Skip to main content
SpringerLink
Log in

Evaluation of oxidative enzymes for efficient oxidation of aniline and phenolic pollutants

  • Original Paper
  • Published:
International Journal of Environmental Science and Technology Aims and scope Submit manuscript

Abstract

Tyrosinases, laccases, and peroxidases are three important groups of oxidative enzymes. A characteristic feature of these enzymes is their ability for the oxidation of aniline and phenolic compounds. Literature review reveals some overlap between the organic substrates of these enzymes, but how exactly they are different and how much they have in common from both substrate structure and rate of oxidation points of views. Can they complete functional efficiency of each other when co-immobilized in a multi-enzymes system? To address these questions, edible mushroom (Agaricus bisporus) tyrosinase, Neurospora crassa laccase, and horseradish peroxidase were examined for the oxidation of azo derivatives of anilines and phenols. These substances were selected because their enzymatic degradation is of interest to environmentalists and can be followed spectrophotometrically. Experiments showed that tyrosinase and laccase had limitations in oxidizing these substances, especially anilines, while peroxidase oxidized all the selected compounds. However, substrates carrying electron-withdrawing substituents had slower oxidation. Co-immobilization of tyrosinase and laccase would be effective against phenolic compounds, but phenols oxidation proceeds faster (between 100 and 500 times) if peroxidase and H2O2 are used. Combination of peroxidase and H2O2, instead of co-immobilization of tyrosinase, laccase, and peroxidase, seems to be more promising for the removal of organic pollutants from contaminated water resources.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abbas ME, Luo W, Zhu L, Zou J, Tang H (2010) Fluorometric determination of hydrogen peroxide in milk by using a Fenton reaction system. Food Chem 120:327–331

    Article  CAS  Google Scholar 

  • Adinew B (2012) Textile effluent treatment and decolourization techniques—a review. Bulg J Sci Educ 21:434–456

    CAS  Google Scholar 

  • Arca-Ramos A, Ammann EM, Gasser CA, Nastold P, Eibes G, Feijoo G, Lema JM, Moreira MT, Corvini PF (2016) Assessing the use of nanoimmobilized laccases to remove micropollutants from wastewater. Environ Sci Pollut Res Int 23:3217–3228

    Article  CAS  Google Scholar 

  • Asgher M, Bhatti HN, Ashraf M, Legge R (2008) Recent developments in biodegradation of industrial pollutants by white rot fungi and their enzyme system. Biodegradation 19:771–783

    Article  CAS  Google Scholar 

  • Babuponnusami A, Muthukumar K (2014) A review on Fenton and improvements to the Fenton process for wastewater treatment. J Environ Chem Eng 2:557–572

    Article  CAS  Google Scholar 

  • Behbahani I, Miller SA, Okeeffe HF (1993) A comparison of mushroom tyrosinase dopaquinone and dopachrome assays using diode-array spectrophotometry: dopachrome formation vs ascorbate-linked dopaquinone reduction. Microchem J 47:251–260

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bhuvaneshwari DS, Elango KP (2006) Substituent and solvent effects on the electrochemical oxidation of para- and meta-substituted anilines. Z Naturforsch 61b:1254–1260

    Article  Google Scholar 

  • Casella L, Monzani E, Nicolis S (2010) Potential applications of peroxidases in the fine chemical industries. In: Torres E, Ayala M (eds) Biocatalysis Based on heme peroxidases: peroxidases as potential industrial biocatalysts, 1sd edn. Springer, Berlin

    Google Scholar 

  • Chang Q, Zhu L, Jiang G, Tang H (2009) Sensitive fluorescent probes for determination of hydrogen peroxide and glucose based on enzyme-immobilized magnetite/silica nanoparticles. Anal Bioanal Chem 395:2377–2385

    Article  CAS  Google Scholar 

  • Chiong T, Lau SY, Khor EH, Danquah MK (2014) Enzymatic approach to phenol removal from wastewater using peroxidases. OA Biotechnol 10:3–9

    Google Scholar 

  • Crecchio C, Ruggiero P, Pizzigallo M (1995) Polyphenol oxidases immobilized in organic gels: properties and applications in the detoxification of aromatic compounds. Biotechnol Bioeng 48:585–591

    Article  CAS  Google Scholar 

  • Davis S, Burns RG (1990) Decolorization of phenolic effluents by soluble and immobilized phenol oxidases. Appl Microbiol Biotechnol 32:721–726

    Article  CAS  Google Scholar 

  • Dedeyan B, Klonowska A, Tagger S, Tron T, Iacazio G, Gil G, Le Petit J (2000) Biochemical and molecular characterization of a laccase from Marasmius quercophilus. Appl Environ Microbiol 66:925–929

    Article  CAS  Google Scholar 

  • Dsikowitzky L, Schwarzbauer J (2014) Industrial organic contaminants: identification, toxicity and fate in the environment. Environ Chem Lett 12:371–386

    Article  CAS  Google Scholar 

  • Durán N, Esposito E (2000) Potential applications of oxidative enzymes and phenoloxidase-like compounds in wastewater and soil treatment: a review. Appl Catal B Environ 28:83–99

    Article  Google Scholar 

  • Farhadi S, Haghbeen K, Marefatjo MJ, Hoor MG, Zahiri HS, Rahimi K (2011) Anionic peroxidase production by Arnebia euchroma callus. Biotechnol Appl Biochem 58:456–463

    Article  CAS  Google Scholar 

  • Fishbein L (1984) Aromatic amines. In: Choudry GG, Hutzinger O (eds) The handbook of environmental chemistry, anthropogenic compounds. Springer, Berlin, pp 1–40

    Google Scholar 

  • Haghbeen K, Legge RL (2016) Synthesis of a novel class of chromophoric cross-linkers. J Iran Chem Soc 13:1–9

    Article  CAS  Google Scholar 

  • Haghbeen K, Tan EW (1998) Facile synthesis of catechol azo dyes. J Org Chem 63:4503–4505

    Article  CAS  Google Scholar 

  • Haghbeen K, Tan EW (2003) Direct spectrophotometric assay of monooxygenase and oxidase activities of mushroom tyrosinase in the presence of synthetic and natural substrates. Anal Biochem 312:23–32

    Article  CAS  Google Scholar 

  • Haghbeen K, Rastgar Jazii F, Karkhane AA, Shareefi Borojerdi S (2004a) Purification of tyrosinase from edible mushroom. Iran J Biotechnol 2:189–194

    CAS  Google Scholar 

  • Haghbeen K, Saboury AA, Karbassi F (2004b) Substrate share in the suicide inactivation of mushroom tyrosinase. Biochim Biophys Acta 1675:139–146

    Article  CAS  Google Scholar 

  • Haghbeen K, Mozaffarian V, Ghaffari F, Pourazeezi E, Saraji M, Daliri Joupari M (2006) Lithospermum officinale callus produces shikalkin. Biol Bratisl 61(4):463–467

    Article  CAS  Google Scholar 

  • Haghbeen K, Babaeikhalili M, Saeid Nematpour F, Gheibi N, Fazli M, Alijanianzadeh M, Zolghadri Jahromi S, Sariri RJ (2010) Surveying allosteric cooperativity and cooperative inhibition in mushroom tyrosinase. J Food Biochem 34:308–328

    Article  CAS  Google Scholar 

  • Hodgman CE, Jewet MC (2012) Cell-free synthetic biology: thinking outside the cell. Metab Eng 14:261–269

    Article  CAS  Google Scholar 

  • Huang J, Chang Q, Ding Y, Han H, Tang H (2014) Catalytic oxidative removal of 2,4-dichlorophenol by simultaneous use of horseradish peroxidase and graphene oxide/Fe3O4 as catalyst. Chem Eng J 254:434–442

    Article  CAS  Google Scholar 

  • Khan AA, Alzohairy MA (2010) Recent advances and applications of immobilized enzyme technologies: a review. Res J Biol Sci 5:565–575

    Article  Google Scholar 

  • Krastanov AJ (2000) Removal of phenols from mixtures by co-immobilized laccase/tyrosinase and polyclar adsorption. J Indust Microbiol Biotechnol 24:383–388

    Article  CAS  Google Scholar 

  • Liu W, Wang WC, Li HS, Zhou X (2011) Immobilization of horseradish peroxidase on silane-modified ceramics and their properties: potential for oily wastewater treatment. Water Sci Technol 63:1621–1628

    Article  CAS  Google Scholar 

  • Liu S, Wang W, Chen J, Sun J (2012) Determination of aniline and its derivatives in environmental water by capillary electrophoresis with on-line concentration. Int J Mol Sci 13:6863–6872

    Article  CAS  Google Scholar 

  • Maciel MJM, Castro e Silva A, Ribeiro HCT (2010) Industrial and biotechnological applications of ligninolytic enzymes of the basidiomycota: a review. Electron J Biotechnol 13:14–15

    Google Scholar 

  • Martelli A, Robbiano L, Carrozzino R (2000) DNA damage induced by 3,3′-dimethoxybenzidine in liver and urinary bladder cells of rats and humans. Toxicol Sci 53:71–76

    Article  CAS  Google Scholar 

  • Martins AS, Vasconcelos VM, Ferreira TCR, Pereira-Filho ER, Lanza MRV (2015) Simultaneous degradation of diuron and hexazinone herbicides by photo-fenton: assessment of concentrations of H2O2 and Fe2+ by the response surface methodology. J Adv Oxid Technol 18:9–14

    CAS  Google Scholar 

  • Mattos C, Ringe D (2001) Proteins in organic solvents. Curr Opin Struc Biol 11:761–764

    Article  CAS  Google Scholar 

  • Michałowicz J, Duda W (2007) Phenols—sources and toxicity. Pol J Environ Stud 16:347–362

    Google Scholar 

  • Mikolasch A, Schauer F (2009) Fungal laccases as tools for the synthesis of new hybrid molecules and biomaterials. Appl Microbiol Biotechnol 82:605–624

    Article  CAS  Google Scholar 

  • Mirazizi F, Bahrami A, Haghbeen K, Shahbani Zahiri H, Bakavoli M, Legge RL (2015) Rapid and direct spectrophotometric method for kinetics studies and routine assay of peroxidase based on aniline diazo substrates. J Enzyme Inhib Med Chem 2:1–8

    Google Scholar 

  • Moshtaghioun SM, Haghbeen K, Sahebghadam A, Legge RL, Khoshneviszadeh R, Farhadi S (2011) Direct spectrophotometric assay of laccase using diazo derivatives of guaiacol. Anal Chem 83:4200–4205

    Article  CAS  Google Scholar 

  • Moshtaghioun SM, Dadkhah M, Bahremandjo K, Haghbeen K, Aminzadeh S, Legge RL (2017) Optimization of Simultaneous Production of Tyrosinase and Laccase by Neurospora crassa. Biotrans J 35(1):1–10

    Article  CAS  Google Scholar 

  • Pereira L, Alves M (2012) Dyes—environmental impact and remediation. In: Malik A, Grohmann E (eds) Environmental protection strategies for sustainable development. Springer, Dordrecht, pp 111–162

    Chapter  Google Scholar 

  • Rouhani Shohre, Salimi Shabnam, Haghbeen Kamahldin (2008) Development of optical pH sensors based on derivatives of hydroxyazobenzene, and the extended linear dynamic range using mixture of dyes. Dyes Pigments 77:363

    Article  CAS  Google Scholar 

  • Shareefi Borojerdi S, Haghbeen K, Karkhane AA, Fazli M, Saboury AA (2004) Successful resonance Raman study of cresolase activity of mushroom tyrosinase. Biochem Biophys Res Commun 314:925–930

    Article  CAS  Google Scholar 

  • Sung YM, Gayam SR, Wu SP (2013) The oxidation of phenylhydrazine by tyrosinase. Appl Biochem Biotechnol 169:2420–2429

    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 46:1–15

    Article  CAS  Google Scholar 

  • Van Haandel MJ, Claassens MM, Van der Hout N, Vervoort J, Rietjens IM (1999) Differential substrate behavior of phenol and aniline derivatives during conversion by horseradish peroxidase. Biochim Biophys Acta 1435:22–29

    Article  Google Scholar 

  • Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR, Lee D, Shioda T, Soto AM, Vom Saal FS, Welshons WV, Zoeller RT, Myers JP (2012) Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev 33:1–78

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Yildiz HB, Caliskan S, Kamaci M, Caliskan A, Yilmaz H (2013) l-Dopa synthesis catalyzed by tyrosinase immobilized in poly(ethyleneoxide) conducting polymers. Int J Biol Macromol 56:34–40

    Article  CAS  Google Scholar 

  • Yotova L, Yaneva S, Marinkova D, Serfaty S (2013) Co-immobilization of peroxidase and tyrosinase onto hybrid membranes obtained by the sol-gel method for the construction of an optical biosensor. Biotechnol Biotechnol Equip 27:3585–3589

    Article  CAS  Google Scholar 

  • Zaharia C, Suteu D (2012) Textile organic dyes—characteristics, polluting effects and separation/elimination procedures from industrial effluents—a critical overview. In: Puzyn T, Mostrag-Szlichtyng A (eds) Organic pollutants ten years after the Stockholm convention-environmental and analytical update. InTech, Croatia

    Google Scholar 

Download references

Acknowledgements

Financial support for the laccase and tyrosinase experiments was provided by National Institute of Genetic Engineering and Biotechnology (Ph.D. and master student grants), and financial support for the peroxidase experiments was provided by Center for International Scientific Studies and Collaboration, Ministry of Science, Research and Technology of the Islamic Republic of Iran for the ICRP project (Research Contract 259).

Author information

Authors and Affiliations

  1. National Institute of Genetic Engineering and Biotechnology, P.O.Box: 14965/161, Tehran, Iran

    F. Mirazizi, A. Bahrami, S. Soleimani Asl, A. Zaribafan, K. Haghbeen & S. Aminzadeh

Authors
  1. F. Mirazizi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Bahrami
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Soleimani Asl
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Zaribafan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. K. Haghbeen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. Aminzadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. Haghbeen.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 300 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mirazizi, F., Bahrami, A., Soleimani Asl, S. et al. Evaluation of oxidative enzymes for efficient oxidation of aniline and phenolic pollutants. Int. J. Environ. Sci. Technol. 15, 1679–1686 (2018). https://doi.org/10.1007/s13762-017-1493-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13762-017-1493-x

Keywords

Search

Navigation