Abstract
Plants and bacterial consortium of Portulaca grandiflora and Pseudomonas putida showed complete decolorization of a sulfonated diazo dye Direct Red 5B within 72 h, while in vitro cultures of P. grandiflora and P. putida independently showed 92 and 81 % decolorization within 96 h, respectively. A significant induction in the activities of lignin peroxidase, tyrosinase, 2,6-dichlorophenol indophenol reductase and riboflavin reductase was observed in the roots of P. grandiflora during dye decolorization; whereas, the activities of laccase, veratryl alcohol oxidase and 2,6-dichlorophenol indophenol reductase were induced in the cells of P. putida. Plant and bacterial enzymes in the consortium gave an enhanced decolorization of Direct Red 5B synergistically. The metabolites formed after dye degradation analyzed by UV–Vis spectroscopy, Fourier transformed infrared spectroscopy and high performance liquid chromatography confirmed the biotransformation of Direct Red 5B. Differential fate of metabolism of Direct Red 5B by P. grandiflora, P. putida and their consortium were proposed with the help of gas chromatography–mass spectroscopy analysis. P. grandiflora metabolized the dye to give 1-(4-diazenylphenyl)-2-phenyldiazene, 7-(benzylamino) naphthalene-2-sulfonic acid, 7-aminonaphthalene-2-sulfonic acid and methylbenzene. P. putida gave 4-hydroxybenzenesulfonic acid and 4-hydroxynaphthalene-2-sulfonic acid and benzamide. Consortium showed the formation of benzenesulfonic acid, 4-diazenylphenol, 6-aminonaphthalen-1-ol, methylbenzene and naphthalen-1-ol. Consortium achieved an enhanced and efficient degradation of Direct Red 5B. Phytotoxicity study revealed the nontoxic nature of metabolites formed after parent dye degradation. Use of such combinatorial systems of plant and bacteria could prove to be an effective and efficient strategy for the removal of textile dyes from soil and waterways.
References
Arthur EL, Rice PJ, Rice PJ, Anderson TA, Baladi SM, Henderson KLD, Coats JR (2005) Phytoremediation—an overview. Crit Rev Plant Sci 24:109–122. doi:10.1080/07352680590952496
Aubert S, Schwitzguebel JP (2004) Screening of plant species for the phytotreatment of wastewater containing sulphonated anthraquinones. Water Res 38:3569–3575. doi:10.1016/j.watres.2004.04.057
Bafana A, Jain M, Agrawal G, Chakrabarti T (2009) Bacterial reduction in genotoxicity of Direct Red 28 dye. Chemosphere 74:1404–1406. doi:10.1016/j.chemosphere.2008.11.043
Brandt R, Merkl N, Schultze-Kraft R, Infante C, Broll G (2006) Potential of vetiver (Vetiveria zizanioides (L.) Nash) for phytoremediation of petroleum hydrocarbon-contaminated soils in Venezuela. Int J Phytorem 8:273–284. doi:10.1080/15226510600992808
Carias CC, Novais JM, Martins-Dias S (2007) Phragmites australis peroxidases role in the degradation of an azo dye. Water Sci Technol 56:263–269. doi:10.2166/wst.2007.526
Chivukula M, Renganathan V (1995) Phenolic azo dye oxidation by laccase from Pyricularia oryza. Appl Environ Microb 61:4374–4377
Davies LC, Carias CC, Novais JM, Martins-Dias S (2005) Phytoremediation of textile effluents containing azo dye by using Phragmites australis in a vertical flow constructed intermittent feeding constructed wetland. Ecol Eng 25:594–605. doi:10.1016/j.ecoleng.2005.07.003
Escalante-Espinosa E, Gallegos-Martínez ME, Favela-Torres E, Gutiérrez-Rojas M (2005) Improvement of the hydrocarbon phytoremediation rate by Cyperus laxus Lam. inoculated with a microbial consortium in a model system. Chemosphere 59:405–413. doi:10.1016/j.chemosphere.2004.10.034
Gharbani P, Tabatabaii SM, Mehrizad A (2008) Removal of Congo red from textile wastewater by ozonation. Int J Environ Sci Tech 5:495–500
Ghodake GS, Telke AA, Jadhav JP, Govindwar SP (2009) Potential of Brassica juncea in order to treat textile effluent contaminated sites. Int J Phytorem 11:297–312. doi:10.1080/15226510802429518
Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374. doi:10.1016/j.biotechadv.2010.02.001
Govindwar SP, Kagalkar AN (2010) Phytoremediation technologies for the removal of textile dyes: An overview and future prospectus. Nova Science Publishers Inc., New York
Jadhav UU, Dawkar VV, Tamboli DP, Govindwar SP (2009) Purification and characterization of veratryl alcohol oxidase from Comamonas sp. UVS and its role in decolorization of textile dyes. Biotechnol Bioprocess Eng 14:3369–3376. doi:10.1007/s12257-008-0300-4
Kabra AN, Khandare RV, Kurade MB, Govindwar SP (2011a) Phytoremediation of a sulphonated azo dye Green HE4B by Glandularia pulchella (Sweet) Tronc. (Moss Verbena). Environ Sci Pollut Res 18:1360–1373. doi:10.1007/s11356-011-0491-7
Kabra AN, Khandare RV, Waghmode TR, Govindwar SP (2011b) Differential fate of metabolism of a sulfonated azo dye Remazol Orange 3R by plants Aster amellus Linn., Glandularia pulchella (Sweet) Tronc. and their consortium. J Hazard Mater 190:424–431. doi:10.1016/j.jhazmat.2011.03.065
Kagalkar AN, Jagtap UB, Jadhav JP, Bapat VA, Govindwar SP (2009) Biotechnological strategies for phytoremediation of the sulphonated azo dye Direct Red 5B using Blumea malcolmii Hook. Bioresour Technol 100:4104–4110. doi:10.1016/j.biortech.2009.03.049
Kagalkar AN, Jagtap UB, Jadhav JP, Govindwar SP, Bapat VA (2010) Studies on phytoremediation potentiality of Typhonium flagelliforme for the degradation of Brilliant Blue R. Planta 232:271–285. doi:10.1007/s00425-010-1157-2
Kalme SD, Parshetti GK, Jadhav SU, Govindwar SP (2007) Biodegradation of benzidine based dye Direct Blue-6 by Pseudomonas desmolyticum NCIM 2112. Bioresour Technol 98:1405–1410. doi:10.1016/j.biortech.2006.05.023
Khandare RV, Kabra AN, Tamboli DP, Govindwar SP (2011a) The role of Aster amellus Linn. in the degradation of a sulfonated azo dye Remazol red: A phytoremediation strategy. Chemosphere 82:1147–1154. doi:10.1016/j.chemosphere.2010.12.073
Khandare RV, Kabra AN, Kurade MB, Govindwar SP (2011b) Phytoremediation potential of Portulaca grandiflora Hook. (Moss-Rose) in degrading a sulfonated diazo reactive dye Navy Blue HE2R (Reactive Blue 172). Bioresour Technol 102:6774–6777. doi:10.1016/j.biortech.2011.03.094
Lowry OH, Rosebrough NJ, Farr AL, Randall RL (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275
Murashige T, Skoog F (1962) A revised medium for the rapid growth and bioassays with tobacco cultures. Physiol Plant 15:473–497
Nilratnisakorn S, Thiravetyan P, Nakbanpote W (2007) Synthetic reactive dye wastewater treatment by narrow-leaved cattails (Typha angustifolia Linn.): effects of dye, salinity and metals. Sci Total Environ 384:67–76. doi:10.1016/j.scitotenv.2007.06.027
Olukanni OD, Osuntoki AA, Kalyani DC, Gbenle GO, Govindwar SP (2010) Decolorization and biodegradation of Reactive Blue 13 by Proteus mirabilis LAG. J Hazard Mater 184:290–298. doi:10.1016/j.jhazmat.2010.08.035
Patil P, Desai N, Govindwar S, Jadhav J, Bapat V (2009) Degradation analysis of Reactive Red 198 by hairy roots of Tagetes patula L. (Marigold). Planta 230:725–735. doi:10.1007/s00425-009-0980-9
Peralta-Zamora P, Esposito E, Pelegrini R, Groto R, Reyes J, Duran N (1998) Effluent treatment of pulp and paper and textile industries using immobilized horseradish peroxidase. Environ Technol 19:55–63. doi:10.1080/09593331908616655
Pilon-Smits E (2005) Phytoremediation. Ann Rev Plant Biol 56:15–39. doi:10.1146/annurev.arplant.56.032604.144214
Rentz JA, Alvarez PJJ, Schnoor JL (2005) Benzo[a]pyrene co-metabolism in the presence of plant root extracts and exudates: Implications for phytoremediation. Environ Pollut 136:477–484. doi:10.1016/j.envpol.2004.12.034
Russ R, Rau J, Stolz A (2000) The function of cytoplasm flavin reductases in the reduction of azo dye by bacteria. Appl Environ Microbiol 66:1429–1434. doi:10.1128/AEM.66.4.1429-1434.2000
Salokhe MD, Govindwar SP (1999) Effect of carbon source on the biotransformation enzymes in Serratia marcescens. World J Microbiol Biotechnol 15:229–232. doi:10.1023/A:1008875404889
Saratale RG, Saratale GD, Chang JS, Govindwar SP (2011) Bacterial decolorization and degradation of azo dyes: a review. J Taiwan Inst Chem Eng 42:138–157. doi:10.1016/j.jtice.2010.06.006
Shaffiqu TS, Roy JJ, Nair RA, Abraham TE (2002) Degradation of textile dyes mediated by plant peroxidases. Appl Biochem Biotechnol 102–103:315–326. doi:10.1385/ABAB:102-103:1-6:315
Sun TR, Cang L, Wang Q, Zhou D, Cheng J, Xu H (2010) Roles of abiotic losses, microbes, plant roots, and root exudates on phytoremediation of PAHs in a barren soil. J Hazard Mater 176:919–925. doi:10.1016/j.jhazmat.2009.11.124
Surwase SN, Jadhav JP (2010) Bioconversion of l-tyrosine to L-DOPA by a novel bacterium Bacillus sp. JPJ. Amino Acids 41:495–506. doi:10.1007/s00726-010-0768-z
Tamboli DP, Telke AA, Dawkar VV, Jadhav SB, Govindwar SP (2011) Purification and characterization of bacterial aryl alcohol oxidase from Sphingobacterium sp. ATM and its uses in textile dye decolorization. Biotechnol Bioprocess Eng 16:661–668. doi:10.1007/s12257-011-0031-9
Telke AA, Kadam AA, Jagtap SS, Jadhav JP, Govindwar SP (2010) Biochemical characterization and potential for textile dye degradation of blue laccase from Aspergillus ochraceus NCIM-1146. Biotechnol Bioprocess Eng 15:696–703. doi:10.1007/s12257-009-3126-9
Tesar M, Reichenauer TG, Sessitsch A (2002) Bacterial rhizosphere populations of black poplar and herbal plants to be used for phytoremediation of diesel fuel. Soil Biol Biochem 34:1883–1892. doi:10.1016/S0038-0717(02)00202-X
Timmis KN (2002) Pseudomonas putida: a cosmopolitan opportunist par excellence. Environ Microbiol 4:779–781. doi:10.1046/j.1462-2920.2002.00365.x
Weyens N, Lelie D, Taghavi S, Vangronsveld J (2009) Phytoremediation: plant–endophyte partnerships take the challenge. Curr Opin Biotech 20:248–254. doi:10.1016/j.copbio.2009.02.012
Wild E, Dent J, Thomas G, Jones K (2005) Direct observation of organic contaminant uptake, storage, and metabolism within plant roots. Environ Sci Technol 39:3695–3702. doi:10.1021/es048136a
Acknowledgments
R.V. Khandare and A.N. Kabra wish to thank the Department of Biotechnology (DBT), New Delhi, India, for providing Junior Research Fellowships and research grant (numbered DBT-JRF/2010-2011/647). A.V. Awate wishes to thank the DBT, New Delhi, India, for providing studentship.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Khandare, R.V., Kabra, A.N., Awate, A.V. et al. Synergistic degradation of diazo dye Direct Red 5B by Portulaca grandiflora and Pseudomonas putida . Int. J. Environ. Sci. Technol. 10, 1039–1050 (2013). https://doi.org/10.1007/s13762-013-0244-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13762-013-0244-x