Skip to main content
Log in

Oxidation of polycyclic aromatic hydrocarbons by horseradish peroxidase in water containing an organic cosolvent

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Polycyclic aromatic hydrocarbons (PAHs) are environmental contaminants that are toxic, mutagenic, and carcinogenic. We investigated the horseradish peroxidase (HRP)-catalyzed oxidation of PAHs in water containing N,N-dimethylformamide. Four PAHs (anthracene, phenanthrene, pyrene, and fluoranthene) were investigated using single-PAH and mixed-PAH systems. The results provide useful information regarding the preferential oxidation of anthracene over other PAHs regardless of the reaction time, enzyme dosage, and hydrogen peroxide concentration. The removal of PAHs was found to be very strongly correlated with the ionization potential (IP), and much greater PAH oxidation was observed at a lower IP. The oxidation of anthracene was specifically pH- and temperature-dependent, with the optimal pH and temperature being 8.0 and 40 °C, respectively. The redox mediators 1-hydroxybenzotriazole and veratryl alcohol promoted the transformation of anthracene by HRP; 9,10-anthraquinone was the main product detected from the anthracene oxidation system. The results of this study not only provide a better understanding of the oxidation of PAHs by utilizing a plant biocatalyst, but also provide a theoretical basis for establishing the HRP-catalyzed treatment of PAH-contaminated wastewater.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

HOBT:

1-hydroxybenzotriazole

ABTS:

2, 2’-azinobis(3-ethylbenzthiazoline-6-sulfonic acid)

GC-MS:

gas chromatography/mass spectrometry

HPLC:

high-performance liquid chromatography

HRP:

horseradish peroxidase

H2O2 :

hydrogen peroxide

LiP:

lignin peroxidase

MnP:

manganese peroxidase

DMF:

N,N-dimethylformamide

PAHs:

polycyclic aromatic hydrocarbons

SPE:

solid phase extraction

IP:

ionization potential

References

  • Anyakora C, Ogbeche A, Palmer P, Coker H (2005) Determination of polynuclear aromatic hydrocarbons in marine samples of Siokolo Fishing Settlement. J Chromatogr A1073:323–330

    Article  Google Scholar 

  • ATSDR (1995) Toxicological profile for polycyclic aromatic hydrocarbons, US Department of Health and Human Services, Public Health Service, Agency for Toxic Substances and Disease Registry, Atlanta, GA

  • Berglund GI, Carlsson GH, Smith AT, Szoke H, Henriksen A, Hajdu J (2002) The catalytic pathway of horseradish peroxidase at high resolution. Nature 417:463–468

    Article  CAS  Google Scholar 

  • Bhunia A, Durani S, Wangikar PP (2001) Horseradish peroxidase catalyzed degradation of industrially important dyes. Biotechnol Bioeng 72:562–567

    Article  CAS  Google Scholar 

  • Bogan BW, Lamar RT (1995) One-electron oxidation in the degradation of creosote polycyclic aromatic hydrocarbons by Phanerochaete chrysosporium. Appl Environ Microbiol 61:2631–2635

    CAS  Google Scholar 

  • Bourbonnais R, Paice MG (1990) Oxidation of non-phenolic substrates: an expanded role for laccase in lignin biodegradation. FEBS Lett 267:99–102

    Article  CAS  Google Scholar 

  • Canas AI, Alcalde M, Plou F, Martinez MJ, Martinez AT, Camarero S (2007) Transformation of polycyclic aromatic hydrocarbons by laccase is strongly enhanced by phenolic compounds present in soil. Environ Sci Technol 41:2964–2971

    Article  CAS  Google Scholar 

  • Cavalieri EL, Rogan EG, Roth RW, Saugier RK, Hakam A (1983) The relationship between ionization potential and horseradish peroxidase/hydrogen peroxide-catalyzed binding of aromatic hydrocarbons to DNA. Chem Biol Interact 47:87–109

    Article  CAS  Google Scholar 

  • Chen B, Xuan X, Zhu L, Wang J, Gao Y, Yang K (2004) Distributions of polycyclic aromatic hydrocarbons in surface waters, sediments and soils of Hangzhou City, China. Water Res 38:3558–3568

    Article  CAS  Google Scholar 

  • Chroma L, Mackova M, Kucerova P, Wiesche CI, Burkhard C, Macek T (2002) Enzymes in plant metabolism of PCBs and PAHs. Acta Biotechnol 22:35–41

    Article  CAS  Google Scholar 

  • Devanesan P, Rogan E, Cavalieri E (1987) The relationship between ionization potential and prostaglandin Hsynthase-catalyzed binding of aromatic hydrocarbons to DNA. Chem Biol Interact 61:89–95

    Article  CAS  Google Scholar 

  • Duran N, Bromberg N, Kunz A (2001) Kinetic studies on veratryl alcohol transformation by horseradish peroxidase. J Inorg Biochem 84:279–286

    Article  CAS  Google Scholar 

  • Eibes G, Lu-Chau T, Feijoo G, Moreira MT, Lema JM (2005) Complete degradation of anthracene by manganese peroxidase in organic solvent mixtures. Enzym Microb Technol 37:365–372

    Article  CAS  Google Scholar 

  • Eibes G, Cajthaml T, Moreira MT, Feijoo G, Lema JM (2006) Enzymatic degradation of anthracene, dibenzothiophene and pyrene by manganese peroxidase in media containing acetone. Chemosphere 64:408–414

    Article  CAS  Google Scholar 

  • Eibes G, Moreira MT, Feijoo G, Daugulis AJ, Lema JM (2007) Operation of a two-phase partitioning bioreactor for the oxidation of anthracene by the enzyme manganese peroxidase. Chemosphere 66:1744–1751

    Article  CAS  Google Scholar 

  • Fang J, Barcelona MJ (2003) Coupled oxidation of aromatic hydrocarbons by horseradish peroxidase and hydrogen peroxide. Chemosphere 50:105–109

    Article  CAS  Google Scholar 

  • Gao Y, Xiong W, Ling W, Wang X, Li Q (2007) Impact of exotic and inherent dissolved organic matter on phenanthrene sorption by soils. J Hazard Mater 140:138–144

    Article  CAS  Google Scholar 

  • Gao Y, Xiong W, Ling W, Wang H, Ren L, Yang Y (2008) Partitioning of polycyclic aromatic hydrocarbons between plant roots and water. Plant Soil 311:201–209

    Article  CAS  Google Scholar 

  • Gao Y, Ren L, Ling W, Gong S, Sun B, Zhang Y (2010) Desorption of phenanthrene and pyrene in soils by root exudates. Bioresour Technol 101:1159–1165

    Article  CAS  Google Scholar 

  • Grosjean N, Descorme C, Besson M (2010) Catalytic wet air oxidation of N, N-dimethylformamide aqueous solutions: deactivation of TiO2 and ZrO2-supported noble metal catalysts. Appl Catal B Environ 97:276–283

    Article  CAS  Google Scholar 

  • Gunther T, Sack U, Hofrichter M, Latz M (1998) Oxidation of PAH and PAH-derivatives by fungal and plant oxidoreductases. J Basic Microbiol 38:113–122

    Article  Google Scholar 

  • Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15

    Article  CAS  Google Scholar 

  • Huang Q, Weber WJ Jr (2004) Peroxidase-catalyzed coupling of phenol in the presence of model inorganic and organic solid phases. Environ Sci Technol 38:5238–5245

    Article  CAS  Google Scholar 

  • Husain M, Husain Q (2008) Applications of redox mediators in the treatment of organic pollutants by using oxidoreductive enzymes: a review. Crit Rev Environ Sci Technol 38:1–42

    Article  CAS  Google Scholar 

  • Kang F, Chen D, Gao Y, Zhang Y (2010a) Distribution of polycyclic aromatic hydrocarbons in subcellular root tissues of ryegrass (Lolium multiflorum Lam.). BMC Plant Biol 10:210

    Article  Google Scholar 

  • Kang F, Gao Y, Wang Q (2010b) Inhibition of free DNA degradation by the deformation of DNA exposed to trace polycyclic aromatic hydrocarbon contaminants. Environ Sci Technol 44:8891–8896

    Article  CAS  Google Scholar 

  • Karim Z, Husain Q (2010) Removal of anthracene from model wastewater by immobilized peroxidase from Momordica charantia in batch process as well as in a continuous spiral-bed reactor. J Mol Catal B Enzym 66:302–310

    Article  CAS  Google Scholar 

  • Kraus JJ, Munir IZ, McEldoon JP, Clark DS, Dordick JS (1999) Oxidation of polycyclic aromatic hydrocarbons catalyzed by soybean peroxidase. Appl Biochem Biotechnol 80:221–230

    Article  CAS  Google Scholar 

  • Krupadam RJ, Khan MS, Wate SR (2010) Removal of probable human carcinogenic polycyclic aromatic hydrocarbons from contaminated water using molecularly imprinted polymer. Water Res 44(3):681–688

    Article  CAS  Google Scholar 

  • Kvesitadze E, Sadunishvili T, Kvesitadze G (2009) Mechanisms of organic contaminants uptake and degradation in plants. World Acad Sci Eng Technol 55:458–468

    Google Scholar 

  • Liu JZ, Song HY, Weng LP, Ji LN (2002) Increased thermostability and phenol removal efficiency by chemical modified horseradish peroxidase. J Mol Catal B Enzym 18:225–232

    Article  CAS  Google Scholar 

  • Malomo SOA, Lateef Babatunde RI, Saheed IA, Iniaghe MO, Olorunniji FJ (2011) Suicide inactivation of horseradish peroxidase by excess hydrogen peroxide: the effects of reaction pH, buffer ion concentration, and redox mediation. Biokemistri 23:124–128

    Google Scholar 

  • Mao L, Lu J, Habteselassie M, Luo Q, Gao S, Cabrera M (2010) Ligninase-mediated removal of natural and synthetic estrogens from water: II. Reactions of 17β-estradiol. Environ Sci Technol 44:2599–2604

    Article  CAS  Google Scholar 

  • Matto M, Husain Q (2007)Decolorization of direct dyes by salt fractionated turnip proteins enhanced in the presence of hydrogen peroxide and redox mediators. Chemosphere 69:338–345

  • Nicell JA, Bewtra JK, Biswas N, Stpierre CC, Taylor KE (1993) Enzyme-catalyzed polymerization and precipitation of aromatic-compounds from aqueous-solution. Can J Civ Eng 20:725–735

    Article  Google Scholar 

  • Pradeep N, Anupama, U.S. Hampannavar (2012) Polymerization of phenol using free and immobilized horseradish peroxidase. Environ Earth Sci 2:31

    Google Scholar 

  • Saby Johna K, Bhatb SG, Prasada Raob UJS (2011) Isolation and partial characterization of phenol oxidases from Mangifera indica L.sap (latex). J Mol Catal B Enzym 68:30–36

    Article  Google Scholar 

  • Satar R, Husain Q (2009) Use of bitter gourd (Momordica charantia) peroxidase together with redox mediators to decolorize disperse dyes. Biotechnol Bioproc Eng 14:213–219

    Article  CAS  Google Scholar 

  • Song HY, Liu JZ, Xiong YH, Weng LP, Ji LN (2003) Treatment of aqueous chlorophenol by phthalic anhydride-modified horseradish peroxidase. J Mol Catal B Enzym 22:37–44

    Article  CAS  Google Scholar 

  • Srogi K (2007) Monitoring of environmental exposure to polycyclic aromatic hydrocarbons: a review. Environ Chem Lett 5:169–195

    Article  CAS  Google Scholar 

  • Steffen KT, Hatakka A, Hofrichter M (2002) Removal and mineralization of polycyclic aromatic hydrocarbons by litter-decomposing basidiomycetous fungi. Appl Microbiol Biotechnol 60:212–217

    Article  CAS  Google Scholar 

  • Temoç Z, Yigitoglu M (2009) Studies on the activity and stability of immobilized horseradish peroxidase on poly(ethylene terephthalate) grafted acrylamide fiber. Bioprocess Biosyst Eng 32:467–474

    Article  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 46:1–15

    Article  CAS  Google Scholar 

  • Ulson de Souza SMAG, Forgiarini E, Ulson de Souza AA (2007) Toxicity of textile dyes and their degradation by the enzyme horseradish peroxidase (HRP). J Hazard Mater 147:1073–1078

    Article  CAS  Google Scholar 

  • Vazquez-duhalt R, Westlake DWS, Fedorak PM (1994) Lignin peroxidase oxidation of aromatic-compounds in systems containing organic-solvents. Appl Environ Microbiol 60:459–466

    CAS  Google Scholar 

  • Veitch NC (2004) Horseradish peroxidase: a modern view of a classic enzyme. Phytochemistry 65:249–259

    Article  CAS  Google Scholar 

  • Weber WJ Jr, Huang Q (2003) Inclusion of persistent organic pollutants in humification processes: direct chemical incorporation of phenanthrene via oxidative coupling. Environ Sci Technol 37:4221–4227

    Article  CAS  Google Scholar 

  • Wirstam M, Blomberg MRA, Siegbahn PEM (1999) Reaction mechanism of compound I formation in heme peroxidase: a density functional theory study. J Am Chem Soc 121:10178–10185

    Article  CAS  Google Scholar 

  • Zhang Y (2008) Research on the recovery of N, N-dimethylformamide in wastewater with pulse extraction column. Dalian University Of Technology, China

    Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (41171193, 51278252, 41171380), the Natural Science Foundation of Jiangsu province, China (BK20130030), the Key Technology R&D Program of Jiangsu Province (BE2011780), the Foundation of State Key Laboratory of Pollution Control and Resources Reuse, China (PCRRF11034), and a scholarship from the China Scholarship Council (CSC).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yanzheng Gao.

Additional information

Responsible editor: Ester Heath

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, Z., Li, H., Peng, A. et al. Oxidation of polycyclic aromatic hydrocarbons by horseradish peroxidase in water containing an organic cosolvent. Environ Sci Pollut Res 21, 10696–10705 (2014). https://doi.org/10.1007/s11356-014-3005-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3005-6

Keywords

Navigation