Bioremediation of Pesticides by Laccases using Recent Approaches: A Review

International Journal of Bio-Technology and Research (IJBTR) ISSN (P):2249–6858; ISSN (E):2249–796X Vol. 10, Issue 1, Jun 2020, 29–40 © TJPRC Pvt. Ltd.

BIOREMEDIATION OF PESTICIDES BY LACCASES USING RECENT APPROACHES: A REVIEW PAIKRAO VIDYA SADASHIVRAO1 & BORKAR PRITA SHAMRAO2 1

School of Life Sciences, Swami Ramanand Teerth Marathwada University, Nanded, Maharashtra, India 2

Department of Microbiology, NES Science College, Nanded, Maharashtra, India

ABSTRACT Agricultural pesticides and herbicides are highly hazardous, and have tendency to bio-accumulate. Their extensive use to meet increasing demand of food crops has resulted in hazardous environmental pollution problems. Bioremediation plays an important role in pesticide degradation. Soil microorganisms are capable of producing various enzymes, amongst whichlaccase enzyme has great pesticide degradation potential. The aim of this review is to focus on recent approaches and applications of laccase in pesticide degradation.

KEYWORDS: Laccase, Bioremediation, Applications & Agricultural

INTRODUCTION A wide range of agro-chemicals have been used in developing countries to sustain the food productivity essential for feeding the ever growing population. These agro chemicals, mostly pesticides are used to control pest attacks[1]. In many cases, these compounds are observed to be persistent in nature. On the whole it has

Original Article

Received: Sep 14, 2019; Accepted: Oct 04, 2019; Published: Jan 02, 2020; Paper Id.: IJBTRJUN20203

been observed that the rapid increase in the use of these chemicals have caused considerable damage to the environment.[2] Pesticides have been consistently used for decades with the aim to prevent and reduce pest infestation, safeguard crop yield and maintain the quality of the agricultural produce. The use of pesticides in large scale farming has resulted in a tremendous growth in crop production and in the reduction of vector borne diseases. For example in 1948-49 food grain production was only 50 million tons that has increased to almost fourfold by the end of 1996-97 to 198 million tons from an estimated 169 million hectares of cropped land. The rise in food grain production was because of field application of pesticides, by using high yield varieties of seeds and improved irrigation infrastructure.(91). Similarly an impressive increase in crop yields has been observed in the United States during the twentieth century[3]. On the other hand a considerable amount of applied pesticides fail to reach their desired targets due to their leaching, degradation and volatilization and thus results in serious environmental problems [5]. Although pesticides are useful in containing the pest multiplication and growth, their constant and unregulated application can adversely affect human health, and the entire eco system. Pesticides pose a serious health risk to living organisms on account of their rapid fat solubility and bio-accumulation in non-target organisms[6].

To overcome the above mentioned problems of pesticide application, technologies for pesticide removal in a safe, systematic and economical manner need to be developed and adopted[7]. The existent technologies employ

www.tjprc.org

editor@tjprc.org

30

Paikrao Vidya Sadashivrao & Borkar Prita Shamrao

various types of physical and chemical methods including percolator filters, adsorption, oxidation, hydrolysis, photolysis and reduction respectively[8, 9]. Food and Agricultural Organisation (FAO) estimated the cost of these operations lies between 3000-4000 USD per ton [7].

The use of above mentioned physiochemical techniques are highly expensive and the process of remediation is also not feasible as the transformed parent product to toxic metabolite is equally or more hazardous to the non - target organisms[10]. These physiochemical approaches conventionally used are cost prohibitive and remediation process is often incomplete due to the transformation of the parent compound to the metabolites which are more persistent and equally or more toxic to non- target organisms [10].

Scientific attempts to eliminate these contaminants from the environment using bio degradation approach have been appreciated. Biological degradation is a process in which soil microorganisms consume or utilize pesticides [11-13].

Pesticide degrading microorganisms can be found in numerous sources including agricultural crops, waste water, sewage sludge, fresh waters, neighbouring pesticide manufacturing areas and industrial effluents. Majorly the microorganisms that have known to possess pesticide degrading activity are found in pesticide contaminated area [7].

Literature is available showing excellent microbial pesticides degradation by microbial species, such as Pseudomonasis the most efficient bacterial genus known for the degradation of toxic compounds [2]. These groups of bacteria degrade toxic compounds depending on the basis of contact time with the compound, climatic conditions in which they are available and their physiological ability.

Various fungal species from Algerian pesticides contaminated soils such as Aspergillusfumigates, A. niger, A. tires, Absidia and Rhizopusmicrosporus are actively involved in pesticide degradation [14]. The research article cited reported 53 of the isolated species for their ability to degrade the herbicide metribuzin in liquid medium. In the same set of experiment potential ability of herbicide in promoting the growth of two genera that is Fusarium and Absidia was also explained; these genera eliminated 50% of the herbicide after 5 days. Furthermore Species of Botrytis cinerea were involved in the elimination of linurol and metroburon herbicides almost completely and other 31 isolated species also could eliminate metroburon[7]. Senthilkumar et al., reports the degradation of endosulfan and methyl parathion by the fungi Tricodermaviridae[14]. White rot fungi exhibit great potential in bioremediation for compounds weakly degraded by bacteria. This is possible due to the production of extracellular enzymes acting on a broad range of organic compounds.

Enzymatic remediation has been proved to be a rapid and highly efficient method of removing pesticides residue from the environment [15-17]. Lignolytic enzymes such as laccase, lignin peroxidase and manganese peroxidase have great potential of pesticide degradation, among which laccase have been widely used to degrade pollutants from environment [18, 19].

Laccase (benzenediol: oxygen oxidoreductase; p-diphenol oxidase EC1.10.3.2), a blue copper oxidase was first discovered in the latex of Japanese lacquer trees (Rhus sp.) by Yoshida[20, 21]. Since then, these enzymes have been observed in various species of plants, insects and bacteria[22]. However, most of the laccases mentioned in the literature have been isolated from higher fungi.

MECHANISM OF CATALYSIS Laccases are the enzyme of interest for many biotechnological industries as they exhibit a wide range of substrate utilization such as polyphenols, anilines, aryldiamines, methoxy-substituted phenols, hydroxyindols, benzenethiols,

Impact Factor (JCC): 5.9084

NAAS Rating: 3.80

Bioremediation of Pesticides by Laccases using Recent Approaches: A Review

31

organic/ inorganic metal compounds and many more[23]. These enzymes are involved in the coupling of four single electron oxidation of the reducing substrate to the four electron reductive cleavage of the dioxygen bond with four copper atoms [24]. Depending on the characteristics obtained by UV/Visible and electron paramagnetic resonance (EPR) spectroscopy these copper atoms are classified into three groups. The type I Copper (T1) imparts dark blue colour to the enzyme, has a strong electronic absorption at nearly 600nm and is EPR detectable. The type II Copper (T2) is colourless but EPR detectable and the type III Copper (T3) composed of two copper atoms that give a poor absorbance near the UV spectrum and no EPR detectable. The T2 and T3 copper atoms form a trinuclear cluster where the binding of multi electron reduction of dioxygen takes place [22, 25].

In the mechanism of catalysis laccase enzyme liberates an electron from T1 copper site to the substrate subsequent to that an internal electron is transferred from the reduced T1 to T2 and T3 copper site. The T3 copper accepts two electrons in the aerobic oxidation process, in which T2 copper is mandatory. The reduction of oxygen to water takes place at the T2 and T3 cluster and passes through a peroxide intermediate[22, 25, 26].

Since laccases catalyse redox reactions, the redox potential value of the compounds is an important consideration to determine whether a compound can be oxidised by laccase or not. The reported redox potential of non- phenolic compounds is higher than laccases, so role of these enzymes has been limited to phenolic compounds for lignin biodegradation. There are small molecules capable of electron transfer mediators, such as laccase mediator systems(LMSs) able to oxidize non-phenolic structure expanding thus the range of compounds that can be oxidized by these enzymes (22,26). The LMSs have successfully been used for applications such as paper pulp bleaching and delignification[27], degradation of polycyclic aromatic hydrocarbons[28] and the decolourization of textile dyes [29].

APPLICATIONS Environmental Applications of Laccase Mediator Systems Laccases exhibit a wide range of natural and synthetic substrates therefore it is used in various biotechnological industries [31]. Moreover, the range of substrates of the enzymes can be expanded by combining with laccase mediators which are substrates of laccase enzyme [25, 32, 33].

Several reports published shows pesticide degradation by laccase mediator systems. Many insecticides and nerve poisons are phosphoorganic compounds and are very hazardous. The purified laccase from Pleurotusostreatus in presence of ABTS (2’azinobis 3-ethylbenzothiazoline) has been shown to perform rapid and complete oxidative degradation of nerve gases VX and Russian VX and the insecticide diisopropylamiton[34]. Glyphosate is a widely used agricultural herbicide, having a potential ability to alter the physiology of aquatic organisms. Pizzul et al. demonstrated the degradation of glyphosate using laccase mediator system[35]. Moreover it is estimated that by using the above mentioned mediators, the enzyme was able to degrade glyphosate in its commercial formulation Roundup. This study reveals an extraordinary substrate range of laccase showing again its potential in bioremediation. Organic halogenated pesticides transformed by laccase mediator system has been investigated by Torres-Duarte et al.[36]. It was suggested that laccase and mediators such as ABTS, HBT1 (hydroxybenzotriazole)napthaso-2naphthol 3,6 disulphonic acid were efficiently performing the biodegradation of dioxins in ash and soil [36]. The degradation of polyurethane and polyolefine with laccase mediator systems has been patented[21]. Also a high yielding laccase from T. versicolor with violuric acid as mediator degraded pyrimethanil and isoproturon up to 100% after 24 hours of incubation[37]. laccase mediator system significantly utilized for the treatment of soil and www.tjprc.org

editor@tjprc.org

32

Paikrao Vidya Sadashivrao & Borkar Prita Shamrao

drain water contaminated with herbicide dymron has been performed[38]. In this study laccase with ABTS as mediator degraded about 90%of dymron within 24 hours.

Applications of Immobilized Laccase Enzyme immobilization is achieved by its attachment to an insoluble natural or synthetic support [39]. Enzyme immobilization have resulted in attaining great benefits over regular biological systems utilizing free enzymes such as easy recovery of cells from the reaction mixture, frequently use of cells, prevention of cell washout at high dilution rate, utilising high cell density and shielding of enzyme from severe environmental conditions[7]. Enzyme immobilization enables the retention of catalytic activity over a long period of time which makes it suitable for bioremediation of pesticides [40].

Generally enzyme immobilization process involves two basic methods making use of physical or chemical interaction as enzyme supporting link. These different links utilise various methodologies for enzyme immobilization. In physical coupling method enzyme is entrapped in a three dimensional matrix or it is encapsulated in an organic or inorganic polymer where as in chemical coupling adsorption, covalent binding to the support or self-immobilization takes place [41, 42].

Experimental evidence shows that pesticide degradation is most effective when laccases are immobilised on different supports such as microporous polypropylene, hollow fiber, Sol-gel silica, alginate-chitosan microcapsules etc.

Rhusvernicefera laccase immobilised in fibre membrane involved in the degradation of some hydroxylated aromatic compounds. In this method laccsae was attached with horseradish peroxidase in microporous propylene. 3, 4dimethylphenols, 4 ethyl phenol 2 hydroxy-1, 2, 3, 4tetrahydronapthaleneand 4hydroxybiphenyl were also degraded up to 50 to 100 %after 48 hours of incubation period [44].

Georgieva et al. [43] studied phenol degradation with laccase from R. verniceferain which laccase was immobilised in a propylene membrane modified with chromic acid and consequently activated by ethylene diamine and GLU (glutaraldehyde).

Immobilizations of enzymes have advantage over free enzyme as this technique enhances thermal stability and their activity in the varied range of pH. Polycyclic aromatic hydrocarbons (PAHs) are one of the major sources of contamination in soil and water, therefore their degradation is of great importance to avoid its accumulation in the environment (30). Kaolinite activated with 3, Aminopyltrithoxysilane (APTES) and GLU have been utilised for the immobilisation of laccase from T. versicolor results in 80% oxidation of anthracene and benzo (a) pyrene(Bap) [89]. Furthermore, research experiments showed that kaolinite in combination with nanoparticles of mesoporous silica Santa Barbara amorphous (SBA-15) utilized for the attachment of laccase from T. versicolor significantly showed stability towards high pH, temperature and efficient oxidation of Bap, explaining the classic role of laccase for PAHs remediation[93]. Later on, the support SBA-15 was functionalised aminopropyl and aminobutyl and laccase from T. Versicolor immobilised by covalent binding and adsorption resulted in degradation of naphthalene [45]. Zhang et al. demonstrated phenolic compounds degradation by enzyme immobilisation method[46]. In this laccase from Coriolus. versicolor was immobilised by the process of adsorption on activated carbon and then by entrapment into calcium alginate gels resulting in the degradation of 2, 4 dichlorophenol. Immobilised laccase found more stable towards pH and temperature than the free enzyme thus more useful in long process of bioremediation.

Impact Factor (JCC): 5.9084

NAAS Rating: 3.80

Bioremediation of Pesticides by Laccases using Recent Approaches: A Review

33

Laccase Mediated Coupling and Grafting Reaction in Pesticides Degradation In coupling reactions two molecules of similar sizes are bound with the aid of catalyst, in grafting, molecules of small size are linked to natural or synthetic polymers. Coupling reactions are mainly of two types such as cross coupling and homocoupling.

Cross coupling involves reaction between two different molecules for the formation of one new molecule, whereas reactant molecules are the same in homo-coupling. [47]. Metal catalysts such as Na, Cu, Pd or Ni are generally utilized in such type of reactions. In bioremediation, coupling reactions play significant role as they can perform various polymerization reactions which results in detoxification and prevention of leaching of highly poisonous and noxious molecules by immobilising them [47]. Enzymatic coupling reactions are significant in removal of natural and synthetic phenolics from soils by binding them on to humic material [47]. Laccases are associated with coupling of molecules through a number of various covalent linkages (C-C; C-O; C-N) which can be achieved by partial demethylation and dehalogenation, significant in bioremediation [47]. Several reports are available showing fungal laccases can degrade or polymerize environment pollutants such as chlorophenol [49], chlorinated hydroxyl biphenyl [25] and nonyl-phenol [28].

Table 1: Application of Laccase Infused Coupling Reactions in Regulating Environmental Pollution Application/Potential Reactants Laccase Source References Application Soil remediation TNT + Guaiacol Pyriculariaoryzae, Trametesversicolor [50] contaminated with TNT Soil remediation TNT + Catechol Trametesvillosa [51, 52] contaminated with TNT TNT+ Syringaldehyde, TNT+ syringic acid, Soilremidiation TNT+ protocatechuic Trametesvillosa [52] contaminated with TNT acid, TNT+ phenol TNT+ caffeic acid.

Soil remediation Ferulic Acid and CeriporiopsisSubvermispora, contaminated with [55] pentachlorophenol Phanerochatetechrysosporium pentachlorophenol TNT+ Ferulic acid, Soil remediation TNT+ guaiacol Trametesmodesta [53,54] contaminated with TNT Catechol+ aromatic amine Syringic acid+ methyl phenols /syringic acid + chlorophenols, vanillic acid, ferulic acid or guaiacol Oxidative coupling of halogenated phenols/coupling halogenated phenols to sugar organic matter Polymerization of oxidised 2,6dimethoxyphenol andsyringaldazine, odiadianisidine www.tjprc.org

Remediation of pollution causingazo dye (methyl orange)

Trametesvillosa

Removal of phenolic pollutants

Rhizocotoniaparaticola

Detoxification through dehalogenation of chlorinated phenols

Trametesvillosa,, Trametesversicolor, Pycnoporuscinnabarinus, Pyriculariaoryzae, Rhizocotoniaparaticola

Detoxification of phenolic pollutants.

Pleurotusostreatus, Rhizocotoniaparaticola

[56]

[57,58]

[57’59-61]

[62,63]

editor@tjprc.org

34

Paikrao Vidya Sadashivrao & Borkar Prita Shamrao

Precipitation and polymerization of phenol Mixture of phenolic compounds (possible coupling and polymerization) α-Naphthol polymerization Guaiacol + 4 chloroaniline Oligomerisation of acetaminophen Oligomerisation of various halogen-, alkyl-, and alkoxysubstituted anilines Clphaoniferyl alcohol + chlorinated phenols Phenol +2,4 – dichlorophenol ß, – Naphthol, 4 – methoxyphenolcatechi n (possible polymerisation Polymerisation of guaiacol, catechol and m – cresol Bisphenol A, Triclosannonylphenol, octyphenol, ethynylestradiol (Oligomersation through oxidative coupling) Cresol, xylenol (possible polymerisation) Methoxy and methyl substituted phenols (possible polymerisation) N’, N’-(dimethyl)-N(2-hydroxyphenyl) urea (polymerisation)

Phenolic effluents decolorization Removal and /or detoxification of phenolic wastes and other aromatic compounds Removal of α- naphthol as insoluble polymer from water bodies Soil or wastewater decontamination Treatment of wastewater to remove acetaminophen Removal or decontamination of substituted anilines from the environment Removal of chlorophenols from water effluent Removal of phenolic compounds in water

Coriolusversicolor

Trametesversicolor, Letinulaedodes

Trametesversicolor, Pyriculariaoryzae, Rhizocotoniaparaticola

[64]

[65,66]

[62,67,68]

Rhizocotoniaparaticola, Trametesversicolor

[69]

Commercial (Sigma-Aldrich)

[70]

Trametesversicolor, Rhizocotoniaparaticola(only active with p – methoxyaniline)

[71]

RhizocotoniaparaticolaandCerrena unicolor

[72]

Coriolusversicolor

[73]

Removal of phenolic mixtures from wastewater

Pyriculariaoryzae

[67]

Removal of phenolic compounds from industrial effluents

Novozym 51003 from geneticallymodified Aspergillus spp. Rhizocotoniaparaticola

Removal of endocrine disrupting chemicals from wastewater.

Claviriopsis aquatic, fungal strain coded as UHH 1-6-18-4; Coriolopsispolyzona, Trametesvillosa, Pycnoporuscoccineus, Coriolus,(Trametes) versicolor, and Pleurotusostreatus

[62,74]

[75-77]

Removal of phenolics from polluted aquatic systems

Trametes sp. Rhizocotoniaparaticola

Wastewater treatment

Rhizocotoniaparaticola

[62]

Removal of phenylurea pesticides in wastewater

Trametesversicolor

[79]

[62,78]

The coupling of 2,4,6- trinitrotoluene(TNT) to humic substances results in the formation of products such as aminodinitrotoluenes, diaminonitrotoluenes, azoxytetranitrotoluenes, dinitrotoluenes these are transformed products of TNT and are less toxic to the parent compound but even though toxic [73]. Dawel et al. proposed a model for irreversible laccase mediated coupling of reduced 2,4,6trinitrotoulene (TNT) metabolites to organic soil matrix. In this model structure of an isolated coupling product of 2, 4 diamino-6 nitrotoulene (2,4-DANT) to guaiacol is explained [49]. This work builds foundation for the same work on detoxification by enzymatic coupling reaction. TNT molecules have also been detoxified Impact Factor (JCC): 5.9084

NAAS Rating: 3.80

Bioremediation of Pesticides by Laccases using Recent Approaches: A Review

35

by coupling to soil humic acid or catechol during an aerobic/anaerobic incubation [50]. Reports are available showing potential of anaerobic microorganisms from cow manure in reduction of TNT during anaerobic phase; consequently in aerobic phase a laccase from T. villosa was used to oxidatively couple to humic matter yielding coupling of 74% with catechol and 25% with humicacid. Significant coupling of TNT metabolite 4 amino -2,6- dinitrotoluene (4 A DNT)on to phenolic humic monomers were reported by Wang et al.[51]. Recent work is done by Nyanhongo et al. in which TNT and principle stable TNT metabolites were immobilised by the application of humic monomers ferulic acid and guaiacol [52].

This work can be conducted in areas highly contaminated with humic substances or can be added. Cheong S, et al. successfully cloned a laccase gene from Trametesversicolor strain involved in the immediate transformation of TNT in culture [53]. This set of work formed the basis for identical work, and again explained the transformation of TNT and its catabolites in fungal culture. The process of transformation completed in a couple of hours and significant increase is seen in the expression of laccase gene during the initial stage of development. Coupling of TNT metabolite 4 amino-2,6dinitrotoulene(4 A DNT) onto phenolic humic monomers were reported by Wang et al.[51]. Laccases also shows efficient covalent coupling of humic ferulicacid and pentachlorophenol, applicable in lands highly polluted with pentachlorophenol [54]. Laccases with mediator (ABTS) involved in the successful oxidation of benzo (alpha) pyrene and anthracene exhibiting polymerization and minimizing toxicity [55. Rhizocotoniaparaticola laccase alone or in combination with syringic acid detoxifies 2,6xylenol (2,6-dimethylphenol), o-cresol and p-cresol [56]. Similarly chlorophenols and methoxyphenols have also been made less toxic by coupling them on to humic acid [66].

CONCLUSIONS The presented review highlights various approaches of laccase enzyme in detoxification of pesticides and potential contaminants in the soil by the application of immobilised laccase, laccase mediator systems and by using laccase coupling and grafting reactions. To increase biotechnological applications of laccase in various indusries, laccase immobilisation, mediators and enhancers should be economical, environment friendly and also enhance the stability of enzymes over a broad range of pH, temperature and substrates.

REFERENCES 1.

Ramanathan, M. P. and D. Lalithakumari, Complete mineralization of methylparathion by Pseudomonas sp. A3. Appl Biochem Biotechnol, 1999. 80(1): p. 1-12.

2.

Abo-Amer, A. E., Biodegradation of Diazinon by Serratia marcescens DI101 and its Use in Bioremediation of Contaminated Environment. Journal of Microbiology and Biotechnology, 2011. 21(1): p. 71-80.

3.

Aktar, W., D. Sengupta, and A. Chowdhury, Impact of Pesticides Use in Agriculture: Their Benefits and Hazards.

Interdisciplinary toxicology, 2009. 2: p. 1-12.

4.

Warren, G. F., Spectacular Increases in Crop Yields in the United States in the Twentieth Century. Weed Technology, 1998.

12(4): p. 752-760.

5.

Chevillard, A., et al., Investigating the biodegradation pattern of an ecofriendly pesticide delivery system based on wheat gluten and organically modified montmorillonites. Polymer Degradation and Stability, 2012. 97: p. 2060–2068.

6.

Agrawal, A., Water Pollution with Special Reference to Pesticide Contamination in India. Journal of Water Resource and Protection, 2010. 02: p. 432-448.

7.

Ortiz-Hernandez, L., et al., Pesticide biodegradation: Mechanisms, genetics and strategies to enhance the process. 2013. p.

www.tjprc.org

editor@tjprc.org

36

Paikrao Vidya Sadashivrao & Borkar Prita Shamrao 251-287.

8.

Bavcon, M., P. Trebse, and L. Zupancic-Kralj, Investigations of the Determination and Transformations of Diazinon and Malathion under Environmental Conditions Using Gas Chromatography Coupled with a Flame Ionisation Detector.

Chemosphere, 2003. 50: p. 595-601.

9.

Kodaka, R., et al., Clay-Catalyzed Nitration of a Carbamate Fungicide Diethofencarb. Journal of agricultural and food chemistry, 2004. 51: p. 7730-7.

10. Nawab, A., A. Aleem, and A. Malik, Determination of Organochlorine Pesticides in Agricultural Soil with Special Reference to ??-HCH Degradation by Pseudomonas Strains. Bioresource technology, 2003. 88: p. 41-6.

11. Sassman, S., et al., Assessing N, N′-Dibutylurea (DBU) Formation in Soils after Application of n-Butylisocyanate and Benlate Fungicides. Journal of agricultural and food chemistry, 2004. 52: p. 747-54.

12. Ghadiri, H., Degradation of Endosulfan in a Clay Soil from Cotton Farms of Western Queensland. Journal of environmental management, 2001. 62: p. 155-69.

13. Bordjiba, O., et al., Removal of Herbicides from Liquid Media by Fungi Isolated from a Contaminated Soil. Journal of environmental quality, 2001. 30: p. 418-26.

14. Senthilkumar, S., et al., Biodegradation of methyl parathion and endosulfan using Pseudomonas aeruginosa and Trichoderma viridae. Journal of environmental science & engineering, 2011. 53: p. 115-22.

15. Sutherland, T., et al., Enzymatic bioremediation: From enzyme discovery to applications. Clinical and experimental pharmacology & physiology, 2004. 31: p. 817-21.

16. Velmurugan, N., et al., Characterization of chikusaku-eki and mokusaku-eki and its inhibitory effect on sapstaining fungal growth in laboratory scale. International Journal of Environment Science and Technology (ISSN: 1735-1472) Vol 6 Num 1, 2008. 6.

17. Omokaro, O. and E. Anyanwu, Impact of Various Concentrations of Crude Oil on Fungal Populations of Soil. International Journal of Environment Science and Technology (ISSN: 1735-1472) Vol 6 Num 2, 2009. 6.

18. Khlifi, R., et al., Effect of HBT on the stability of laccase during the decolourization of textile wastewater. Journal of Chemical Technology and Biotechnology, 2009. 84: p. 1828-1833.

19. Steevensz, A., et al., Comparison of soybean peroxidase with laccase in the removal of phenol from synthetic and refinery wastewater samples. Journal of Chemical Technology and Biotechnology, 2009. 84: p. 761-769.

20. Yoshida, H., LXIII.—Chemistry of lacquer (Urushi). Part I. Communication from the Chemical Society of Tokio. Journal of the Chemical Society, Transactions, 1883. 43(0): p. 472-486.

21. Morozova, O., et al., Laccase-mediator systems and their applications: A review. Applied Biochemistry and Microbiology, 2007. 43: p. 523-535.

22. Madhavi, V. and S. S. Lele, Laccase: Properties and Applications. Bioresources, 2009. 4(4): p. 1694-1717.

23. Kunamneni, A., et al., Decolorization of synthetic dyes by laccase immobilized on epoxy-activated carriers. Process Biochemistry, 2008. 43(2): p. 169-178.

24. Singh, R., Ahirwar, N. K., Tiwari, J., & Pathak, J. Review on Sources and Effect of Heavy Metal in Soil: Its Bioremediation.

25. Giardina, P., et al., Laccases: a never-ending story. Cellular and Molecular Life Sciences, 2010. 67(3): p. 369-385.

Impact Factor (JCC): 5.9084

NAAS Rating: 3.80

Bioremediation of Pesticides by Laccases using Recent Approaches: A Review

37

26. Duran, N., et al., Applications of laccases and tyrosinases (phenoloxidases) immobilized on different supports: a review.

Enzyme and Microbial Technology, 2002. 31(7): p. 907-931.

27. Morozova, O. V., et al., "Blue" laccases. Biochemistry (Mosc), 2007. 72(10): p. 1136-50.

28. Moldes, D., E. M. Cadena, and T. Vidal, Biobleaching of eucalypt kraft pulp with a two laccase-mediator stages sequence.

Bioresour Technol, 2010. 101(18): p. 6924-9.

29. Gomez, J., et al., Applicability of Coriolopsis rigida for biodegradation of polycyclic aromatic hydrocarbons. Biotechnol Lett, 2006. 28(13): p. 1013-7.

30. Moldes, D. and M. A. Sanroman, Amelioration of the ability to decolorize dyes by laccase: relationship between redox mediators and laccase isoenzymes in Trametes versicolor. World Journal of Microbiology & Biotechnology, 2006. 22(11): p.

1197-1204.

31. Yaropolov, A. I., et al., Laccase - Properties, Catalytic Mechanism, and Applicability. Applied Biochemistry and Biotechnology, 1994. 49(3): p. 257-280.

32. Call, H. P. and I. Mucke, History, overview and applications of mediated lignolytic systems, especially laccase-mediatorsystems (Lignozym(R)-process). Journal of Biotechnology, 1997. 53(2-3): p. 163-202.

33. Galli, C. and P. Gentili, Chemical messengers: mediated oxidations with the enzyme laccase. Journal of Physical Organic Chemistry, 2004. 17(11): p. 973-977.

34. Amitai, G., et al., Oxidative biodegradation of phosphorothiolates by fungal laccase. FEBS Lett, 1998. 438(3): p. 195-200.

35. Pizzul, L., M. Castillo, and J. Stenstrรถm, Degradation of glyphosate and other pesticides by ligninolytic enzymes.

Biodegradation, 2009. 20: p. 751-759.

36. Torres-Duarte, C., et al., Halogenated pesticide transformation by a laccase-mediator system. Chemosphere, 2009. 77: p. 68792.

37. Jin, X., et al., Conditions Optimizing and Application of Laccase-mediator System (LMS) for the Laccase-catalyzed Pesticide Degradation. Scientific Reports, 2016. 6.

38. Maruyama, T., et al., Laccase-Mediated Oxidative Degradation of the Herbicide Dymron. Biotechnology progress, 2006. 22: p. 426-30.

39. Arica, M. Y., B. Altintas, and G. Bayramoglu, Immobilization of laccase onto spacer-arm attached non-porous poly(GMA/EGDMA) beads: application for textile dye degradation. Bioresour Technol, 2009. 100(2): p. 665-9.

40. Richins, R. D., A. Mulchandani, and W. Chen, Expression, immobilization, and enzymatic characterization of cellulosebinding domain-organophosphorus hydrolase fusion enzymes. Biotechnol Bioeng, 2000. 69(6): p. 591-6.

41. Matijosyte, I., et al., Preparation and use of cross-linked enzyme aggregates (CLEAs) of laccases. Journal of Molecular Catalysis B-Enzymatic, 2010. 62(2): p. 142-148.

42. Chauhan, M. P., & Singh, N. K. Characterization of Rhizobium Isolates from Sesbania Rhizosphere and their Role in Bioremediation of Glyphosate and Monocrotophos.

43. Sheldon, R. A., Enzyme immobilization: The quest for optimum performance. Advanced Synthesis & Catalysis, 2007. 349(8-9): p. 1289-1307.

44. Moeder, M., C. Martin, and G. Koeller, Degradation of hydroxylated compounds using laccase and horseradish peroxidase immobilized on microporous polypropylene hollow fiber membranes. Journal of Membrane Science, 2004. 245(1-2): p. 183www.tjprc.org

editor@tjprc.org

38

Paikrao Vidya Sadashivrao & Borkar Prita Shamrao 190.

45. Georgieva, S., et al., Advantages in using non-isothermal bioreactors in bioremediation of water polluted by phenol by means of immobilized laccase from Rhus vernicifera. Journal of Molecular Catalysis B-Enzymatic, 2008. 55(3-4): p. 177-184.

46. Couto, S. R. and J. L. T. Herrera, Industrial and biotechnological applications of laccases: A review. Biotechnology Advances, 2006. 24(5): p. 500-513.

47. Dodor, D. E., H. M. Hwang, and S. I. N. Ekunwe, Oxidation of anthracene and benzo[a]pyrene by immobilized laccase from Trametes versicolor. Enzyme and Microbial Technology, 2004. 35(2-3): p. 210-217.

48. Hu, X., X. Zhao, and H.-M. Hwang, Comparative study of immobilized Trametes versicolor laccase on nanoparticles and kaolinite. Chemosphere, 2007. 66: p. 1618-26.

49. Bautista, L., G. Morales, and R. Sanz, Immobilization strategies for laccase from Trametes versicolor on mesostructured silica materials and the application to the degradation of naphthalene. Bioresource technology, 2010. 101: p. 8541-8.

50. Zhang, S., E. Gao, and L. Xia, Dechlorination of dichlorophenol in waste water by immobilized laccase. Huagong Xuebao/Journal of Chemical Industry and Engineering (China), 2006. 57: p. 359-362.

51. Leontievsky, A. A., et al., Transformation of 2,4,6-trichlorophenol by the white rot fungi Panus tigrinus and Coriolus versicolor. Biodegradation, 2000. 11(5): p. 331-40.

52. Dawel, G., et al., Structure of a laccase-mediated product of coupling of 2,4-diamino-6-nitrotoluene to guaiacol, a model for coupling of 2,4,6-trinitrotoluene metabolites to a humic organic soil matrix. Appl Environ Microbiol, 1997. 63(7): p. 2560-5.

53. Thiele, S., E. Fernandes, and J. M. Bollag, Enzymatic transformation and binding of labeled 2,4,6-trinitrotoluene to humic substances during an anaerobic/aerobic incubation. J Environ Qual, 2002. 31(2): p. 437-44.

54. Wang, C. J., T.-B. SĂśren, and J.-M. Bollag, Interaction of 2,4,6-Trinitrotoluene (TNT) and 4-Amino-2,6-Dinitrotoluene with Humic Monomers in the Presence of Oxidative Enzymes. Archives of environmental contamination and toxicology, 2002. 42: p. 1-8.

55. Nyanhongo, G. S., S. R. Couto, and G. M. Guebitz, Coupling of 2,4,6-trinitrotoluene (TNT) metabolites onto humic monomers by a new laccase from Trametes modesta. Chemosphere, 2006. 64(3): p. 359-70.

56. Nyanhongo, G. S., et al., Enzymatic immobilization of 2,4,6-trinitrotoluene (TNT) biodegradation products onto model humic substances. Enzyme and Microbial Technology, 2006. 39(6): p. 1197-1204.

57. RĂźttimann-Johnson, C. and R. Lamar, Polymerization of pentachlorophenol and ferulic acid by fungal extracellular lignindegrading enzymes. Applied and environmental microbiology, 1996. 62: p. 3890-3.

58. Zille, A., et al., Laccase kinetics of degradation and coupling reactions. Journal of Molecular Catalysis B-Enzymatic, 2005.

33: p. 23-28.

59. Bollag, J. M., Decontaminating Soil with Enzymes. Environmental Science & Technology, 1992. 26(10): p. 1876-1881.

60. Bollag, J. M., K. L. Shuttleworth, and D. H. Anderson, Laccase-Mediated Detoxification of Phenolic-Compounds. Applied and Environmental Microbiology, 1988. 54(12): p. 3086-3091.

61. Schultz, A., et al., Dehalogenation of chlorinated hydroxybiphenyls by fungal laccase. Appl Environ Microbiol, 2001. 67(9): p.

4377-81.

62. Dec, J. and J. M. Bollag, Effect of Various Factors on Dehalogenation of Chlorinated Phenols and Anilines during Oxidative Coupling. Environmental Science & Technology, 1995. 29(3): p. 657-663.

Impact Factor (JCC): 5.9084

NAAS Rating: 3.80

Bioremediation of Pesticides by Laccases using Recent Approaches: A Review

39

63. Ahn, M. Y., et al., Treatment of 2,4-Dichlorophenol polluted soil with free and immobilized laccase. Journal of Environmental Quality, 2002. 31(5): p. 1509-1515.

64. Shobana, M., Meenatchi, M., & Mekala, M. Production and Purification of Pectinase Enzyme from Aspergillus Candidus and its Application on Tea Processing.

65. Shuttleworth, K. L. and J. M. Bollag, Soluble and Immobilized Laccase as Catalysts for the Transformation of Substituted Phenols. Enzyme and Microbial Technology, 1986. 8(3): p. 171-177.

66. Hublik, G. and F. Schinner, Characterization and immobilization of the laccase from Pleurotus ostreatus and its use for the continuous elimination of phenolic pollutants. Enzyme and microbial technology, 2000. 27: p. 330-336.

67. Davis, S. and R. G. Burns, Covalent Immobilization of Laccase on Activated Carbon for Phenolic Effluent Treatment. Applied Microbiology and Biotechnology, 1992. 37(4): p. 474-479.

68. Crecchio, C., P. Ruggiero, and M. D. R. Pizzigallo, Polyphenoloxidases Immobilized in Organic Gels - Properties and Applications in the Detoxification of Aromatic-Compounds. Biotechnology and Bioengineering, 1995. 48(6): p. 585-591.

69. D'Annibale, A., et al., Oxirane-immobilized Lentinula edodes laccase: Stability and phenolics removal efficiency in olive mill wastewater. Journal of biotechnology, 2000. 77: p. 265-73.

70. Krastanov, A., Removal of phenols from mixtures by co-immobilized laccase/tyrosinase and Polyclar adsorption. Journal of Industrial Microbiology and Biotechnology, 2000. 24: p. 383-388.

71. AktaĹ&#x;, N., G. Kibarer, and A. Tanyolaç, Effects of reaction conditions on laccase-catalyzed ?-naphthol polymerization.

Journal of Chemical Technology and Biotechnology, 2000. 75: p. 840-846.

72. Simmons, K. E., R. D. Minard, and J. M. Bollag, Oxidative Co-Oligomerization of Guaiacol and 4-Chloroaniline.

Environmental Science & Technology, 1989. 23(1): p. 115-121.

73. Lu, J. H. and Q. G. Huang, Removal of Acetaminophen Using Enzyme-Mediated Oxidative Coupling Processes: II. CrossCoupling with Natural Organic Matter. Environmental Science & Technology, 2009. 43(18): p. 7068-7073.

74. Hoff, T., S. Y. Liu, and J. M. Bollag, Transformation of Halogen-, Alkyl-, and Alkoxy-Substituted Anilines by a Laccase of Trametes versicolor. Appl Environ Microbiol, 1985. 49(5): p. 1040-5.

75. Cho, N. S., et al., Effect of coniferyl alcohol addition on removal of chlorophenols from water effluent by fungal laccase.

Journal of Wood Science, 1999. 45(2): p. 174-178.

76. Kadhim, H., et al., Removal of phenolic compounds in water using Coriolus versicolor grown on wheat bran. Enzyme and Microbial Technology, 1999. 24(5-6): p. 303-307.

77. Ko, C. H. and S. S. Chen, Enhanced removal of three phenols by laccase polymerization with MF/UF membranes. Bioresour Technol, 2008. 99(7): p. 2293-8.

78. Uchida, H., et al., Polymerization of bisphenol A by purified laccase from Trametes villosa. Biochemical and Biophysical Research Communications, 2001. 287(2): p. 355-358.

79. Ramalingam, P., & DEVI, S. V. (2017). Biodegradation and decolourization of azo dyes using marine bacteria. Int. J. Adv. Biotechnol. Res, 7, 1-12.

80. Michizoe, J., M. Goto, and S. Furusaki, Catalytic activity of laccase hosted in reversed micelles. J Biosci Bioeng, 2001. 92(1): p. 67-71.

81. Junghanns, C., et al., Degradation of xenoestrogen nonylphenol by aquatic fungi and their laccases. Microbiology (Reading, www.tjprc.org

editor@tjprc.org

40

Paikrao Vidya Sadashivrao & Borkar Prita Shamrao England), 2005. 151: p. 45-57.

82. Shin-Ya, Y., et al., Efficacy of amphiphile-modified laccase in enzymatic oxidation and removal of phenolics in aqueous solution. Enzyme and Microbial Technology, 2005. 36: p. 147-152.

83. Jolivalt, C., et al., Immobilization of laccase from Trametes versicolor on a modified PVDF microfiltration membrane: characterization of the grafted support and application in removing a phenylurea pesticide in wastewater. Journal of Membrane Science, 2000. 180(1): p. 103-113.

84. Sรถren, T.-B., E. Fernandes, and J.-M. Bollag, Enzymatic Transformation and Binding of Labeled 2,4,6Trinitrotoluene to Humic Substances during an Anaerobic/Aerobic Incubation. Journal of Environmental Quality - J ENVIRON QUAL, 2002. 31.

85. Cheong, S., et al., Determination of laccase gene expression during degradation of 2,4,6-trinitrotoluene and its catabolic intermediates in Trametes versicolor. Microbiological research, 2006. 161: p. 316-20.

86. Collins, P., et al., Oxidation of Anthracene and Benzo[a]pyrene by Laccases from Trametes versicolor. Applied and Environmental Microbiology 62 (1996) 4563-4567., 1996. 62.

AUTHOR'S PROFILE

Vidya Sadashiv Paikrao, did her M.sc. NET Microbiology. She is a Research Scholar In Swami Ramanand Teerth Marathwada University, Nanded. Her topic of research is "Studies on Production and Molecular Characterization of Laccase from Pesticide Degrading Bacteria".

Dr. Mrs. Prita Shamrao Borkar (Chaware), currently working as Associate Professor in Agricultural Microbiology at Department of Botany, Microbiology and Biotechnology, NES Science College, Nanded, Maharashtra, Indai. She has 17 years teaching experience to UG and PG Microbiology and Agricultural Microbiology students. She also contributed in publish of more than 17 research articles in various national and international journals.

Impact Factor (JCC): 5.9084

NAAS Rating: 3.80