Water, Air, & Soil Pollution

, Volume 223, Issue 5, pp 2333–2345 | Cite as

The Production of Ligninolytic Enzymes by Marine-Derived Basidiomycetes and Their Biotechnological Potential in the Biodegradation of Recalcitrant Pollutants and the Treatment of Textile Effluents

  • Rafaella C. Bonugli-Santos
  • Lucia Regina Durrant
  • Lara Durães Sette
Article
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Abstract

Filamentous fungi derived from marine environments are well known as a potential genetic resource for various biotechnological applications. Although terrestrial fungi have been reported to be highly efficient in the remediation of xenobiotic pollutants, fungi isolated from the marine environment may possess biological advantages over terrestrial fungi because of their adaptations to high salinity and pH extremes. The present study describes the production of ligninolytic enzymes under saline and non-saline conditions and the decolorization of Remazol Brilliant Blue R (RBBR) dye by three basidiomycetes recovered from marine sponges (Tinctoporellus sp. CBMAI 1061, Marasmiellus sp. CBMAI 1062, and Peniophora sp. CBMAI 1063). Ligninolytic enzymes were primarily produced by these fungi in a salt-free malt extract and malt extract formulated with artificial seawater (saline condition). CuSO4 and wheat bran were the best inducers of lignin peroxidase and manganese peroxidase activity. RBBR was decolorized up to 100% by the three fungi, and Tinctoporellus sp. CBMAI 1061 was the most efficient. Our results revealed the biotechnological potential of marine-derived basidiomycetes for dye decolorization and the treatment of colored effluent as well as for the degradation of other organopollutants by ligninolytic enzymes in non-saline and saline conditions that resemble the marine environment.

Keywords

Marine-derived fungi Basidiomycetes Dye decolorization Ligninolytic enzymes Biotechnological applications 
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Notes

Acknowledgments

This work was supported by a grant from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), 05/60175-2. R.C. Bonugli-Santos was supported by a Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and by FAPESP fellowship.

References

  1. Arora, D. S., & Gill, P. K. (2001). Comparison of two assay procedures for lignin peroxidase. Enzyme and Microbial Technology, 28, 602–605.CrossRefGoogle Scholar
  2. Arora, D. S., & Sharma, R. K. (2010). Ligninolytic fungal laccases and their biotechnological applications. Applied Biochemistry and Biotechnology, 160(6), 1760–1788.CrossRefGoogle Scholar
  3. Barrasa, J. M., Martínez, A. T., & Martínez, M. J. (2009). Isolation and selection of novel basidiomycetes for decolorization of recalcitrant dyes. Folia Microbiologica, 54(1), 59–66.CrossRefGoogle Scholar
  4. Bonugli-Santos, R. C., Durrant, L. R., & Sette, L. D. (2010). Laccase activity and putative laccase genes in marine-derived basidiomycetes. Fungal Biology, 114, 863–872.CrossRefGoogle Scholar
  5. 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, 32–37.CrossRefGoogle Scholar
  6. Buswell, J. K., Cai, Y. J., & Chang, S. T. (1995). Effect of nutrient nitrogen on manganese peroxidase and lacase production by Lentinula (Lentinus) edodes. FEMS Microbiology Letters, 128, 81–88.CrossRefGoogle Scholar
  7. Call, H. P., & Mucke, I. (1997). History, overview and applications of mediated lignolytic systems, especially laccase-mediator-systems (Lignozym-process). Journal of Biotechnology, 53, 163–202.CrossRefGoogle Scholar
  8. Chung, K. T., Stevens, S. E., Jr., & Cerniglia, C. R. (1992). The reduction of azo dyes by the intestinal microflora. Critical Reviews in Microbiology, 18, 175–190.CrossRefGoogle Scholar
  9. Commanday, F., & Macy, J. M. (1985). Effect of substrate nitrogen on lignin degradation by Pleurotus ostreatus. Archives of Microbiology, 142, 61–65.CrossRefGoogle Scholar
  10. Cullen, D. (1997). Recent advances on the molecular genetics of ligninolytic fungi. Journal of Biotechnology, 53, 273–289.CrossRefGoogle Scholar
  11. D'Souza, D. T., TiwarI, R., Sah, A. K., & Raghukumara, C. (2006). Enhanced production of laccase by a marine fungus during treatment of colored effluents and synthetic dyes. Enzyme and Microbial Technology, 38, 504–511.CrossRefGoogle Scholar
  12. D'Souza-Ticlo, D., Sharma, D., & Raghukumar, C. A. (2009). Thermostable metal-tolerant laccase with bioremediation potential from a marine derived fungus. Marine Biotechnology, 11(6), 725–737.CrossRefGoogle Scholar
  13. da Silva, M., Passarini, M. R. Z., Bonugli, R. C., & Sette, L. D. (2008). Cnidarian-derived filamentous fungi from Brazil: isolation, characterisation and RBBR decolourisation screening. Environmental Technology, 29, 1331–1339.CrossRefGoogle Scholar
  14. Elisashvili, V., Kachlishvili, E., Tsiklauri, N., Metreveli, E., Khardziani, T., & Agathos, S. N. (2008). Lignocellulose-degrading enzyme production by white-rot Basidiomycetes isolated from the forests of Georgia. World Journal of Microbiology and Biotechnology, 25, 331–339.CrossRefGoogle Scholar
  15. Enayatzamir, K., Tabandeh, F., Yakhchali, B., Alikhani, H. A., & Couto, S. R. (2009). Assessment of the joint effect of laccase and cellobiose dehydrogenase on the decolouration of different synthetic dyes. Journal of Hazardous Materials, 169, 176–181.CrossRefGoogle Scholar
  16. Fu, Y., & Viraraghavan, T. (2001). Fungal decolorization of dye wastewaters: a review. Bioresource Technology, 79, 251–262.CrossRefGoogle Scholar
  17. Hamid, M., & Khalil-ur-Rehman. (2009). Potential applications of peroxidases. Food Chemistry, 115, 1177–1186.CrossRefGoogle Scholar
  18. Hammel, K. E. (1992). Oxidation of aromatic pollutants by lignin degrading fungi and their extracellular peroxidases. Metal Ions in Biological Systems, 28, 41–60.Google Scholar
  19. Harms, H., Schlosser, D., & Wick, L. Y. (2011). Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Applied and Industrial Microbial, 9, 177–192.Google Scholar
  20. Hernández-Luna, C. E., Gutiérrez-Soto, G., & Salcedo-Martínez, S. M. (2008). Screening for decolorizing basidiomycetes in Mexico. World Journal of Microbiology and Biotechnology, 24, 465–473.CrossRefGoogle Scholar
  21. Junghanns, C., Krauss, G., & Schlosser, D. (2008). Potential of aquatic fungi derived from diverse freshwater environments to decolourise synthetic azo and anthraquinone dyes. Bioresource Technology, 99, 1225–1235.CrossRefGoogle Scholar
  22. Kaushik, P., & Malik, A. (2009). Fungal dye decolourization: recent advances and future potential. Environmental International, 35, 127–141.CrossRefGoogle Scholar
  23. Kiiskinen, L.-L., Rättö, M., & Kruus, K. (2004). Screening for novel laccase-producing microbes. Journal of Applied Microbiology, 97, 640–646.CrossRefGoogle Scholar
  24. Kirk, T. K., & Farrel, R. L. (1987). Enzymatic “combustion”: the microbial degradation of lignin. Annual Review of Microbiology, 41, 465–505.CrossRefGoogle Scholar
  25. Kohlmeyer, J., & Kohlmeyer, E. (1979). Marine mycology: the higher fungi. New York: Academic.Google Scholar
  26. Kuwahara, M., Glenn, J. K., Morgan, M. A., & Gold, M. H. (1984). Separation and characterization of two extracellular H2O2 dependent oxidases from ligninolytic cultures of Phanerochaete chrysosporium. FEBS Letters, 169, 247–250.CrossRefGoogle Scholar
  27. Leonowicz, A., Cho, N. S., Luterek, J., Wilkolazka, A., Wojtas-Wasilewska, M., Matuszewsha, A., Hofrichter, M., Wesernberg, D., & Rogalski, J. (2001). Fungal laccase: properties and activity on lignin. Journal of Basic Microbial, 41(4), 185–227.CrossRefGoogle Scholar
  28. Levin, L., Forchiassin, F., Ramos, A. M. (2002). Copper induction of lignin-modifying enzymes in the white-rot fungus Trametes trogii. Mycologia, 94(30), 377–383.Google Scholar
  29. Levin, L., Herrmann, C., & Papinutti, V. L. (2008). Optimization of lignocellulolytic enzyme production by the white-rot fungus Trametes trogii in solid-state fermentation using response surface methodology. Biochemical Engineering Journal, 39, 207–214.CrossRefGoogle Scholar
  30. Lewis, D. M. (1999). Coloration for the next century. Review of Progress in Coloration, 29, 23–28.CrossRefGoogle Scholar
  31. López, M. J., Guisado, G., Vargas-García, M. C., Suárez-Estrella, F., & Moreno, J. (2006). Decolourisation of industrial dyes by ligninolytic microorganisms isolated from composting environment. Enzyme and Microbial Technology, 40, 42–45.CrossRefGoogle Scholar
  32. Machado, K. M. G., Matheus, D. R., & Bononi, V. L. R. (2005). Ligninolytic enzymes production and Remazol Brilliant Blue R decolorization by tropical brazilian basidiomycetes fungi. Brazilian Journal of Microbiology, 36, 246–252.CrossRefGoogle Scholar
  33. Menezes, C. B., Bonugli-Santos, R. C., Miqueletto, P. B., Passarini, M. R. Z., Silva, C. H. D., Justo, M. R., Leal, R. R., Fantinatti-Garboggini, F., Oliveira, V. M., Berlinck, R. G. S., & Sette, L. D. (2010). Microbial diversity associated with algae, ascidians and sponges from the north coast of São Paulo state, Brazil. Microbiological Research, 165(6), 466–482.CrossRefGoogle Scholar
  34. Palmieri, G., Cennamo, G., & Sannia, G. (2005). Remazol Brilliant Blue R decolourisation by the fungus Pleurotus ostreatus and its oxidative enzymatic system. Enzyme and Microbial Technology, 36, 17–24.CrossRefGoogle Scholar
  35. Papinutti, L., & Forchiassin, F. (2007). Lignocellulolytic enzymes from Fomes sclerodermeus growing in solid-state fermentation. Journal of Food Engineering, 81, 54–59.CrossRefGoogle Scholar
  36. Papinutti, V. L., Diorio, L. A., & Forchiassin, F. (2003). Production of laccase and manganese peroxidase by Fomes sclerodermeus grown on wheat bran. Journal of Industrial Microbiology and Biotechnology, 30, 157–160.CrossRefGoogle Scholar
  37. Pointing, S. B., Jones, E. B. G., & Vrijmoed, L. L. P. (2000). Optimization of laccase production by Pycnoporus sanguineus in submerged liquid culture. Mycologia, 92, 139–144.CrossRefGoogle Scholar
  38. Raghukumar, C. (2008). Marine fungal biotechnology: an ecological perspective. Fungal Divers, 31, 19–35.Google Scholar
  39. 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, 189–206.CrossRefGoogle Scholar
  40. Reddy, C. A. (1995). The potential for white-rot fungi in the treatment of pollutants. Current Opinion in Biotechnology, 6, 320–328.CrossRefGoogle Scholar
  41. Sánchez-López, M. I., Vanhulle, S. F., Mertens, V., Guerra, G., Figueroa, S. H., Decock, C., Corbisier, A.-N., & Penninckx, M. J. (2008). Autochthonous white rot fungi from the tropical forest: potential of Cuban strains for dyes and textile industrial effluents decolourisation. African Journal of Biotechnology, 7(12), 1983–1990.Google Scholar
  42. Sette, L. D., de Oliveira, V. M., & Rodrigues, M. F. A. (2008). Microbial lignocellulolyticenzymes: industrial applications and future perspectives. Microbiology Australia, 29, 18–20.Google Scholar
  43. Tien, M., & Kirk, T. K. (1984). Lignin-degrading enzyme from Phanerochaete chrysosporium: purification, characterization and catalytic properties of unique H2O2 requiring oxygenase. Proceedings of the National Academy of Science, 81, 2280–2284.CrossRefGoogle Scholar
  44. Vanhulle, S., Enaud, E., Trovaslet, M., Billottet, L., Kneipe, L., Jiwan, J.-L. H., Corbisier, A.-M., & Marchand-Brynaert, J. (2008). Coupling occurs before breakdown during biotransformation of Acid Blue 62 by white rot fungi. Chemosphere, 70, 1097–1107.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. Vyas, B. R. M., & Molitoris, H. P. (1995). Involvement of an extracellular H2O2-dependent ligninolytic activity of the white rot fungus Pleurotus ostreatus in the decolorization of Remazol Brilliant Blue R. Applied and Environmental Microbiology, 61(11), 3919–3927.Google Scholar
  47. Wang, G. (2006). Diversity and biotechnological potential of the sponge-associated microbial consortia. Journal of Industrial Microbiology and Biotechnology, 33, 545–551.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Rafaella C. Bonugli-Santos
    • 1
    • 2
  • Lucia Regina Durrant
    • 1
  • Lara Durães Sette
    • 2
    • 3
  1. 1.Departamento de Ciência de Alimentos, Faculdade de Engenharia de AlimentosUniversidade Estadual de CampinasCampinasBrazil
  2. 2.Divisão de Recursos Microbianos-CPQBAUniversidade Estadual de CampinasCampinasBrazil
  3. 3.Departamento de Bioquímica e Microbiologia AplicadaIB/UNESPRio ClaroBrazil

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