Abstract
The current study investigates the potential for discolouration and degradation of Reactive Blue 19 and Reactive Black 5 textile dyes by endophytic fungi Phlebia sp. and Paecilomyces formosus as well as the potential cytotoxicity of products or by-products generated by the treatments in fish erythrocytes. It was observed at 30 days that both endophytes showed biodegradation activity with 0.1 g mL−1 of dyes. P. formosus showed highest extracellular and intracellular protein content levels after the 15th day, and Phlebia sp. stands out for production of extracellular laccase, indicating that this enzyme may be associated with the decolouration capacity. The dyes showed toxic effects in fishes at 0.01 g mL−1 concentration, resulting in the appearance of micronuclei in erythrocyte cells. When degraded dyes treated by endophytes were tested, the frequency of micronuclei reduced approximately 20%, indicating the effectiveness of these endophytic in the treatment of textile dyes with less environmental impact, thus indicating a potential for application of these fungi in bioremediation process.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Afzal, M., Shabir, G., Tahseen, R., Islam, E. U., Iqbal, S., Khan, Q. M., & Khalid, Z. M. (2014). Endophytic Burkholderia sp. strain PsJN improves plant growth and phytoremediation of soil irrigated with textile effluent. CLEAN–Soil, Air, Water, 42(9), 1304–1310.
Al-Sabti, K. (2000). Chlorotriazine reactive azo red 120 textile dye induces micronuclei in fish. Ecotoxicology and Environmental Safety, 47(2), 149–155.
Avni, P., & Jagruti, B. (2016). Determination of genotoxic effect of azo dye CI RR 120 on fish Catla catla. Biotechnological Research, 2(2), 77–80.
Azevedo, J. L., & Araújo, W. L. (2007). Diversity and applications of endophytic fungi isolated from tropical plants. In B. N. Ganguli & S. K. Deshmukh (Eds.), Fungi: multifaceted microbes (pp. 189–207). New Delhi: Anamaya Publishers.
Banat, I. M., Nigam, P., Singh, D., & Marchant, R. (1996). Microbial decolorization of textile-dyecontaining effluents: a review. Bioresource Technology, 58(3), 217–227.
Bisschops, I., & Spanjers, H. (2003). Literature review on textile wastewater characterization. Environmental Technology, 24(11), 1399–1411.
Bongiorno, V. A., Rhoden, S. A., Garcia, A., Polonio, J. C., Azevedo, J. L., Pereira, J. O., & Pamphile, J. A. (2016). Genetic diversity of endophytic fungi from Coffea arabica cv. IAPAR-59 in organic crops. Annals of Microbiology, 66, 855–865.
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1–2), 248–254.
Cañamares, M. V., Reagan, D. A., Lombardi, J. R., & Leona, M. (2014). TLC-SERS of mauve, the first synthetic dye. Journal of Raman Spectroscopy, 45(11–12), 1147–1152.
Chung, K. T. (2016). Azo dyes and human health: a review. Journal of Environmental Science and Health, Part C, 34(4), 233–261.
Eggert, C., Temp, U., & Eriksson, K. E. L. (1996). The ligninolytic system of the white rot fungus Pycnoporus cinnabarinus: purification and characterization of the laccase. Applied and Environmental Microbiology, 62(4), 1151–1158.
Gill, P. K., Arora, D. S., & Chander, M. (2002). Biodecolourization of azo and triphenylmethane dyes by Dichomitus squales and Phlebia spp. Journal of Industrial Microbiology and Biotechnology, 28(4), 201–203.
Grisolia, C. K., Rivero, C. L. G., Starling, F. L. R. M., Silva, I. C. R., Barbosa, A. C., & Dorea, J. G. (2009). Profile of micronucleus frequencies and DNA damage in different species of fish in a eutrophic tropical lake. Genetics and Molecular Biology, 32(1), 138–143.
Hooftman, R. N., & De Raat, W. K. (1982). Induction of nuclear anomalies (miconuclei) in the peripheral blood erythrocytes of the eastern mudminnow Umbra pygmaea by ethyl methanesulphonate. Mutation Research Letters, 104(1), 147–152.
Hunger, K., Gregory, P., Miederer, P., Berneth, H., Heid, C., & Mennicke, W. (2004). Important chemical chromophores of dye classes. In K. Hunger (Ed.), Industrial Dyes: Chemistry, Properties, Applications (pp. 13–112). Weinheim: Wiley-VCH Verlag GmbH & Co. KGaA.
Kamida, H., & Durrant, L. R. (2005). Biodegradation of textile effluents by Pleurotus sajor-caju. Quimica Nova, 28(4), 629–632.
Kaur, R., & Dua, A. (2016). Fish liver and gill cells as cytogenotoxic indicators in assessment of water quality. Environmental Science and Pollution Research, 23(18), 18892–18900.
Kaushik, P., & Malik, A. (2009). Fungal dye decolourization: recent advances and future potential. Environment International, 35(1), 127–141.
Khatri, A., Peerzada, M. H., Mohsin, M., & White, M. (2015). A review on developments in dyeing cotton fabrics with reactive dyes for reducing effluent pollution. Journal of Cleaner Production, 87, 50–57.
Kusari, S., Hertweck, C., & Spiteller, M. (2012). Chemical ecology of endophytic fungi: origins of secondary metabolites. Chemistry & Biology, 19(7), 792–798.
Lima, R. O. A., Bazo, A. P., Salvadori, D. M. F., Rech, C. M., Oliveira, D. P., & Umbuzeiro, G. A. (2007). Mutagenic and carcinogenic potential of a textile azo dye processing plant that impacts a drinking water. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 626(1), 53–60.
Ma, Y., Rajkumar, M., Zhang, C., & Freitas, H. (2016). Beneficial role of bacterial endophytes in heavy metal phytoremediation. Journal of Environmental Management, 174, 14–25.
Machado, K. M. G., & Matheus, D. R. (2006). Biodegradation of Remazol Brilliant Blue R by ligninolytic enzymatic complex produced by Pleurotus ostreatus. Brazilian Journal of Microbiology, 37(4), 468–473.
Manai, I., Miladi, B., El Mselmi, A., Smaali, I., Hassen, A. B., Hamdi, M., & Bouallagui, H. (2016a). Industrial textile effluent decolourization in stirred and static batch cultures of a new fungal strain Chaetomium globosum IMA1 KJ472923. Journal of Environmental Management, 170, 8–14.
Manai, I., Miladi, B., El Mselmi, A., Hamdi, M., & Bouallagui, H. (2016b). Improvement of activated sludge resistance to shock loading by fungal enzyme addition during textile wastewater treatment. Environmental Technology, 1–11.
Mcmullan, G., Mehan, C., Conneely, A., Kirby, N., Robinson, T., Nigam, P., Banat, I. M., Marchant, R., & Smyth, W. F. (2001). Microbial decolourisation and degradation of textile dyes. Applied Microbiology and Biotechnology, 56(1–2), 81–87.
Meehan, C., Banat, I. M., Mcmullan, G., Nigam, P., Amyth, F., & Marchant, R. (2006). Descolorization of Remazol Black B using a thermotolerant yeast, Kluyveromyces marxianus IMB3. Environment International, 26(1), 75–79.
Niebisch, C. H., Malinowski, A. K., Schadeck, R., Mitchell, D. A., Kava-Cordeiro, V., & Paba, J. (2010). Decolorization and biodegradation of reactive blue 220 textile dye by Lentinus crinitus extracelular extract. Journal of Hazardous Materials, 180(1), 316–322.
Orlandelli, R. C., Alberto, R. N., Rubin-Filho, C. J., & Pamphile, J. A. (2012). Diversity of endophytic fungal community associated with Piper hispidum (Piperaceae) leaves. Genetics and Molecular Research, 11(2), 1575–1585.
Pamphile, J. A., & Azevedo, J. L. (2002). Molecular characterization of endophytic strains of Fusarium verticillioides (=Fusarium moniliforme) from maize (Zea mays L). World Journal of Microbiology and Biotechnology, 18(5), 391–396.
Polonio, J.C., Polli, A.D., Azevedo, J.L., & Pamphile, J.A. (2016). RNA applications for endophytic research. Genetics and Molecular Research: GMR 15(3), gmr.15038879.
Raeder, U., & Broda, P. (1985). Rapid preparation of DNA from filamentous fungi. Letters in Applied Microbiology, 1(1), 17–20.
Samsin, R. A., Houbraken, J., Varga, J., & Frisvad, J. C. (2009). Polyphasic taxonomy of the heat resistant ascomycete genus Byssochlamys and its Paecilomyces anamorphs. Persoonia-Molecular Phylogeny and Evolution of Fungi, 22(1), 14–27.
Saotome, K., & Hayashi, M. (2003). Application of a sea urchin micronucleus assay to monitoring aquatic pollution: influence of sample osmolality. Mutagenesis, 18(1), 73–76.
Silva, M. C., Corrêa, A. D., Torres, J. A., & Amorim, M. T. S. P. (2012). Descoloration of industrial dyes and simulated textile effluents dyes by turnip peroxidase. Química Nova, 35(5), 889–894.
Singh, R., Singh, P., & Sharma, R. (2014). Microorganism as a tool of bioremediation technology for cleaning environment: a review. Proceedings of the International Academy of Ecology and Environmental Sciences, 4(1), 1–6.
Solís, M., Solís, A., Perez, H. I., Manjarrez, N., & Flores, M. (2012). Microbial decolourization of azo dyes: a review. Process Biochemistry, 47(12), 1723–1748.
Urra, J., Sepúlveda, L., Contreras, E., & Palma, C. (2006). Screening of static culture and comparison of batch and continuous culture for the textile dye biological decolorization by Phanerochaete chrysosporium. Brazilian Journal of Chemical Engineering, 23(3), 281–290.
Van Den Ende, A. H. G., & De Hoog, G. S. (1999). Variability and molecular diagnostics of the neurotropic species Cladophialophora bantiana. Studies in Mycology, 43, 151–162.
Verma, S. K., Kumar, A., Lal, M., & Debnath, M. (2015). Biodegradation of synthetic dye by endophytic fungal isolate in Calotropis procera root. International Journal of Applied Sciences and Biotechnology, 3(3), 373–380.
Von Ledebur, M., & Schmid, W. (1973). The micronucleus test methodological aspects. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, 19(1), 109–117.
Wang, C., Yediler, A., Lienert, D., Wang, Z., & Kettrup, A. (2003). Ozonation of an azo dye C.I. Remazol Black 5 and toxicological assessment of its oxidation products. Chemosphere, 52(7), 1225–1232.
Welham, A. (2000). The theory of dyeing (and the secret of life). Journal of the Society of Dyers and Colourists, 116(5), 140–143.
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), 161–187.
White Jr., J. F., Morrow, A. C., & Morgan-Jones, G. (1990). Endophyte-host associations in forage grasses. XII. A fungal endophyte of Trichachne insularis belongin to Psedocercosporella. Mycologia, 82, 218–226.
Rhoden, S. A., Garcia, A., Rubin-Filho, C. J., Azevedo, J. L., & Pamphile, J. A. (2012). Phylogenetic diversity of endophytic leaf fungus isolates from the medicinal tree Trichilia elegans (Meliaceae). Genetics Molecular Research, 11(3), 2513–2522.
Acknowledgements
The authors thank the Complexo Central de Apoio à Pesquisa (COMCAP/UEM), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarship and the CNPq (311534/2014-7; 447265/2014-8) and Fundação Araucária (FA) (276/2014) for financial support.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical approval
All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.
Rights and permissions
About this article
Cite this article
Bulla, L.M.C., Polonio, J.C., Portela-Castro, A.L.d. et al. Activity of the endophytic fungi Phlebia sp. and Paecilomyces formosus in decolourisation and the reduction of reactive dyes’ cytotoxicity in fish erythrocytes. Environ Monit Assess 189, 88 (2017). https://doi.org/10.1007/s10661-017-5790-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10661-017-5790-0