engineering more robust enzymes. Chem Biol 9:555–565. https://doi.org/10.1016/s1074-5521(02)00149-7
Vitaku E, Smith DT, Njardarson JT (2014) Analysis of the structural diversity, substitution patterns, and frequency of nitrogen heterocycles among U.S. FDA approved pharmaceuticals. J Med Chem 57:10257–10274. https://doi.org/10.1021/jm501100b
Wang Q, Wang Y, Kurosu M (2012) A new oxyma derivative for non-racemizable amide-forming reactions in water. Org Lett 14:3372–3375. https://doi.org/10.1021/ol3013556
Wang L, Liu Y, Ma J, Zhao F (2016) Rapid degradation of sulphamethoxazole and the further transformation of 3-amino-5-methylisoxazole in a microbial fuel cell. Water Res 88:322–328. https://doi.org/10.1016/j.watres.2015.10.030
Zhang X (2019) Enzymatic treatment of selected pesticides in aqueous system. MASc thesis, University of Windsor.
Acknowledgements
The authors would like to thank the Natural Sciences and Engineering Research Council (NSERC) of Canada and the University of Windsor Master’s Entrance Scholarship for their financial support.
Availability of data and materials
All data generated or analyzed during this study are included in this published article and its supplementary information files.
Funding
Natural Sciences and Engineering Research Council of Canada, DG 2019-04426; University of Windsor.
Author information
Authors and Affiliations
Contributions
NZB designed and conducted experiments, collected and analyzed data, and prepared the manuscript; NM assisted with experiment design and data analysis; KET and NB assisted with experiment design, critiqued the manuscript and assisted with its revision and editing, and provided operating funding through a granting agency as noted above. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Ta Yeong Wu
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 32 kb)
Rights and permissions
About this article
Cite this article
Bideh, N.Z., Mashhadi, N., Taylor, K.E. et al. Elimination of selected heterocyclic aromatic emerging contaminants from water using soybean peroxidase. Environ Sci Pollut Res 28, 37570–37579 (2021). https://doi.org/10.1007/s11356-021-13403-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-13403-w