Advertisement

Laccase from Scytalidium thermophilum: Production Improvement, Catalytic Behavior and Detoxifying Ability of Diclofenac

  • Sonia Ben YounesEmail author
  • Saoussen Ben Khedher
  • Yongjun Zhang
  • Sven-Uwe Geissen
  • Sami Sayadi
Article
  • 14 Downloads

Abstract

The intensive use of diclofenac (DCF), a nonsteroidal anti-inflammatory drug, has led to its wide occurrence in the environment. The present study investigated the potential use of the fungal Scytalidium thermophilum laccase for DCF removal and detoxification. Firstly, the culture conditions for the maximum fungal laccase production were optimized with a hybrid design and the obtained conditions were: glucose, 13 g L−1; ammonium tartrate, 7.5 g L−1; yeast extract, 11.5 g L−1; CuSO4, 300 µM; temperature, 42 °C and aeration, 30%. A maximum laccase activity of 8220 U L−1 was detected at 5th day, which was fivefold higher than the result with the initial medium. Secondly and for the first time, the laccase successfully removed 98% of DCF at optimum conditions (37 °C, pH 4.5 and DCF 200 mg L−1) within 8 h and without mediators. Genotoxicity, cytotoxicity and phytotoxcity revealed a non toxic metabolites after biologic treatment via S. thermophilum laccase. In fact, hemolytic effect of treated DCF was significantly less than that of untreated DCF. This result was confirmed by morphological variations in erythrocyte shape in both treated and untreated DCF, in comparison to untreated control of red blood cells. In addition, the algal toxicity suggested that treated DCF was significantly less toxic than untreated DCF in chlorophyll contents showing an increase of carotenoids and lycopenes, in comparison to the control culture of D. salina. The effectiveness of S. thermophilum laccase in the DCF biotransformation and its toxicity removal can be considered an interesting option for further environmental applications.

Graphical Abstract

Keywords

Scytalidium thermophilum laccase Hybrid design Diclofenac Degradation Detoxification 

Notes

Acknowledgements

This work is financially supported by the “Tunisian Ministry of Higher Education and Scientific Research”.

Supplementary material

10562_2019_2771_MOESM1_ESM.doc (702 kb)
Supplementary material 1 (DOC 702 kb)

References

  1. 1.
    Barcelos RP, Bresciani G, Rodriguez-Miguelez P, Cuevas MJ, Antunes Soares FA, Barbosa NV, González-Gallego J (2016) Diclofenac pretreatment effects on the toll-like receptor 4/nuclear factor kappa B-mediated inflammatory response to eccentric exercise in rat liver. Life Sci 148:247–253CrossRefGoogle Scholar
  2. 2.
    Zhang Y, Geissen SU, Gal C (2008) Carbamazepine and diclofenac: removal in wastewater treatment plants and occurrence in water bodies. Chemosphere 73:1151–1161CrossRefGoogle Scholar
  3. 3.
    Ziltener JL, Leal S, Fournier PE (2010) Non-steroidal anti-inflammatory drugs for athletes: an update. Ann Phys Rehabil Med 53:278–282CrossRefGoogle Scholar
  4. 4.
    Moreira NFF, Orge CA, Ribeiro AR, Faria JL, Nunes OCM, Pereira FR, Silva AMT (2015) Fast mineralization and detoxification of amoxicillin and diclofenac by photocatalytic ozonation and application to an urban wastewater. Water Res 87:87–96CrossRefGoogle Scholar
  5. 5.
    Naidoo V, Swan GE (2009) Diclofenac toxicity in Gyps vulture is associated with decreased uric acid excretion and not renal portal vasoconstriction. Comp Biochem Physiol C 149:269–274Google Scholar
  6. 6.
    Rodriguez-Delgado M, Orona-Navar C, García-Morales R, Hernandez-Luna C, Parra R, Mahlknecht J, Ornelas-Soto N (2016) Biotransformation kinetics of pharmaceutical and industrial micropollutants in groundwaters by a laccase cocktail from Pycnoporus sanguineus CS43 fungi. Int Biodeterior Biodegrad 108:34–41CrossRefGoogle Scholar
  7. 7.
    Hata T, Shintate H, Kawai S, Okamura H, Nishida T (2010) Elimination of carbamazepine by repeated treatment with laccase in the presence of 1-hydroxybenzotriazole. J Hazard Mater 181:1175–1178CrossRefGoogle Scholar
  8. 8.
    Nguyen LN, Hai FI, Price WE, Leusch FDL, Roddick F, Mc Adam EJ, Magram SF, Nghiem LD (2014) Continuous biotransformation of bisphenol A and DCF by laccase in an enzymatic membrane reactor. Int Biodeterior Biodegrad 95:25–32CrossRefGoogle Scholar
  9. 9.
    Grasser CA, Ammann EM, Shahgaldian P, Corvini PFX (2014) Laccases to take on the challenge of emerging organic contaminants in wastewater. Appl Microbiol Biotechnol 98:9931–9952CrossRefGoogle Scholar
  10. 10.
    Ben Younes S, Cherif I, Dhouib A, Sayadi S (2016) Trametes trogii: a biologic powerful tool for dyes decolorization and detoxification. Catal Lett 146:204–211CrossRefGoogle Scholar
  11. 11.
    Aghaie-Khouzania M, Forootanfar H, Moshfegh M, Khoshayand MR, Faramarzi MA (2012) Decolorization of some synthetic dyes using optimized culture broth of laccase producing ascomycete Paraconiothyrium variabile. Biochem Eng J 60:9–15CrossRefGoogle Scholar
  12. 12.
    Ben Younes S, Karray F, Sayadi S (2011) Isolation of thermophilic fungal strains producing oxido-reductase and hydrolase enzymes from various Tunisian biotopes. Int Biodeter Biodegrad 65:1104–1109CrossRefGoogle Scholar
  13. 13.
    Tahmasbi H, Khoshayand MR, Bozorgi-Koushalshahi M, Heidary M, Ghazi-Khansari M, Faramarzi MA (2016) Biocatalytic conversion and detoxification of imipramine by the laccase-mediated system. Int Biodeterior Biodegrad 108:1–8CrossRefGoogle Scholar
  14. 14.
    Ben Younes S, Sayadi S (2012) Detoxification of indigo carmine using a combined treatment via a novel trimeric thermostable laccase and microbial consortium. J Mol Catal B 87:62–68CrossRefGoogle Scholar
  15. 15.
    Ben Younes S, Bouallagui Z, Sayadi S (2012) Catalytic behavior and detoxifying ability of an atypical homotrimeric laccase from the thermophilic strain Scytalidium thermophilum on selected azo and triarylmethane dyes. J Mol Catal B 79:41–48CrossRefGoogle Scholar
  16. 16.
    Ben Younes S, Ellouze M, Sayadi S (2013) A comparative study of an industrial effluent treatment using enzymatic and alkaline adapted consortium assays. J Chem Technol Biotechnol 88:563–571CrossRefGoogle Scholar
  17. 17.
    Bae S, Kim D, Lee W (2013) Degradation of diclofenac by pyrite catalyzed Fenton oxidation. Appl Catal B 134:93–102CrossRefGoogle Scholar
  18. 18.
    Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  19. 19.
    Plackett RL, Burman JP (1946) The design of optimal multifactorial experiments. Biometrika 33:305–325CrossRefGoogle Scholar
  20. 20.
    Lewis GA, Mathieu D, Phan Tan Luu R (1999) Pharmaceutical experimental design. Marcel Dekker, New YorkGoogle Scholar
  21. 21.
    Mathieu D, Nony J, Phan Tan Luu R (2000) NEMRODW software, LPRAI sarl, Marseille, F-13331, FranceGoogle Scholar
  22. 22.
    Ben Younes S, Bouallagui Z, Gargoubi A, Sayadi S (2011) Investigation of dyes degradation intermediates with Scytalidium thermophilum laccase. Eur Food Res Technol 233:751–758CrossRefGoogle Scholar
  23. 23.
    Gupta AK, Ahmad I, Ahmad M (2015) Genotoxicity of refinery waste assessed by some DNA damage tests. Ecotoxicol Environ Saf 114:250–256CrossRefGoogle Scholar
  24. 24.
    Guo-Xiang L, Zai-Qun L (2008) The protective effects of ginsenosides on human erythrocytes against hemin-induced hemolysis. Food Chem Toxicol 46:886–892CrossRefGoogle Scholar
  25. 25.
    Alimi H, Hfaeidh N, Bouoni Z, Sakly M, Ben Rhouma K (2012) Protective effect of Opuntia ficus indica f. inermis prickly pear juice upon ethanol-induced damages in rat erythrocytes. Alcohol 46:235–243CrossRefGoogle Scholar
  26. 26.
    Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembrane. In: Lucas WJ, Berry JA (eds) Methods in enzymology, vol 148. American Society of Plant Physiologists, Rockville, pp 350–382Google Scholar
  27. 27.
    Fish WW, Perkins-Veazie P, Collins JK (2002) A quantitative assay for lycopene that utilizes reduced volumes of organic solvents. J Food Comp Anal 15:309–317CrossRefGoogle Scholar
  28. 28.
    Tong P, Hong Y, Xiao Y, Zhang M, Tu X, Cui T (2007) High production of laccase by a new basidiomycete. Biotechnol Lett 29:295–301CrossRefGoogle Scholar
  29. 29.
    Arockiasamy S, Krishnan IP, Anandakrishnan N, Seenivasan S, Sambath A, Venkatasubramani JP (2008) Enhanced production of laccase from Coriolus versicolor NCIM 996 by nutrient optimization using response surface methodology. Appl Biochem Biotechnol 151:371–379CrossRefGoogle Scholar
  30. 30.
    Diwaniyan S, Sharma KK, Kuhad RC (2012) Laccase from an alkalitolerant basidiomycetes Crinipellis sp. RCK-1: production optimization by response surface methodology. J Basic Microbiol 52:397–407CrossRefGoogle Scholar
  31. 31.
    Zhang Y, Sun S, Hu K, Lin X (2012) Improving production of laccase from novel basidiomycete with response surface methodology. Afr J Biotechnol 11:7009–7015CrossRefGoogle Scholar
  32. 32.
    Saravanakumar K, Saranya R, Sankaranarayana A, Kaviyarasan V (2010) Statistical designs and response surface technique for the optimization of extracellular laccase enzyme production by using Pleurotus sp. Rec Res Sci Tech 2:104–111Google Scholar
  33. 33.
    Ben Younes S, Sayadi S (2011) Purification and characterization of a novel trimeric and thermotolerant laccase produced from the ascomycete Scytalidium thermophilum strain. J Mol Catal B: enzyme 73:35–42CrossRefGoogle Scholar
  34. 34.
    Baldrian P (2006) Fungal laccases occurrence and properties. FEMS Microbiol Rev 30:215–242CrossRefGoogle Scholar
  35. 35.
    Lu C, Vonshak A (2002) Effects of salinity on photosystem II function in cyanobacterial Spirulina platensis cells. Physiol Planta 114:405–413CrossRefGoogle Scholar
  36. 36.
    Borowitzka M, Borowitzka L (1988) Dunaliella. In: Borowitzka MA, Borowitzka LJ (eds) Microalgal biotechnology. Cambridge Univ Press, Cambridge, pp 27–58Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Sonia Ben Younes
    • 1
    Email author
  • Saoussen Ben Khedher
    • 2
  • Yongjun Zhang
    • 3
  • Sven-Uwe Geissen
    • 3
  • Sami Sayadi
    • 1
    • 4
  1. 1.Laboratoire des Bioprocédés Environnementaux, Centre de Biotechnologie de SfaxUniversité de SfaxSfaxTunisia
  2. 2.Agronomical Institute of KefUniversity of JendoubaKefTunisia
  3. 3.Chair of Environmental Process Engineering, Department of Environmental TechnologyTechnical University of BerlinBerlinGermany
  4. 4.Center for Sustainable Development, College of Arts and SciencesQatar UniversityDohaQatar

Personalised recommendations