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Applied Biochemistry and Biotechnology

, Volume 187, Issue 2, pp 583–611 | Cite as

Laccases from Marine Organisms and Their Applications in the Biodegradation of Toxic and Environmental Pollutants: a Review

  • Monnat Theerachat
  • David Guieysse
  • Sandrine Morel
  • Magali Remaud-Siméon
  • Warawut ChulalaksananukulEmail author
Article
  • 217 Downloads

Abstract

The discharge of industrial effluent creates environmental problems around the world and so necessitates the need for the economically expensive and sometimes technically problematic treatment of the wastewater. Laccases have enormous potential for the oxidative bioremediation of toxic xenobiotic compounds using only molecular oxygen as the sole cofactor for their reaction, and their application is regarded as environmentally friendly. Due to the low substrate specificity of laccases, they can oxidize a variety of substrates. Moreover, by using appropriate mediators, laccases can degrade a wide range of substrates, including those with structural complexity. Thus, laccases are an attractive alternative for wastewater treatment. Marine environments are rich in microorganisms that are exposed to extreme conditions, such as salinity, temperature, and pressure. Laccases from these microorganisms potentially have suitable properties that might be adaptive to bioremediation processes. This review provides the latest information on laccases from marine environments, their sources, biochemical properties, media composition for laccase production, and their applications in the bioremediation of industrial waste, especially focusing on dye decolorization.

Keywords

Laccase Bioremediation Xenobiotic compounds Marine environment Dye decolorization 

Notes

Acknowledgements

We gratefully acknowledge Chulalongkorn University for financial support.

Compliance with Ethical Standards

Conflict of Interest

All authors declare that they have no conflict of interest.

References

  1. 1.
    Solomon, E. I., Sundaram, U. M., & Machonkin, T. E. (1996). Multicopper oxidases and oxygenases. Chemical Reviews, 96(7), 2563–2606.Google Scholar
  2. 2.
    Brijwani, K., Rigdon, A., & Vadlani, P. V. (2010). Fungal laccases: Production, function, and applications in food processing. Enzyme Research. Research article.  https://doi.org/10.4061/2010/149748.
  3. 3.
    Baldrian, P. (2006). Fungal laccases—occurrence and properties. FEMS Microbiology Reviews, 30(2), 215–242.  https://doi.org/10.1111/j.1574-4976.2005.00010.x.Google Scholar
  4. 4.
    Riva, S. (2006). Laccases: Blue enzymes for green chemistry. Trends in Biotechnology, 24(5), 219–226.  https://doi.org/10.1016/j.tibtech.2006.03.006.Google Scholar
  5. 5.
    Zeng, S., Qin, X., & Xia, L. (2017). Degradation of the herbicide isoproturon by laccase-mediator systems. Biochemical Engineering Journal, 119, 92–100.  https://doi.org/10.1016/j.bej.2016.12.016.Google Scholar
  6. 6.
    Bonugli-santos, R. C., Durrant, L. R., & Sette, L. D. (2010). Laccase activity and putative laccase genes in marine-derived basidiomycetes. Fungal Biology, 114(10), 863–872.  https://doi.org/10.1016/j.funbio.2010.08.003.Google Scholar
  7. 7.
    Theerachat, M., Emond, S., Cambon, E., Bordes, F., Marty, A., Nicaud, J.-M., Chulalaksananukul, W., Guieysse, D., Remaud-Siméon, M., & Morel, S. (2012). Engineering and production of laccase from Trametes versicolor in the yeast Yarrowia lipolytica. Bioresource Technology, 125, 267–274.  https://doi.org/10.1016/j.biortech.2012.07.117.Google Scholar
  8. 8.
    Theerachat, M., Tanapong, P., & Chulalaksananukul, W. (2017). The culture or co-culture of Candida rugosa and Yarrowia lipolytica strain rM-4A, or incubation with their crude extracellular lipase and laccase preparations, for the biodegradation of palm oil mill wastewater. International Biodeterioration & Biodegradation, 121, 11–18.  https://doi.org/10.1016/j.ibiod.2017.03.002.Google Scholar
  9. 9.
    Saravanakumar, K., & Kathiresan, K. (2014). Bioremoval of the synthetic dye malachite green by marine Trichoderma sp. SpringerPlus, 3(631). Doi: https://doi.org/10.1186/2193-1801-3-631.
  10. 10.
    Eldridge, H. C., Milliken, A., Farmer, C., Hampton, A., Wendland, N., Coward, L., Gregory, D. J., & Johnson, C. M. (2017). Efficient remediation of 17α-ethinylestradiol by Lentinula edodes (shiitake) laccase. Biocatalysis and Agricultural Biotechnology, 10, 64–68.  https://doi.org/10.1016/j.bcab.2017.02.004.Google Scholar
  11. 11.
    Vallecillos, L., Sadef, Y., Borrull, F., Pocurull, E., & Bester, K. (2017). Degradation of synthetic fragrances by laccase-mediated system. Journal of Hazardous Materials, 334, 233–243.  https://doi.org/10.1016/j.jhazmat.2017.04.003.Google Scholar
  12. 12.
    D’Souza-Ticlo, D., Sharma, D., & Raghukumar, C. (2009). A thermostable metal-tolerant laccase with bioremediation potential from a marine-derived fungus. Marine Biotechnology (NY), 11(6), 725–737.  https://doi.org/10.1007/s10126-009-9187-0.Google Scholar
  13. 13.
    Kennedy, J., O’Leary, N. D., Kiran, G. S., Morrissey, J. P., O’Gara, F., Selvin, J., & Dobson, A. D. W. (2011). Functional metagenomic strategies for the discovery of novel enzymes and biosurfactants with biotechnological applications from marine ecosystems. Journal of Applied Microbiology, 111(4), 787–799.  https://doi.org/10.1111/j.1365-2672.2011.05106.x.Google Scholar
  14. 14.
    Nikolaivits, E., Dimarogona, M., Fokialakis, N., & Topakas, E. (2017). Marine-derived biocatalysts: Importance, accessing, and application in aromatic pollutant bioremediation. Frontiers in Microbiology, 8, 265.  https://doi.org/10.3389/fmicb.2017.00265.Google Scholar
  15. 15.
    Trincone, A. (2011). Marine biocatalysts: Enzymatic features and applications. Marine Drugs, 9(4), 478–499.  https://doi.org/10.3390/md9040478.Google Scholar
  16. 16.
    Coulon, F., McKew, B. A., Osborn, A. M., McGenity, T. J., & Timmis, K. N. (2007). Effects of temperature and biostimulation on oil-degrading microbial communities in temperate estuarine waters. Environmental Microbiology, 9(1), 177–186.  https://doi.org/10.1111/j.1462-2920.2006.01126.x.Google Scholar
  17. 17.
    Passarini, M. R., Ottoni, C. A., Santos, C., Lima, N., & Sette, L. D. (2015). Induction, expression and characterisation of laccase genes from the marine-derived fungal strains Nigrospora sp. CBMAI 1328 and Arthopyrenia sp. CBMAI 1330. AMB Express, 5, 19.  https://doi.org/10.1186/s13568-015-0106-7.
  18. 18.
    Li, L., Purnima, S., Ying, L., Shenquan, P., & Guangyi, W. (2014). Diversity and biochemical features of culturable fungi from the coastal waters of southern China. AMB Express, 4(60), 60.  https://doi.org/10.1186/s13568-014-0060-9.Google Scholar
  19. 19.
    Panno, L., Bruno, M., Voyron, S., Anastasi, A., Gnavi, G., Miserere, L., & Varese, G. C. (2013). Diversity, ecological role and potential biotechnological applications of marine fungi associated to the seagrass Posidonia oceanica. New Biotechnology, 30(6), 685–694.  https://doi.org/10.1016/j.nbt.2013.01.010.Google Scholar
  20. 20.
    Mydlarz, L. D., & Palmer, C. V. (2011). The presence of multiple phenoloxidases in Caribbean reef-building corals. Comparative Biochemistry and Physiology: A Molecular and Integrative Physiology, 159(4), 372–378.  https://doi.org/10.1016/j.cbpa.2011.03.029.Google Scholar
  21. 21.
    Irving, P., Troxler, L., & Hetru, C. (2004). Is innate enough? The innate immune response in Drosophila. Comptes Rendus Biologies, 327(6), 557–570.Google Scholar
  22. 22.
    Amparyup, P., Charoensapsri, W., & Tassanakajon, A. (2013). Prophenoloxidase system and its role in shrimp immune responses against major pathogens. Fish & Shellfish Immunology, 34(4), 990–1001.  https://doi.org/10.1016/j.fsi.2012.08.019.Google Scholar
  23. 23.
    Luna-Acosta, A., Rosenfeld, E., Amari, M., Fruitier-Arnaudin, I., Bustamante, P., & Thomas-Guyon, H. (2010). First evidence of laccase activity in the Pacific oyster Crassostrea gigas. Fish & Shellfish Immunology, 28(4), 719–726.  https://doi.org/10.1016/j.fsi.2010.01.008.Google Scholar
  24. 24.
    Li, Q., Wang, X., Korzhev, M., Schroder, H. C., Link, T., Tahir, M. N., Diehl-Seifert, B., & Muller, W. E. (2015). Potential biological role of laccase from the sponge Suberites domuncula as an antibacterial defense component. Biochimica et Biophysica Acta, 1850(1), 118–128.  https://doi.org/10.1016/j.bbagen.2014.10.007.Google Scholar
  25. 25.
    Priya, B., Uma, L., Ahamed, A. K., Subramanian, G., & Prabaharan, D. (2011). Ability to use the diazo dye, C.I. Acid Black 1 as a nitrogen source by the marine cyanobacterium Oscillatoria curviceps BDU92191. Bioresource Technology, 102(14), 7218–7223.  https://doi.org/10.1016/j.biortech.2011.02.117.Google Scholar
  26. 26.
    Lucas-Elio, P., Goodwin, L., Woyke, T., Pitluck, S., Nolan, M., Kyrpides, N. C., Detter, J. C., Copeland, A., Teshima, H., Bruce, D., Detter, C., Tapia, R., Han, S., Land, M. L., Ivanova, N., Mikhailova, N., Johnston, A. W. B., & Sanchez-Amat, A. (2012). Complete genome sequence of the melanogenic marine bacterium Marinomonas mediterranea type strain (MMB-1(T)). Standards in Genomic Science, 6(1), 63–73.  https://doi.org/10.4056/sigs.2545743. Google Scholar
  27. 27.
    Liu, G., Zhou, J., Meng, X., Fu, S. Q., Wang, J., Jin, R., & Lv, H. (2013). Decolorization of azo dyes by marine Shewanella strains under saline conditions. Applied Microbiology and Biotechnology, 97(9), 4187–4197.  https://doi.org/10.1007/s00253-012-4216-8.Google Scholar
  28. 28.
    Moghadam, M. S., Albersmeier, A., Winkler, A., Cimmino, L., Rise, K., Hohmann-Marriott, M. F., Kalinowski, J., Ruckert, C., Wentzel, A., & Lale, R. (2016). Isolation and genome sequencing of four Arctic marine Psychrobacter strains exhibiting multicopper oxidase activity. BMC Genomics, 17(1), 117.  https://doi.org/10.1186/s12864-016-2445-4.Google Scholar
  29. 29.
    Raghukumar, C., D’Souza, T. M., Thorn, R. G., & Reddy, C. A. (1999). Lignin-modifying enzymes of Flavodon flavus, a basidiomycete isolated from a coastal marine environment. Applied and Environmental Microbiology, 65(5), 2103–2111.Google Scholar
  30. 30.
    Verma, A. K., Raghukumar, C., Verma, P., Shouche, Y. S., & Naik, C. G. (2010). Four marine-derived fungi for bioremediation of raw textile mill effluents. Biodegradation, 21(2), 217–233.  https://doi.org/10.1007/s10532-009-9295-6.Google Scholar
  31. 31.
    Bonugli-Santos, R. C., Durrant, L. R., da Silva, M., & Sette, L. D. (2010). Production of laccase, manganese peroxidase and lignin peroxidase by Brazilian marine-derived fungi. Enzyme and Microbial Technology, 46(1), 32–37.  https://doi.org/10.1016/j.enzmictec.2009.07.014.Google Scholar
  32. 32.
    Chen, H. Y., Xue, D. S., Feng, X. Y., & Yao, S. J. (2011). Screening and production of ligninolytic enzyme by a marine-derived fungal Pestalotiopsis sp. J63. Applied Biochemistry and Biotechnology, 165(7–8), 1754–1769.  https://doi.org/10.1007/s12010-011-9392-y.Google Scholar
  33. 33.
    Jiang, J., Zhou, Z., Dong, Y., Guan, X., Wang, B., Jiang, B., Yang, A., Chen, Z., Gao, S., & Sun, H. (2014). Characterization of phenoloxidase from the sea cucumber Apostichopus japonicus. Immunobiology, 219(6), 450–456.  https://doi.org/10.1016/j.imbio.2014.02.006.Google Scholar
  34. 34.
    Shi, L., Chan, S., Li, C., & Zhang, S. (2017). Identification and characterization of a laccase from Litopenaeus vannamei involved in anti-bacterial host defense. Fish and Shellfish Immunology, 66, 1–10.  https://doi.org/10.1016/j.fsi.2017.04.026.Google Scholar
  35. 35.
    Cerenius, L., Babu, R., Söderhäll, K., & Jiravanichpaisal, P. (2010). In vitro effects on bacterial growth of phenoloxidase reaction products. Journal of Invertebrate Pathology, 103(1), 21–23.  https://doi.org/10.1016/j.jip.2009.09.006.Google Scholar
  36. 36.
    Jiang, J., Zhou, Z., Dong, Y., Cong, C., Guan, X., Wang, B., Chen, Z., Jiang, B., Yang, A., Gao, S., & Sun, H. (2014). In vitro antibacterial analysis of phenoloxidase reaction products from the sea cucumber Apostichopus japonicus. Fish and Shellfish Immunology, 39(2), 458–463.  https://doi.org/10.1016/j.fsi.2014.06.002.Google Scholar
  37. 37.
    Subramani, R., Kumar, R., Prasad, P., & Aalbersberg, W. (2013). Cytotoxic and antibacterial substances against multi-drug resistant pathogens from marine sponge symbiont: Citrinin, a secondary metabolite of Penicillium sp. Asian Pacific Journal of Tropical Biomedicine, 3(4), 291–296.  https://doi.org/10.1016/s2221-1691(13)60065-9.Google Scholar
  38. 38.
    Raghukumar, C., D’Souza-Ticlo, D., & Verma, A. K. (2008). Treatment of colored effluents with lignin-degrading enzymes: An emerging role of marine-derived fungi. Critical Reviews in Microbiology, 34(3–4), 189–206.  https://doi.org/10.1080/10408410802526044.Google Scholar
  39. 39.
    Bonugli-Santos, R. C., Vieira, G. A., Collins, C., Fernandes, T. C., Marin-Morales, M. A., Murray, P., & Sette, L. D. (2016). Enhanced textile dye decolorization by marine-derived basidiomycete Peniophora sp. CBMAI 1063 using integrated statistical design. Environmental Science and Pollution Research International, 23(9), 8659–8668.  https://doi.org/10.1007/s11356-016-6053-2.Google Scholar
  40. 40.
    Prabaharan, D., Sumathi, M., & Subramanian, G. (1994). Ability to use ampicillin as a nitrogen source by the marine cyanobacterium Phormidium valderianum BDU 30501. Current Microbiology, 28(6), 315–320.Google Scholar
  41. 41.
    Saha, S. K., Swaminathan, P., Raghavan, C., Uma, L., & Subramanian, G. (2010). Ligninolytic and antioxidative enzymes of a marine cyanobacterium Oscillatoria willei BDU 130511 during poly R-478 decolourization. Bioresource Technology, 101(9), 3076–3084.  https://doi.org/10.1016/j.biortech.2009.12.075.Google Scholar
  42. 42.
    Palanisami, S., Prabaharan, D., & Uma, L. (2009). Fate of few pesticide-metabolizing enzymes in the marine cyanobacterium Phormidium valderianum BDU 20041 in perspective with chlorpyrifos exposure. Pesticide Biochemistry and Physiology, 94(2-3), 68–72.  https://doi.org/10.1016/j.pestbp.2009.03.003.Google Scholar
  43. 43.
    Priya, B., Sivaprasanth, R. K., Jensi, V. D., Uma, L., Subramanian, G., & Prabaharan, D. (2010). Characterization of manganese superoxide dismutase from a marine cyanobacterium Leptolyngbya valderiana BDU20041. Saline Systems, 6(6), 6.  https://doi.org/10.1186/1746-1448-6-6.Google Scholar
  44. 44.
    Wang, X., Wang, Q., Guo, X., Liu, L., Guo, J., Yao, J., & Zhu, H. (2015). Functional genomic analysis of Hawaii marine metagenomes. Science Bulletin, 60(3), 348–355.  https://doi.org/10.1007/s11434-014-0658-y.Google Scholar
  45. 45.
    Fang, Z. M., Li, T. L., Chang, F., Zhou, P., Fang, W., Hong, Y. Z., Zhang, X. C., Peng, H., & Xiao, Y. Z. (2012). A new marine bacterial laccase with chloride-enhancing, alkaline-dependent activity and dye decolorization ability. Bioresource Technology, 111, 36–41.  https://doi.org/10.1016/j.biortech.2012.01.172.Google Scholar
  46. 46.
    Fang, H., Cai, L., Yang, Y., Ju, F., Li, X., Yu, Y., & Zhang, T. (2014). Metagenomic analysis reveals potential biodegradation pathways of persistent pesticides in freshwater and marine sediments. The Science of the Total Environment, 470–471, 983–992.  https://doi.org/10.1016/j.scitotenv.2013.10.076.Google Scholar
  47. 47.
    Cheng, Y., Jiang, J., Dong, Y., & Zhou, Z. (2015). Identification and characterization of proteins with phenoloxidase-like activities in the sea urchin Strongylocentrotus nudus. Fish and Shellfish Immunology, 47(1), 117–121.  https://doi.org/10.1016/j.fsi.2015.08.020.Google Scholar
  48. 48.
    de Souza, D. F., Tychanowicz, G. K., de Souza, C. G., & Peralta, R. M. (2006). Co-production of ligninolytic enzymes by Pleurotus pulmonarius on wheat bran solid state cultures. Journal of Basic Microbiology, 46(2), 126–134.  https://doi.org/10.1002/jobm.200510014.Google Scholar
  49. 49.
    Sharma, P., Goel, R., & Capalash, N. (2007). Bacterial laccases. World Journal of Microbiology and Biotechnology, 23(6), 823–832.  https://doi.org/10.1007/s11274-006-9305-3.Google Scholar
  50. 50.
    Fang, Z., Li, T., Wang, Q., Zhang, X., Peng, H., Fang, W., Hong, Y., Ge, H., & Xiao, Y. (2011). A bacterial laccase from marine microbial metagenome exhibiting chloride tolerance and dye decolorization ability. Applied Microbiology and Biotechnology, 89(4), 1103–1110.  https://doi.org/10.1007/s00253-010-2934-3.Google Scholar
  51. 51.
    Michniewicz, A., Ullrich, R., Ledakowicz, S., & Hofrichter, M. (2006). The white-rot fungus Cerrena unicolor strain 137 produces two laccase isoforms with different physico-chemical and catalytic properties. Applied Microbiology and Biotechnology, 69(6), 682–688.  https://doi.org/10.1007/s00253-005-0015-9.Google Scholar
  52. 52.
    Naki, A., & Varfolomeev, S. D. (1981). Mechanism of the inhibition of laccase activity from Polyporus versicolor by halide ions. Biokhimiia (Moscow, Russia), 46(9), 1694–1702.Google Scholar
  53. 53.
    Raghukumar, C. (2008). Marine fungal biotechnology: An ecological perspective. Fungal Diversity, 31, 19–35.Google Scholar
  54. 54.
    Gianfreda, L., Xu, F., & Bollag, J.-M. (1999). Laccases: A useful group of oxidoreductive enzymes. Bioremediation Journal, 3(1), 1–26.  https://doi.org/10.1080/10889869991219163.Google Scholar
  55. 55.
    Majeau, J.-A., Brar, S. K., & Tyagi, R. D. (2010). Laccases for removal of recalcitrant and emerging pollutants. Bioresource Technology, 101(7), 2331–2350.  https://doi.org/10.1016/j.biortech.2009.10.087.Google Scholar
  56. 56.
    D’Souza, D. T., Tiwari, R., Sah, A. K., & Raghukumar, C. (2006). Enhanced production of laccase by a marine fungus during treatment of colored effluents and synthetic dyes. Enzyme and Microbial Technology, 38(3-4), 504–511.  https://doi.org/10.1016/j.enzmictec.2005.07.005.Google Scholar
  57. 57.
    Divya, L. M., Prasanth, G. K., & Sadasivan, C. (2013). Isolation of a salt tolerant laccase secreting strain of Trichoderma sp. NFCCI-2745 and optimization of culture conditions and assessing its effectiveness in treating saline phenolic effluents. Journal of Environmental Sciences, 25(12), 2410–2416.  https://doi.org/10.1016/S1001-0742(12)60321-0.Google Scholar
  58. 58.
    Li, J., Xie, Y., Wang, R., Fang, Z., Fang, W., Zhang, X., & Xiao, Y. (2018). Mechanism of salt-induced activity enhancement of a marine-derived laccase, Lac15. European Biophysics Journal: EBJ, 47(3), 225–236.  https://doi.org/10.1007/s00249-017-1251-5.Google Scholar
  59. 59.
    DeSouza-Ticlo, D., Verma, A. K., Mathew, M., & Raghukumar, C. (2006). Effect of nutrient nitrogen on laccase production, its isozyme pattern and effluent decolorization by the fungus NIOCC no #2a, isolated from mangrove wood. Indian Journal of Marine Sciences, 35(4), 364–372.Google Scholar
  60. 60.
    Feng, X., Chen, H., Xue, D., & Yao, S. (2013). Enhancement of laccase activity by marine-derived Deuteromycete Pestalotiopsis sp. J63 with agricultural residues and inducers. Chinese Journal of Chemical Engineering, 21(10), 1182–1189.  https://doi.org/10.1016/S1004-9541(13)60567-4.Google Scholar
  61. 61.
    Yang, J., Wang, G., Ng, T. B., Lin, J., & Ye, X. (2016). Laccase production and differential transcription of laccase genes in Cerrena sp. in response to metal ions, aromatic compounds, and nutrients. Frontiers in Microbiology, 6. doi: https://doi.org/10.3389/fmicb.2015.01558.
  62. 62.
    Si, J., & Cui, B.-K. (2013). Study of the physiological characteristics of the medicinal mushroom Trametes pubescens (higher Basidiomycetes) during the laccase-producing process. International Journal of Medicinal Mushrooms, 15(2), 199–210.Google Scholar
  63. 63.
    Nakade, K., Nakagawa, Y., Yano, A., Konno, N., Sato, T., & Sakamoto, Y. (2013). Effective induction of pblac1 laccase by copper ion in Polyporus brumalis ibrc05015. 117, 52–61.  https://doi.org/10.1016/j.funbio.2012.11.005
  64. 64.
    Manavalan, T., Manavalan, A., Thangavelu, K. P., & Heese, K. (2013). Characterization of optimized production, purification and application of laccase from Ganoderma lucidum. Biochemical Engineering Journal, 70, 106–114.  https://doi.org/10.1016/j.bej.2012.10.007.Google Scholar
  65. 65.
    Palmieri, G., Giardina, P., Bianco, C., Fontanella, B., & Sannia, G. (2000). Copper induction of laccase isoenzymes in the ligninolytic fungus Pleurotus ostreatus. Applied and Environmental Microbiology, 66(3), 920–924.  https://doi.org/10.1128/AEM.66.3.920-924.2000.Google Scholar
  66. 66.
    Giardina, P., Palmieri, G., Scaloni, A., Fontanella, B., Faraco, V., Cennamo, G., & Sannia, G. (1999). Protein and gene structure of a blue laccase from Pleurotus ostreatus1. Biochemical Journal, 341(Pt 3), 655–663.Google Scholar
  67. 67.
    Yang, Y., Wei, F., Zhuo, R., Fan, F., Liu, H., Zhang, C., Ma, L., Jiang, M., & Zhang, X. (2013). Enhancing the laccase production and laccase gene expression in the white-rot fungus Trametes velutina 5930 with great potential for biotechnological applications by different metal ions and aromatic compounds. PLoS One, 8(11), e79307.  https://doi.org/10.1371/journal.pone.0079307.Google Scholar
  68. 68.
    Hao, J., Song, F., Huang, F., Yang, C., Zhang, Z., Zheng, Y., & Tian, X. (2007). Production of laccase by a newly isolated deuteromycete fungus Pestalotiopsis sp. and its decolorization of azo dye. Journal of Industrial Microbiology & Biotechnology, 34(3), 233–240.  https://doi.org/10.1007/s10295-006-0191-3.Google Scholar
  69. 69.
    Piscitelli, A., Giardina, P., Lettera, V., Pezzella, C., Sannia, G., & Faraco, V. (2011). Induction and transcriptional regulation of laccases in fungi. Current Genomics, 12(2), 104–112.  https://doi.org/10.2174/138920211795564331.Google Scholar
  70. 70.
    Singh, R. P., Singh, P. K., & Singh, R. L. (2014). Bacterial decolorization of textile azo dye acid orange by Staphylococcus hominis RMLRT03. Toxicology International, 21(2), 160–166.  https://doi.org/10.4103/0971-6580.139797.Google Scholar
  71. 71.
    Pirok, B. W. J., Knip, J., van Bommel, M. R., & Schoenmakers, P. J. (2016). Characterization of synthetic dyes by comprehensive two-dimensional liquid chromatography combining ion-exchange chromatography and fast ion-pair reversed-phase chromatography. Journal of Chromatography A, 1436, 141–146.  https://doi.org/10.1016/j.chroma.2016.01.070.Google Scholar
  72. 72.
    Ambatkar, M., & Mukundan, U. (2014). Enzymatic decolourisation of methyl Orange and Bismarck Brown using crude peroxidase from Armoracia rusticana. Applied Water Science, 5(4), 397–406.  https://doi.org/10.1007/s13201-014-0197-3.Google Scholar
  73. 73.
    Passarini, M. R. Z., Santos, C., Lima, N., Berlinck, R. G. S., & Sette, L. D. (2013). Filamentous fungi from the Atlantic marine sponge Dragmacidon reticulatum. Archives of Microbiology, 195(2), 99–111.  https://doi.org/10.1007/s00203-012-0854-6.Google Scholar
  74. 74.
    Theerachat, M., Morel, S., Guieysse, D., Remaud-Simeon, M., & Chulalaksananukul, W. (2012). Comparison of synthetic dye decolorization by whole cells and a laccase enriched extract from Trametes versicolor DSM11269. African Journal of Biotechnology, 11(8), 1964–1969.  https://doi.org/10.5897/AJB11.2469.Google Scholar
  75. 75.
    Asad, S., Amoozegar, M. A., Pourbabaee, A. A., Sarbolouki, M. N., & Dastgheib, S. M. M. (2007). Decolorization of textile azo dyes by newly isolated halophilic and halotolerant bacteria. Bioresource Technology, 98(11), 2082–2088.  https://doi.org/10.1016/j.biortech.2006.08.020.Google Scholar
  76. 76.
    Ogugbue, C. J., Sawidis, T., & Oranusi, N. A. (2011). Evaluation of colour removal in synthetic saline wastewater containing azo dyes using an immobilized halotolerant cell system. Ecological Engineering, 37(12), 2056–2060.  https://doi.org/10.1016/j.ecoleng.2011.09.003.Google Scholar
  77. 77.
    Wu, J., Kim, K.-S., Sung, N.-C., Kim, C.-H., & Lee, Y.-C. (2009). Isolation and characterization of Shewanella oneidensis WL-7 capable of decolorizing azo dye reactive black 5. The Journal of General and Applied Microbiology, 55(1), 51–55.Google Scholar
  78. 78.
    Ip, A. W. M., Barford, J. P., & McKay, G. (2010). Biodegradation of reactive black 5 and bioregeneration in upflow fixed bed bioreactors packed with different adsorbents. Journal of Chemical Technology & Biotechnology, 85(5), 658–667.  https://doi.org/10.1002/jctb.2349.Google Scholar
  79. 79.
    Gopalakrishnan, R., & Sellappa, S. (2011). Decolourisation of methyl orange and methyl red by live and dead biomass of fungi. Asian Journal of Experimental Biological Sciences, 2(4), 569–574.Google Scholar
  80. 80.
    Wesenberg, D., Kyriakides, I., & Agathos, S. N. (2003). White-rot fungi and their enzymes for the treatment of industrial dye effluents. Biotechnology Advances, 22(1-2), 161–187.  https://doi.org/10.1016/j.biotechadv.2003.08.011.Google Scholar
  81. 81.
    Ali, N., Ikramullah, Lutfullah, G., Hameed, A., & Ahmed, S. (2007). Decolorization of acid red 151 by Aspergillus niger SA1 under different physicochemical conditions. World Journal of Microbiology and Biotechnology, 24(7), 1099–1105.  https://doi.org/10.1007/s11274-007-9581-6.Google Scholar
  82. 82.
    Aksu, Z., & Karabayır, G. (2008). Comparison of biosorption properties of different kinds of fungi for the removal of Gryfalan black RL metal-complex dye. Bioresource Technology, 99(16), 7730–7741.  https://doi.org/10.1016/j.biortech.2008.01.056.Google Scholar
  83. 83.
    Magan, N., Fragoeiro, S., & Bastos, C. (2010). Environmental factors and bioremediation of xenobiotics using white rot fungi. Mycobiology, 38(4), 238–248.  https://doi.org/10.4489/MYCO.2010.38.4.238.Google Scholar
  84. 84.
    Mougin, C., Pericaud, C., Malosse, C., Laugero, C., & Asther, M. (n.d.). Biotransformation of the insecticide lindane by the white rot basidiomycete Phanerochaete chrysosporium. Pesticide Science, 47(1), 51–59.  https://doi.org/10.1002/(SICI)1096-9063(199605)47:1<51::AID-PS391>3.0.CO;2-V.
  85. 85.
    da Coelho-Moreira, J. S., Bracht, A., da Silva de Souza, A. C., Oliveira, R. F., de Sá-Nakanishi, A. B., de Souza, C. G. M., & Peralta, R. M. (2013). Degradation of Diuron by Phanerochaete chrysosporium: role of ligninolytic enzymes and cytochrome P450. BioMed Research International, 2013. ID 251354. doi: https://doi.org/10.1155/2013/251354
  86. 86.
    Nagpal, V., Srinivasan, M. C., & Paknikar, K. M. (2008). Biodegradation of γ-hexachlorocyclohexane (Lindane) by a non-white rot fungus Conidiobolus 03-1-56 isolated from litter. Indian Journal of Microbiology, 48(1), 134–141.  https://doi.org/10.1007/s12088-008-0013-6.Google Scholar
  87. 87.
    Ulčnik, A., Cigić, I. K., & Pohleven, F. (2013). Degradation of lindane and endosulfan by fungi, fungal and bacterial laccases. World Journal of Microbiology and Biotechnology, 29(12), 2239–2247.  https://doi.org/10.1007/s11274-013-1389-y.Google Scholar
  88. 88.
    Donoso, C., Becerra, J., Martínez, M., Garrido, N., & Silva, M. (2008). Degradative ability of 2,4,6-tribromophenol by saprophytic fungi Trametes versicolor and Agaricus augustus isolated from chilean forestry. World Journal of Microbiology and Biotechnology, 24(7), 961–968.  https://doi.org/10.1007/s11274-007-9559-4.Google Scholar
  89. 89.
    Balcázar-López, E., Méndez-Lorenzo, L. H., Batista-García, R. A., Esquivel-Naranjo, U., Ayala, M., Kumar, V. V., Savary, O., Cabana, H., Herrera-Estrella, A., & Folch-Mallol, J. L. (2016). Xenobiotic compounds degradation by heterologous expression of a Trametes sanguineus laccase in Trichoderma atroviride. PLoS One, 11(2), e0147997.  https://doi.org/10.1371/journal.pone.0147997.Google Scholar
  90. 90.
    Bollag, J. M., Chu, H.-L., Rao, M. A., & Gianfreda, L. (2003). Enzymatic oxidative transformation of chlorophenol mixtures. Journal of Environmental Quality, 32(1), 63–69.Google Scholar
  91. 91.
    Arakaki, R. L., Monteiro, D. A., Boscolo, M., Dasilva, R., & Gomes, E. (2014). Halotolerance, ligninase production and herbicide degradation ability of basidiomycetes strains. Brazilian Journal of Microbiology, 44(4), 1207–1214.  https://doi.org/10.1590/S1517-83822014005000014.Google Scholar
  92. 92.
    Petrovič, U., Gunde-Cimerman, N., & Plemenitaš, A. (n.d.). Cellular responses to environmental salinity in the halophilic black yeast Hortaea werneckii. Molecular Microbiology, 45(3), 665–672.  https://doi.org/10.1046/j.1365-2958.2002.03021.x.
  93. 93.
    Bautista, L. F., Morales, G., & Sanz, R. (2015). Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by laccase from Trametes versicolor covalently immobilized on amino-functionalized SBA-15. Chemosphere, 136, 273–280.  https://doi.org/10.1016/j.chemosphere.2015.05.071.Google Scholar
  94. 94.
    Zeng, J., Lin, X., Zhang, J., Li, X., & Wong, M. H. (2011). Oxidation of polycyclic aromatic hydrocarbons by the bacterial laccase CueO from E. coli. Applied Microbiology and Biotechnology, 89(6), 1841–1849.  https://doi.org/10.1007/s00253-010-3009-1.Google Scholar
  95. 95.
    Wu, Y., Teng, Y., Li, Z., Liao, X., & Luo, Y. (2008). Potential role of polycyclic aromatic hydrocarbons (PAHs) oxidation by fungal laccase in the remediation of an aged contaminated soil. Soil Biology and Biochemistry, 40(3), 789–796.  https://doi.org/10.1016/j.soilbio.2007.10.013.Google Scholar
  96. 96.
    Chandra, R., & Chowdhary, P. (2015). Properties of bacterial laccases and their application in bioremediation of industrial wastes. Environmental Science Processes & Impacts, 17(2), 326–342.  https://doi.org/10.1039/c4em00627e.Google Scholar
  97. 97.
    Wu, Y.-R., Luo, Z.-H., & Vrijmoed, L. L. P. (2010). Biodegradation of anthracene and benz[a]anthracene by two Fusarium solani strains isolated from mangrove sediments. Bioresource Technology, 101(24), 9666–9672.  https://doi.org/10.1016/j.biortech.2010.07.049.Google Scholar
  98. 98.
    Louvado, A., Gomes, N. C. M., Simões, M. M. Q., Almeida, A., Cleary, D. F. R., & Cunha, A. (2015). Polycyclic aromatic hydrocarbons in deep sea sediments: Microbe-pollutant interactions in a remote environment. The Science of the Total Environment, 526, 312–328.  https://doi.org/10.1016/j.scitotenv.2015.04.048.Google Scholar
  99. 99.
    Zhang, A., Zhao, S., Wang, L., Yang, X., Zhao, Q., Fan, J., & Yuan, X. (2016). Polycyclic aromatic hydrocarbons (PAHs) in seawater and sediments from the northern Liaodong Bay, China. Marine Pollution Bulletin, 113(1), 592–599.  https://doi.org/10.1016/j.marpolbul.2016.09.005.Google Scholar
  100. 100.
    Marini, M., & Frapiccini, E. (2013). Persistence of polycyclic aromatic hydrocarbons in sediments in the deeper area of the northern Adriatic Sea (Mediterranean Sea). Chemosphere, 90(6), 1839–1846.  https://doi.org/10.1016/j.chemosphere.2012.09.080.Google Scholar
  101. 101.
    Schedler, M., Hiessl, R., Valladares Juárez, A. G., Gust, G., & Müller, R. (2014). Effect of high pressure on hydrocarbon-degrading bacteria. AMB Express, 4, 77.  https://doi.org/10.1186/s13568-014-0077-0.Google Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Botany, Faculty of ScienceChulalongkorn UniversityBangkokThailand
  2. 2.Université de Toulouse, INSA, UPS, INP, LISBPToulouseFrance
  3. 3.CNRS, UMR5504ToulouseFrance
  4. 4.INRA, UMR792, Ingénierie des Systèmes Biologiques et des ProcédésToulouseFrance

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