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Plasticizer phthalate esters degradation with a laccase from Trametes versicolor: effects of TEMPO used as a mediator and estrogenic activity removal

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Abstract

Phthalate esters (PAEs) are toxic and persistent chemicals that are ubiquitous in the environment and have attracted worldwide attention due to their threats to the environment and human health. Dimethyl phthalate (DMP) is a relatively simple structure and one of the most observed PAEs in the environment. This study investigated the degradation of the DMP using Trametes versicolor laccase and its laccase-mediator systems. The degradation effect of laccase alone on DMP was poor, while the laccase-mediator systems can effectively enhance the degradation efficiency. Within 24 h, 45% of DMP (25 mg/L) was degraded in the presence of 0.8 U/mL laccase and 0.053 mM 2, 2, 6, 6-tetramethylpiperidine-1-oxyl (TEMPO). A certain concentration (1 mM) of metal ions Al3+, Cu2+ or Ca2+ can positively promote DMP degradation with the laccase-TEMPO system. Moreover, the structure of PAEs also had a great influence on the degradation efficiency. Higher degradation efficiencies were observed when incubating PAEs with short alkyl side chains by the laccase-TEMPO system compared to that with long alkyl side chains. Additionally, the branched-chain PAEs had a better degradation effect than the straight-chain. The estrogenic activity of the DMP solution after reaction was much smaller than that of the original solution. Finally, transformation products ortho-hydroxylated DMP and phthalic acid were identified by GC–MS and the possible degradation pathway was proposed. This study verifies the feasibility of the laccase-TEMPO system to degrade PAEs and provides a reference for exploring more potential value of laccase.

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References

  • Abdoul Magid ASI, Islam MS, Chen Y, Weng L, Sun Y, Chang X (2021) Competitive adsorption of Dibutyl phthalate (DBP) and Di (2-ethylhexyl) phthalate (DEHP) onto fresh and oxidized corncob biochar. Chemosphere 280:130639–130639

    Article  CAS  PubMed  Google Scholar 

  • Barrios-Estrada C, de Jesus R-A, Munoz-Gutierrez BD, Iqbal HMN, Kannan S, Parra-Saldivar R (2018) Emergent contaminants: endocrine disruptors and their laccase-assisted degradation–A review. Sci Total Environ 612:1516–1531

    Article  CAS  PubMed  Google Scholar 

  • Bilal M, Rasheed T, Nabeel F, Iqbal HMN, Zhao Y (2019) Hazardous contaminants in the environment and their laccase-assisted degradation–a review. J Environ Manage 234:253–264

    Article  CAS  PubMed  Google Scholar 

  • Bonomo RP, Cennamo G, Purrello R, Santoro AM, Zappala R (2001) Comparison of three fungal laccases from Rigidoporus lignosus and Pleurotus ostreatus: correlation between conformation changes and catalytic activity. J Inorg Biochem 83(1):67–75

    Article  CAS  PubMed  Google Scholar 

  • Cajthaml T (2015) Biodegradation of endocrine-disrupting compounds by ligninolytic fungi: mechanisms invovled in the degradation. Environ Microbiol 17(12):4822–4834

    Article  CAS  PubMed  Google Scholar 

  • Cajthaml T, Kresinova Z, Svobodova K, Moeder M (2009) Biodegradation of endocrine-disrupting compounds and suppression of estrogenic activity by ligninolytic fungi. Chemosphere 75(6):745–750

    Article  CAS  PubMed  Google Scholar 

  • Camarero S, Ibarra D, Martinez AT, Romero J, Gutierrez A, del Rio JC (2007) Paper pulp delignification using laccase and natural mediators. Enzyme Microb Technol 40(5):1264–1271

    Article  CAS  Google Scholar 

  • Couto SR, Sanroman M, Gubitz GM (2005) Influence of redox mediators and metal ions on synthetic acid dye decolourization by crude laccase from Trametes hirsuta. Chemosphere 58(4):417–422

    Article  Google Scholar 

  • Deblonde T, Cossu-Leguille C, Hartemann P (2011) Emerging pollutants in wastewater: a review of the literature. Int J Hyg Environ Health 214(6):442–448

    Article  CAS  PubMed  Google Scholar 

  • Dodor DE, Hwang HM, Ekunwe SIN (2004) Oxidation of anthracene and benzo a pyrene by immobilized laccase from Trametes versicolor. Enzyme Microb Technol 35(2–3):210–217

    Article  CAS  Google Scholar 

  • Farounbi AI, Ngqwala NP (2020) Occurrence of selected endocrine disrupting compounds in the eastern cape province of South Africa. Environ Sci Pollut Res 27(14):17268–17279

    Article  CAS  Google Scholar 

  • Feng NX, Feng YX, Liang QF, Chen X, Xiang L, Zhao HM (2021) Complete biodegradation of di-n-butyl phthalate (DBP) by a novel Pseudomonas sp. YJB6. Sci Total Environ 761:143208

    Article  CAS  PubMed  Google Scholar 

  • Gao DW, Wen ZD (2016) Phthalate esters in the environment: a critical review of their occurrence, biodegradation, and removal during wastewater treatment processes. Sci Total Environ 541:986–1001

    Article  CAS  PubMed  Google Scholar 

  • Grelska A, Noszczynska M (2020) White rot fungi can be a promising tool for removal of bisphenol A, bisphenol S, and nonylphenol from wastewater. Environ Sci Pollut Res 27(32):39958–39976

    Article  CAS  Google Scholar 

  • He W, Qin N, Kong XZ, Liu WX, He QS, Ouyang HL (2013) Spatio-temporal distributions and the ecological and health risks of phthalate esters (PAEs) in the surface water of a large, shallow Chinese lake. Sci Total Environ 461:672–680

    Article  PubMed  Google Scholar 

  • Huang S, Qi Z, Ma S, Li G, Long C, Yu Y (2021) A critical review on human internal exposure of phthalate metabolites and the associated health risks. Environ Pollut 279:116941

    Article  CAS  PubMed  Google Scholar 

  • Jia JB, Zhang SP, Wang P, Wang HJ (2012) Degradation of high concentration 2,4-dichlorophenol by simultaneous photocatalytic-enzymatic process using TiO2/UV and laccase. J Hazard Mater 205:150–155

    Article  PubMed  Google Scholar 

  • Koschorreck K, Richter SM, Swierczek A, Beifuss U, Schmid RD, Urlacher VB (2008) Comparative characterization of four laccases from Trametes versicolor concerning phenolic C-C coupling and oxidation of PAHs. Arch Biochem Biophys 474(1):213–219

    Article  CAS  PubMed  Google Scholar 

  • Le TM, Nguyen HMN, Nguyen VK, Nguyen AV, Vu ND, Yen NTH (2021) Profiles of phthalic acid esters (PAEs) in bottled water, tap water, lake water, and wastewater samples collected from Hanoi. Vietnam Sci Total Environ 788:147831–147831

    Article  CAS  PubMed  Google Scholar 

  • Lee SM, Koo BW, Lee SS, Kim MK, Choi DH, Hong EJ (2004) Biodegradation of dibutylphthalate by white rot fungi and evaluation on its estrogenic activity. Enzyme Microb Technol 35(5):417–423

    Article  CAS  Google Scholar 

  • Leme Ike PT, Birolli WG, dos Santos DM, Meleiro Porto AL, Ferreira Souza DH (2019) Biodegradation of anthracene and different PAHs by a yellow laccase from Leucoagaricus gongylophorus. Environ Sci Pollut Res 26(9):8675–8684

    Article  Google Scholar 

  • Lin J, Liu YJ, Chen S, Le XY, Zhou XH, Zhao ZY (2016) Reversible immobilization of laccase onto metal-ion-chelated magnetic microspheres for bisphenol A removal. Int J Biol Macromol 84:189–199

    Article  CAS  PubMed  Google Scholar 

  • Majcherczyk A, Johannes C, Huttermann A (1998) Oxidation of polycyclic aromatic hydrocarbons (PAH) by laccase of Trametes versicolor. Enzyme Microb Technol 22(5):335–341

    Article  CAS  Google Scholar 

  • Margot J, Maillard J, Rossi L, Barry DA, Holliger C (2013) Influence of treatment conditions on the oxidation of micropollutants by Trametes versicolor laccase. New Biotechnol 30(6):803–813

    Article  CAS  Google Scholar 

  • Mashhadi N, Taylor KE, Jimenez N, Varghese ST, Levi Y, Lonergan C (2019) Removal of selected pharmaceuticals and personal care products from wastewater using soybean peroxidase. Environ Manage 63(3):408–415

    Article  PubMed  Google Scholar 

  • Naghdi M, Taheran M, Brar SK, Kermanshahi-pour A, Verma M, Surampalli RY (2018) Removal of pharmaceutical compounds in water and wastewater using fungal oxidoreductase enzymes. Environ Pollut 234:190–213

    Article  CAS  PubMed  Google Scholar 

  • Net S, Sempere R, Delmont A, Paluselli A, Ouddane B (2015) Occurrence, fate, behavior and ecotoxicological state of phthalates in different environmental matrices. Environ Sci Technol 49(7):4019–4035

    Article  CAS  PubMed  Google Scholar 

  • Ngoc Han T, Hu J, Urase T (2013) Removal of the insect repellent N, N-diethyl-m-toluamide (DEET) by laccase-mediated systems. Bioresour Technol 147:667–671

    Article  Google Scholar 

  • Nguyen LN, Hai FI, Price WE, Leusch FDL, Roddick F, McAdam EJ (2014) Continuous biotransformation of bisphenol A and diclofenac by laccase in an enzymatic membrane reactor. Int Biodeterior Biodegrad 95:25–32

    Article  CAS  Google Scholar 

  • Pang X, Skillen N, Gunaratne N, Rooney DW, Robertson PKJ (2021) Removal of phthalates from aqueous solution by semiconductor photocatalysis: a review. J Hazard Mater 402:123461

    Article  CAS  PubMed  Google Scholar 

  • Pinto PA, Fraga I, Bezerra RMF, Dias AA (2020) Phenolic and non-phenolic substrates oxidation by laccase at variable oxygen concentrations: Selection of bisubstrate kinetic models from polarographic data. Biochem Eng J 153:107423

    Article  CAS  Google Scholar 

  • Prasad B, Prasad KS, Dave H, Das A, Asodariya G, Talati N (2022) Cumulative human exposure and environmental occurrence of phthalate esters: a global perspective. Environ Res 210:112987

    Article  CAS  PubMed  Google Scholar 

  • Ren L, Jia Y, Ruth N, Qiao C, Wang JH, Zhao BS (2016) Biodegradation of phthalic acid esters by a newly isolated Mycobacterium sp YC-RL4 and the bioprocess with environmental samples. Environ Sci Pollut Res 23(16):16609–16619

    Article  CAS  Google Scholar 

  • Ren L, Wang G, Huang Y, Guo J, Li C, Jia Y (2021) Phthalic acid esters degradation by a novel marine bacterial strain Mycolicibacterium phocaicum RL-HY01: characterization, metabolic pathway and bioaugmentation. Sci Total Environ 791:148303–148303

    Article  CAS  PubMed  Google Scholar 

  • Shariati S, Pourbabaee AA, Alikhani HA, Rezaei KA (2021) Biodegradation of DEHP by a new native consortium An6 (Gordonia sp and Pseudomonas sp) adapted with phthalates, isolated from a natural strongly polluted wetland. Environ Technol Inno 24:101936

    Article  CAS  Google Scholar 

  • Spina F, Cordero C, Schiliro T, Sgorbini B, Pignata C, Gilli G (2015) Removal of micropollutants by fungal laccases in model solution and municipal wastewater: evaluation of estrogenic activity and ecotoxicity. J Clean Prod 100:185–194

    Article  CAS  Google Scholar 

  • Torres E, Bustos-Jaimes I, Le Borgne S (2003) Potential use of oxidative enzymes for the detoxification of organic pollutants. Appl Catal B-Environ 46(1):1–15

    Article  CAS  Google Scholar 

  • Tran NH, Hu JY, Urase T (2013) Removal of the insect repellent N, N-diethyl-m-toluamide (DEET) by laccase-mediated systems. Bioresour Technol 147:667–671

  • Wang D, Lou J, Xu J, Yuan J, Wang Q, Wang P (2021a) Degradation of octylphenol polyethoxylates with a long ethoxylate chain using the laccase-mediated systems. Environ Sci Pollut Res 28(28):37781

    Article  CAS  Google Scholar 

  • Wang D, Lou J, Yuan J, Xu J, Zhu R, Wang Q (2021b) Laccase immobilization on core-shell magnetic metal-organic framework microspheres for alkylphenol ethoxylate compound removal. J Environ Chem Eng 9(1):105000

    Article  CAS  Google Scholar 

  • Zeng S, Qin X, Xia L (2017) Degradation of the herbicide isoproturon by laccase-mediator systems. Biochem Eng J 119:92–100

    Article  CAS  Google Scholar 

  • Zhang X, Feng M, Qu R, Liu H, Wang L, Wang Z (2016) Catalytic degradation of diethyl phthalate in aqueous solution by persulfate activated with nano-scaled magnetic CuFe2O4/MWCNTs. Chem Eng J 301:1–11

    Article  Google Scholar 

  • Zhang L, Cheng H, Pan D, Wu Y, Ji R, Li W (2021a) One-pot pyrolysis of a typical invasive plant into nitrogen-doped biochars for efficient sorption of phthalate esters from aqueous solution. Chemosphere 280:130712–130712

    Article  CAS  PubMed  Google Scholar 

  • Zhang QQ, Ma ZR, Cai YY, Li HR, Ying GG (2021b) Agricultural plastic pollution in China: Generation of plastic debris and emission of phthalic acid esters from agricultural films. Environ Sci Technol 55(18):12459–12470

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Jiao Y, Li Z, Tao Y, Yang Y (2021c) Hazards of phthalates (PAEs) exposure: a review of aquatic animal toxicology studies. Sci Total Environ 771:145418

    Article  CAS  PubMed  Google Scholar 

  • Zhao HM, Du H, Feng NX, Xiang L, Li YW, Li H (2016) Biodegradation of di-n-butylphthalate and phthalic acid by a novel Providencia sp 2D and its stimulation in a compost-amended soil. Biol Fertility Soils 52(1):65–76

    Article  CAS  Google Scholar 

  • Zhu R, Wang D, Xie J, Liu Y, Liu M, Fu S (2022) Salt-resistant Schiff base cross-linked superelastic photothermal cellulose aerogels for long-term seawater desalination. Chem Eng J 427:131618

    Article  CAS  Google Scholar 

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Acknowledgements

This work was financially supported by the Postgraduate Research & Practice Innovation Program of Jiangsu Province (KYCX21_2016).

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Postgraduate Research and Practice Innovation Program of Jiangsu Province, KYCX21_2016

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Authors and Affiliations

  1. Key Laboratory of Science and Technology of Eco-Textile, Ministry of Education, Jiangnan University, Wuxi, 214122, Jiangsu, China

    Dan Wang, Ruofei Zhu, Jiangfei Lou, Nawon Baek & Xuerong Fan

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  1. Dan Wang
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Contributions

Author contributions: Dan Wang: Conceptualization, Methodology, Investigation, Analysis, Writing-Original Draft. Ruofei Zhu: Review & Editing, Formal analysis, Methodology, Supervision. Jiangfei Lou: Supervision, Resources, investigation. Nawon Baek: Investigation, Methodology, Formal analysis. Xuerong Fan: Conceptualization, Supervision, Project administration, Review & Editing.

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Correspondence to Xuerong Fan.

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Wang, D., Zhu, R., Lou, J. et al. Plasticizer phthalate esters degradation with a laccase from Trametes versicolor: effects of TEMPO used as a mediator and estrogenic activity removal. Biodegradation 34, 431–444 (2023). https://doi.org/10.1007/s10532-023-10030-9

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  • DOI: https://doi.org/10.1007/s10532-023-10030-9

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