Abstract
In consideration of the hazards associated with the presence of the textile azo-dye and their biotransformation products in the environment, the goal of this work was to study bioremediation process by the yeast strain Pichia kudriavzevii CR-Y103 related to the ability to degrade and detoxify the sulfonated Reactive Orange 16 azo-dye. In experimental conditions, the optimal inoculum/dye concentration ratio required for complete decolorization (100%) of culture medium and biomass within 24 h has been 1 g L−1 yeast cell (dry weight)/50 mg L−1 Reactive Orange 16. In the presence of 400 mg L−1 of Reactive Orange 16 (RO16), 95% of the dye was removed after 72 h of incubation. Also, the yeast strain could decolorize other eight textile dyes (56.48–99.98% decolorization within 24 h). NADH-DCIP reductase and azo reductase activities were significantly increased (ca. 5.4 times and ca. 37 times, respectively) during the decolorization process. UV-VIS spectra, high-performance liquid chromatography (HPLC), and Fourier transform infrared spectroscopy (FTIR) analysis confirmed the presence of new biotransformation products in extracted metabolites, highlighting the partial biodegradation of the dye by the new yeast isolate. The phytotoxicity evaluation strongly supported the decreased toxicity of biodegraded products as minor inhibition on germination (%), root and shoots elongation of T. pratense L. and T. aestivum L. seedlings. Increasing of mitotic index value and decreasing the frequency of chromosomal aberrations in tested plant meristem cells treated with biodegraded products, compared with RO16 treatment (500 ppm), confirmed their slightly toxic nature. A cell viability assay also confirmed the reduced toxicity of biodegraded products on healthy monkey kidney cells (Vero cells).
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alinsafi, A., Khemis, M., Pons, M. N., Leclerc, J. P., Yaacoubi, A., Benhammou, A., & Nejmeddine, A. (2005). Electro-coagulation of reactive textile dyes and textile wastewater. Chemical Engineering and Processing: Process Intensification, 44(4), 461–470. https://doi.org/10.1016/j.cep.2004.06.010.
Baldrian, P., & Snajdr, J. (2006). Production of ligninolytic enzymes by litter-decomposing fungi and their ability to decolorize synthetic dyes. Enzyme and Microbial Technology, 39(5), 1023–1029. https://doi.org/10.1016/j.enzmictec.2006.02.011.
Banat, I. M., Nigam, P., Singh, D., & Marchant, R. (1996). Microbial decolorization of textile-dye-containing effluents: a review. Bioresource Technology, 58, 217–227. https://doi.org/10.1016/S0960-8524(96)00113-7.
Bedekar, P. A., Saratale, R. G., Saratale, G. D., & Govindwar, S. P. (2014). Oxidative stress response in dye degrading bacterium Lysinibacillus sp. RGS exposed to Reactive Orange 16, degradation of RO16 and evaluation of toxicity. Environmental Science and Pollution Research International, 21(18), 11075–11085. https://doi.org/10.1007/s11356-014-3041-2.
Bourikas, K., Stylidi, M., Kondarides, D. I., & Verykios, X. E. (2005). Adsorption of Acid Orange 7 on the surface of titanium dioxide. Langmuir, 21, 9222–9923. https://doi.org/10.1021/la051434g.
Cann, A. J. (2002). Maths from scratch for biologists. England: Wiley.
Das, N., & Charumathi, D. (2012). Remediation of synthetic dyes from wastewater using yeast—an overview. Indian Journal of Biotechnology, 11, 369–380 http://nopr.niscair.res.in/bitstream/ 123456789/15693/1/IJBT%2011.
Das, D., Charumathi, D., & Das, N. (2010). Combined effects of sugarcane bagasse extract and synthetic dyes on the growth and bioaccumulation properties of Pichia fermentans MTCC 189. Journal of Hazardous Materials, 183(1–3), 497–505. https://doi.org/10.1016/j.jhazmat.2010.07.051.
Deivasigamani, C., & Das, N. (2011). Biodegradation of Basic Violet 3 by Candida krusei isolated from textile wastewater. Biodegradation, 22(6), 1169–1180. https://doi.org/10.1007/s10532-011-9472-2.
El-Sharoud, W. M., Belloch, C., Peris, D., & Querol, A. (2009). Molecular identification of yeasts associated with traditional Egyptian dairy products. Journal of Food Science, 74(7), M341–M346. https://doi.org/10.1111/j.1750-3841.2009.01258.x.
Feng, C., Fang-yan, C., & Yu-bin Isolation, T. (2014). Identification of a halotolerant Acid Red B degrading strain and its decolorization performance. APCBEE Procedia, 9, 131–139. https://doi.org/10.1016/j.apcbee.2014.01.024.
Gomes, L., Miwa, D. W., Malpass, G. R. P., & Motheo, A. J. (2011). Electrochemical degradation of the dye reactive orange 16 using electrochemical flow-cell. Journal of the Brazilian Chemical Society, 22(7), 1299–1306. https://doi.org/10.1590/S0103-50532011000700015.
Gönen, F., & Aksu, Z. (2009). Predictive expressions of growth and Remazol Turquoise Blue-G reactive dye bioaccumulation properties of C. utilis. Enzyme and Microbial Technology, 45(1), 15–21. https://doi.org/10.1016/j.enzmictec.2009.03.006.
Grant, W. F. (1994). The present status of higher plant bioassays for the detection of environmental mutagens. Mutation Research: Fundamental and Molecular Mechanisms of Mutagenesis, 310(2), 175–185. https://doi.org/10.1016/0027-5107(94)90112-0.
Hatvani, N., & Mécs, I. (2001). Production of laccase and manganese peroxidase by Lentinus elodes on malt-containing by-product of the brewing process. Process Biochemistry, 37(5), 491–496. https://doi.org/10.1016/S0032-9592(01)00236-9.
Herrmann, D., Boller, B., Studer, B., Widmer, F., & Kölliker, R. (2008). Improving persistence in red clover: insights from QTL analysis and comparative phenotypic evaluation. Crop Science, 48(1), 269–277. https://doi.org/10.2135/cropsci2007.03.0143.
Jadhav, J. P., & Govindwar, S. P. (2006). Biotransformation of malachite green by Saccharomyces cerevisiae MTCC 463. Yeast, 23(4), 315–323. https://doi.org/10.1002/yea.1356.
Jadhav, J. P., Parshetti, G. K., Kalme, S. D., & Govindwar, S. P. (2007). Decolourization of azo dye methyl red by Saccharomyces cerevisiae. Chemosphere, 68, 394–400. https://doi.org/10.1016/j.chemosphere.2006.12.087.
Jadhav, S. V., Kalme, S. D., & Govindwar, S. P. (2008). Biodegradation of methyl red by Galactomyces geotrichum MTCC 1360. International Biodeterioration & Biodegradation, 62(2), 135–142. https://doi.org/10.1016/j.ibiod.2007.12.010.
Jadhav, S. U., Ghodake, G. S., Telke, A. A., Tamboli, D. P., & Govindwar, S. P. (2009). Degradation and detoxification of disperse dye scarlet RR by Galactomyces geotrichum MTCC 1360. Journal of Microbiology and Biotechnology, 19(4), 409–415. https://doi.org/10.4014/jmb.0804.294.
Jafari, N., Kasra-Kermanshahi, R., & Soudi, M. R. (2013). Screening, identification and optimization of a yeast strain, Candida palmioleophila JKS4, capable of azo dye decolorization. Iranian Journal of Microbiology, 5(4), 434–440 http://ijm.tums.ac.ir/index.php/ijm/article/Download/550/371.
Jafari, N., Soudi, M. R., & Kasra-Kermanshahi, R. (2014). Biodecolorization of textile azo dyes by isolated yeast from activated sludge: Issatchenkia orientalis JKS6. Annals of Microbiology, 64(2), 475–482. https://doi.org/10.1007/s13213-013-0677-y.
Junnarkar, N., Murty, D. S., Bhatt, N. S., & Madamwar, D. (2006). Decolorization of diazo dye Direct Red 81 by a novel bacterial consortium. World Journal of Microbiology and Biotechnology, 22(2), 163–168. https://doi.org/10.1007/s11274-005-9014-3.
Kao, K. N. (1975). A chromosomal staining method for cultured cells. In O. L. Gamborg & L. R. Wetter (Eds.), Plant tissue culture methods (pp. 63–64). Saskatoon: National Research Council, Prairie Regional Laboratory.
Keharia, H., & Madamwar, D. (2003). Bioremediation concepts for treatment of dye containing wastewater: a review. Indian Journal of Experimental Biology, 41(9), 1068–1075.
Kurtzman, C. P., Fell, J. W., Boekhout, T., & Robert, V. (2011). Methods for isolation, phenotypic characterization and maintenance of yeasts. In C. P. Kurtzman, J. W. Fell, & T. Boekhout (Eds.), The yeasts, a taxonomic study (5th ed., pp. 87–110). Amsterdam: Elsevier.
Lade, H. S., Waghmode, T. R., Kadam, A. A., & Govindwar, S. P. (2012). Enhanced biodegradation and detoxification of disperse azo dye Rubine GFL and textile industry effluent by defined fungal-bacterial consortium. International Biodeterioration and Biodegradation, 72, 94–107. https://doi.org/10.1016/j.ibiod.2012.06.001.
Lade, H., Kadam, A., Paul, D., & Govindwar, S. (2015). Biodegradation and detoxification of textile azo dyes by bacterial consortium under sequential microaerophilic/aerobic processes. EXCLI Journal, 14, 158–174. https://doi.org/10.17179/excli2014-642.
Lucas, M. S., Amaral, C., Sampaio, A., Peres, J. A., & Dias, A. A. (2006). Biodegradation of the diazo dye Reactive Black 5 by a wild isolate of Candida oleophila. Enzyme and Microbial Technology, 39(1), 51–55. https://doi.org/10.1016/j.enzmictec.2005.09.004.
Ma, L., Zhuo, R., Liu, H., Yu, D., Jiang, M., Zhang, X., & Yang, Y. (2014). Efficient decolorization and detoxification of the sulfonated azo dye Reactive Orange 16 and simulated textile wastewater containing reactive Orange 16 by the white-rot fungus Ganoderma sp En3 isolated from the forest of Tzu-chin Mountain in China. Biochemical Engineering Journal, 82, 1–9. https://doi.org/10.1016/j.bej.2013.10.015.
McMullan, G., Meehan, C., Conneely, A., Kirby, N., Robinson, T., Nigam, P., Banat, I. M., Marchant, R., & Smyth, W. F. (2001). Microbial decolorization and degradation of textile dyes. Applied Microbiology and Biotechnology, 56(1–2), 81–87. https://doi.org/10.1007/s002530000587.
Meehan, C., Banat, I. M., McMullan, G., Nigam, P., Smyth, F., & Marchant, R. (2000). Decolourization of Remazol Black-B using a thermotolerant yeast, Kluyveromyces marxianus IMB3. Environment International, 26(1–2), 75–79. https://doi.org/10.1016/S0160-4120(00)00084-2.
Mosmann, T. (1983). Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunological Methods, 65, 55–63. https://doi.org/10.1016/0022-1759(83)90303-4.
Novotný, C., Svobodova, K., Erbanova, P., Cajthaml, T., Kasinath, A., Lang, E., & Sasek, V. (2004). Ligninolytic fungi in bioremediation: extracellular enzyme production and degradation rate. Soil Biology and Biochemistry, 36(10), 1545–1551. https://doi.org/10.1016/j.soilbio.2004.07.019.
Novotný, C., Dias, N., Kapanen, A., Malachová, K., Vándrovcová, M., Itävaara, M., & Lima, N. (2006). Comparative use of bacterial, algal and protozoan tests to study toxicity of azo- and anthraquinone dyes. Chemosphere, 63(9), 1436–1442. https://doi.org/10.1016/j.chemosphere.2005.10.002.
Ostergren, G., & Heneen, W. K. (1962). A squash technique for chromosome morphological studies. Hereditas, 48, 332–341. https://doi.org/10.1111/j.1601-5223.1962.tb01817.x.
Pajot, H. F., de Figueroa, L. I. C., & Fariña, J. I. (2007). Dye-decolorizing activity in isolated yeasts from the ecoregion of Las Yungas (Tucumán, Argentina). Enzyme and Microbial Technology, 40, 1503–1511. https://doi.org/10.1016/j.enzmictec.2006.10.038.
Pajot, H. F., Martorell, M. M., & de Figueroa, L. I. C. (2014). Ecology of dye decolorizing yeasts. In A. Alvarez & M. Polti (Eds.), Bioremediation in Latin America. Cham: Springer. https://doi.org/10.1007/978-3-319-05738-5_14.
Phugare, S. S., Kalyani, D. C., Patil, A. V., & Jadhav, J. P. (2011). Textile dye degradation by bacterial consortium and subsequent toxicological analysis of dye and dye metabolites using cytotoxicity, genotoxicity and oxidative stress studies. Journal of Hazardous Materials, 186, 713–723. https://doi.org/10.1016/j.jhazmat.2010.11.049.
Prasad, A. S., & Rao, K. V. (2013). Aerobic biodegradation of azo dye by Bacillus cohnii MTCC 3616; an obligately alkaliphilic bacterium and toxicity evaluation of metabolites by different bioassay systems. Applied Microbiology and Biotechnology, 97(16), 7469–7481. https://doi.org/10.1007/s00253-012-4492-3.
Puvaneswari, N., Muthukrishnan, J., & Gunasekaran, P. (2006). Toxicity assessment and microbial degradation of azo-dye. Indian Journal of Experimental Biology, 44, 618–626.
Qu, Y., Cao, X., Ma, Q., Shi, S., Tan, L., Li, X., Zhou, H., Zhang, X., & Zhou, J. (2012). Aerobic decolorization and degradation of Acid Red B by a newly isolated Pichia sp. TCL. Journal of Hazardous Materials, 223–224, 31–38. https://doi.org/10.1016/j.jhazmat.2012.04.034.
Ramalho, P. A., Scholze, H., Cardoso, M. H., Ramalho, M. T., & Oliveira-Campos, A. M. (2002). Improved conditions for the aerobic reductive decolorization of azo dyes by Candida zeylanoides. Enzyme and Microbial Technology, 31(6), 848–854. https://doi.org/10.1016/S0141-0229(02)00189-8.
Ramalho, P. A., Cardoso, M. H., Cavaco-Paulo, A., & Ramalho, M. T. (2004). Characterization of azo reduction activity in a novel ascomycete yeast strain. Applied and Environmental Microbiology, 70(4), 2279–2288. https://doi.org/10.1128/AEM.70.4.2279-2288.2004.
Ramalho, P. A., Paiva, S., Cavaco-Paulo, A., Casal, M., Cardoso, M. H., & Ramalho, M. T. (2005). Azo reductase activity of intact Saccharomyces cerevisiae cells is dependent on the Fre1p component of plasma membrane ferric reductase. Applied and Environmental Microbiology, 71(7), 3882–3888. https://doi.org/10.1128/AEM.71.7.3882-3888.2005.
Sahasrabudhe, M. M., & Pathade, G. R. (2011). Biodegradation of sulphonated azo dye C.I. reactive orange 16 by Enterococcus faecalis strain YZ 66. European Journal of Experimental Biology, 1(1), 163–173.
Sahasrabudhe, M. M., & Pathade, G. R. (2013). Biodegradation of azo dye C.I. Reactive Orange 16 by an actinobacterium Georgenia sp. CC-NMPT-T3. International Journal of Advanced Research, 1(7), 91–99.
Saitou, N., & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4), 406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454.
Salokhe, M. D., & Govindwar, S. P. (1999). Effect of carbon source on the biotransformation enzymes in Serratia marcescens. World Journal of Microbiology and Biotechnology, 15, 259–263. https://doi.org/10.1023/A:1008875404889.
Saratale, R. G., Saratale, G. D., Chang, J. S., & Govindwar, S. P. (2009). Decolorization and biodegradation of textile dye Navy blue HER by Trichosporon beigelii NCIM-3326. Journal of Hazardous Materials, 166(2–3), 1421–1428. https://doi.org/10.1016/j.jhazmat.2008.12.068.
Shaul, G. M., Holdsworth, T. J., Dempsey, C. R., & Dostal, K. A. (1991). Fate of water soluble azo dyes in the activated sludge process. Chemosphere, 22(1–2), 107–119. https://doi.org/10.1016/0045-6535(91)90269-J.
Shobana, S., & Thangam, E. B. (2012). Biodegradation and decolorization of Reactive Orange 16 by Nocardiopsis alba soil isolate. Journal of Bioremediation & Biodegradation, 3, 155. https://doi.org/10.4172/2155-6199.1000155.
Singh, L., & Singh, V. P. (2015). Textile dyes degradation: a microbial approach for biodegradation of pollutants. In S. N. Singh (Ed.), Microbial degradation of synthetic dyes in wastewaters, environmental science and engineering (pp. 187–204). Switzerland: Springer-Verlag.
Socrates, G. (2004). Infrared and Raman characteristic group frequencies. Tables and charts (3rd ed.). England: Wiley.
Stylidi, M., Kondarides, D. I., & Verykios, X. E. (2003). Pathways of solar light-induced photocatalytic degradation of azo dyes in aqueous TiO2 suspensions. Applied Catalysis B: Environmental, 40(4), 271–286. https://doi.org/10.1016/S0926-3373(02)00163-7.
Tamura, K., Nei, M., & Kumar, S. (2004). Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences of the United States of America, 101, 11030–11035. https://doi.org/10.1073/pnas.0404206101.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30(12), 2725–2729. https://doi.org/10.1093/molbev/mst197.
Tan, L., Ning, S., Zhang, X., & Shi, S. (2013). Aerobic decolorization and degradation of azo dyes by growing cells of a newly isolated yeast C. tropicalis TL-F1. Bioresource Technology, 138, 307–313. https://doi.org/10.1016/j.biortech.2013.03.183.
Tan, L., He, M., Song, L., Fu, X., & Shi, S. (2016). Aerobic decolorization, degradation and detoxification of azo dyes by a newly isolated salt-tolerant yeast Scheffersomyces spartinae TLHS-SF1. Bioresource Technology, 203, 287–294. https://doi.org/10.1016/j.biortech.2015.12.058.
Telke, A. A., Kalyani, D. C., Dawkar, V. V., & Govindwar, S. P. (2009). Influence of organic and inorganic compounds on oxidoreductive decolorization of sulfonated azo dye CI Reactive Orange 16. Journal of Hazardous Materials, 172, 298–309. https://doi.org/10.1016/j.jhazmat.2009.07.008.
Trama, B., Santos Fernandes, J. D., Labuto, G., Franco de Olivera, J. C., Viana-Niero, C., Pascon, R. C., & Vallim, M. A. (2014). The evaluation of bioremediation potential of a yeast collection isolated from composting. Advances in Microbiology, 4, 796–807. https://doi.org/10.4236/aim.2014.412088.
Truta, E., Mihai, C., Gherghel, D., & Vochita, G. (2014). Assessment of the cytogenetic damage induced by chromium short-term exposure in root tip meristems of barley seedlings. Water, Air, and Soil Pollution, 225, 1933. https://doi.org/10.1007/s11270-014-1933-x.
Van der Zee, F. P., Lettinga, G., & Field, J. A. (2001). Azo dye decolorization by anaerobic granular sludge. Chemosphere, 44, 1169–1176. https://doi.org/10.1016/S0045-6535(00)00270-8.
Vitor, V., & Corso, C. R. (2008). Decolorization of textile dye by Candida albicans isolated from industrial effluents. Journal of Industrial Microbiology and Biotechnology, 35(11), 1353–1357. https://doi.org/10.1007/s10295-008-0435-5.
White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequence of fungal ribosomal RNA genes for phylogenetics. In M. A. Innes, D. H. Gelfan, J. J. Sninsky, & T. J. White (Eds.), PCR protocols: a guide to methods and applications (pp. 315–322). California: San Diego.
Yang, Q., Tao, L., Yang, M., & Zhang, H. (2008). Effects of glucose on the decolourization of Reactive Black 5 by yeast isolates. Journal of Environmental Sciences, 20(1), 105–108. https://doi.org/10.1016/S1001-0742(08)60016-9.
Yu, Z., & Wen, X. (2005). Screening and identification of yeasts for decolorizing synthetic dyes in industrial wastewater. International Biodeterioration & Biodegradation, 56(2), 109–114. https://doi.org/10.1016/j.ibiod.2005.05.006.
Acknowledgments
The authors are grateful to Dr. Liliana Sfichi Duke for revising the English text and language editing assistance.
Funding
This work was supported financially by Romanian Ministry of Research and Innovation (Program NUCLEU/project no. PN 16190301).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
ESM 1
(PDF 813 kb)
Rights and permissions
About this article
Cite this article
Rosu, C.M., Avadanei, M., Gherghel, D. et al. Biodegradation and Detoxification Efficiency of Azo-Dye Reactive Orange 16 by Pichia kudriavzevii CR-Y103. Water Air Soil Pollut 229, 15 (2018). https://doi.org/10.1007/s11270-017-3668-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11270-017-3668-y