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Sequential Microaerophilic-Oxic Phase Mineralization of Azo Dyes by a Monoculture of Pseudomonas Aeruginosa Strain AWF Isolated from Textile Wastewater

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Abstract

A novel dye degrading bacterium capable of decolorizing and mineralizing four different dyes (Methyl red, Orange II, Direct red 80, and Direct blue 71) was isolated from textile industrial wastewater using the selective enrichment technique. The bacterium was identified as Pseudomonas aeruginosa. More than 80 % decolorization of Direct red 80 was obtained under microaerophilic conditions in 48 h, whereas only 10 % color removal was obtained under oxic conditions at the same time. Subsequent aeration of the decolorized medium resulted in the mineralization of the metabolic intermediates generated after azo bond cleavage by P. aeruginosa as confirmed by total organic carbon content and high-performance liquid chromatography analyses. The degradation products were characterized by Fourier transform infrared spectrometer and nuclear magnetic resonance techniques whereas the biotoxicity profile of the samples were evaluated using the brine shrimp lethality test assay. Data from this study provide evidence of dye mineralization and detoxification by a monoculture of P. aeruginosa in successive microaerophilic/oxic stages.

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References

  • Amann, R. I., Ludwig, W., & Schleifer, K. H. (1995). Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiological Reviews, 59, 143–169.

    CAS  Google Scholar 

  • Amoozegar, M. A., Hajighasemi, M., Hamedi, J., Asad, S., & Ventosa, A. (2011). Azo dye decolorization by halophilic and halotolerant microorganisms. Annals of Microbiology, 61, 217–230.

    Article  CAS  Google Scholar 

  • Anjaneyulu, Y., Sreedhara, C. N., & Samuel Suman Raj, D. (2005). Decolourization of industrial effluents—available methods and emerging technologies—a review. Reviews in Environmental Science and BioTechnology, 4, 245–273.

    Article  CAS  Google Scholar 

  • Banat, I. M., Nigam, P., Singh, D., & Marchant, R. (1996). Microbial decolorization of textile-dye containing effluents: a review. Bioresource Technology, 58, 217–227.

    Article  CAS  Google Scholar 

  • Blanquez, P., Casas, N., Font, X., Gabarrell, X., Sarra, M., Caminal, G., et al. (2004). Mechanism of textile metal dye biotransformation by Trametes versicolor. Water Research, 38, 2166–2172.

    Article  CAS  Google Scholar 

  • Boer, C. G., Obici, L., Souza, C. G. M., & Peralta, R. M. (2004). Decolorization of synthetic dyes by solid state cultures of Lentinula (Lentinus) edodes producing manganese peroxidase as the main ligninolytic enzyme. Bioresource Technology, 94, 107–112.

    Article  CAS  Google Scholar 

  • Cervantes, F. J., & Dos Santos, A. B. (2011). Reduction of azo dyes by anaerobic bacteria: microbiological and biochemical aspects. Reviews in Environmental Science and Biotechnology, 10, 125–137.

    Article  CAS  Google Scholar 

  • Chang, J. S., Chen, B. Y., & Lin, Y. S. (2004). Stimulation of bacterial decolorization of an azo dye by extracellular metabolites from Escherichia coli strain NO3. Bioresource Technology, 91, 243–248.

    Article  CAS  Google Scholar 

  • Chang, J. S., Chou, C., Lin, Y. C., Lin, P. J., Ho, J. Y., & Lee Hu, T. (2001). Kinetic characteristics of bacterial azo-dye decolorization by Pseudomonas luteola. Water Research, 35, 2841–2850.

    Article  CAS  Google Scholar 

  • Chen, B. Y. (2002). Understanding decolorization characteristics of reactive azo dyes by Pseudomonas luteola: toxicity and kinetics. Process Biochemistry, 38, 437–446.

    Article  CAS  Google Scholar 

  • Chen, J. P., & Lin, Y. S. (2007). Decolorization of azo dye by immobilized Pseudomonas luteola entrapped in alginate–silicate sol–gel beads. Process Biochemistry, 42, 934–942.

    Article  CAS  Google Scholar 

  • Chen, K., Huang, W., Wu, J., & Houng, J. (1999). Microbial decolorization of azo dyes by Proteus mirabilis. Journal of Industrial Microbiology and Biotechnology, 23, 686–690.

    Article  CAS  Google Scholar 

  • Chung, K. T. (2000). Mutagenicity and carcinogenicity of aromatic amines metabolically produced from azo dyes. Journal of Environmental Science and Health. Part C, 18, 51–74.

    Article  Google Scholar 

  • de Aragão Umbuzeiro, G., Freeman, H. S., Warren, S. H., De Oliveira, D. P., Terao, Y., Watanabe, T., et al. (2005). The contribution of azo dyes to the mutagenic activity of the Cristais River. Chemosphere, 60, 55–64.

    Article  Google Scholar 

  • dos Santos, A. B., Cervantes, F. J., & van Lier, J. B. (2007). Review paper on current technologies for decolourisation of textile wastewaters: perspectives for anaerobic biotechnology. Bioresource Technology, 98, 2369–2385.

    Article  Google Scholar 

  • El Ahwany, A. M. D. (2008). Decolorization of Fast red by metabolizing cells of Oenococcus oeni ML34. World Journal of Microbiology and Biotechnology, 24, 1521–1527.

    Article  Google Scholar 

  • Franciscon, E., Zille, A., Fantinatti-Garboggini, F., Silva, I. S., Cavaco-Paulo, A., & Durrant, L. R. (2009). Microaerophilic–aerobic sequential decolourization/biodegradation of textile azo dyes by a facultative Klebsiella sp. strain VN-31. Process Biochemistry, 44, 446–452.

    Article  CAS  Google Scholar 

  • Gavril, M., & Hodson, P. V. (2007). Chemical evidence for the mechanism of the biodecoloration of Amaranth by Trametes versicolor. World Journal of Microbiology and Biotechnology, 23, 103–124.

    Article  CAS  Google Scholar 

  • Golka, K., Kopps, S., & Myslak, Z. W. (2004). Carcinogenicity of azo colorants: influence of solubility and bioavailability. Toxicology Letters, 151, 203.

    Article  CAS  Google Scholar 

  • Gomare, S. S., Jadhav, J. P., & Govindwar, S. P. (2008). Degradation of sulfonated azo dyes by the purified lignin peroxidase from brevibacillus laterosporus MTCC 2298. Biotechnology and Bioprocess Engineering, 13, 136–143.

    Article  CAS  Google Scholar 

  • Gottlieb, A., Shaw, C., Smith, A., Wheatley, A., & Forsythe, S. (2003). The toxicity of textile reactive azo dyes after hydrolysis and decolourisation. Journal of Biotechnology, 101, 49–56.

    Article  CAS  Google Scholar 

  • Hildenbrand, S., Schmahl, F., Wodarz, R., Kimmel, R., & Dartsch, P. (1999). Azo dyes and carcinogenic aromatic amines in cell cultures. International Archives of Occupational and Environmental Health, 72, 52–56.

    Article  Google Scholar 

  • Hong, Y., Xu, M., Guo, J., Xu, Z., Chen, X., & Sun, G. (2007). Respiration and growth of Shewanella decolorationis S12 with an azo compound as the sole electron acceptor. Applied and Environmental Microbiology, 73, 64–72.

    Article  CAS  Google Scholar 

  • Jadhav, S., Jadhav, U., Dawkar, V., & Govindwar, S. (2008). Biodegradation of disperse dye brown 3REL by microbial consortium of Galactomyces geotrichum MTCC 1360 and Bacillus sp. VUS. Biotechnology and Bioprocess Engineering, 13, 232–239.

    Article  CAS  Google Scholar 

  • Jaspers, E., & Overmann, J. (2004). Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Applied and Environmental Microbiology, 70, 4831–4839.

    Article  CAS  Google Scholar 

  • Joshi, T., Iyengar, L., Singh, K., & Garg, S. (2008). Isolation, identification and application of novel bacterial consortium TJ-1 for the decolourization of structurally different azo dyes. Bioresource Technology, 99, 7115–7121.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Khalid, A., Arshad, M., & Crowley, D. E. (2008a). Accelerated decolorization of structurally different azo dyes by newly isolated bacterial strains. Applied Microbiology and Biotechnology, 78, 361–369.

    Article  CAS  Google Scholar 

  • Khalid, A., Arshad, M., & Crowley, D. E. (2008b). Decolorization of azo dyes by Shewanella sp. under saline conditions. Applied Microbiology and Biotechnology, 79, 1053–1059.

    Article  CAS  Google Scholar 

  • Khan, R., & Banerjee, U. (2010). Decolorization of azo dyes by immobilized bacteria. Biodegradation of Azo Dyes, 73–84.

  • Khehra, M. S., Saini, H. S., Sharma, D. K., Chadha, B. S., & Chimni, S. S. (2005). Decolorization of various azo dyes by bacteria consortium. Dyes and Pigments, 67(1), 55–61.

    Article  CAS  Google Scholar 

  • Kumar, V., Wati, L., FitzGibbon, F., Nigam, P., Banat, I., Singh, D., et al. (1997). Bioremediation and decolorization of anaerobically digested distillery spent wash. Biotechnology Letters, 19, 311–314.

    Article  CAS  Google Scholar 

  • Litchfield, J. T., & Wilcoxon, F. (1949). A simplified method of evaluating dose–effect experiments. Journal of Pharmacology and Experimental Therapeutics, 96, 99–113.

    CAS  Google Scholar 

  • Lucas, M. S., & Peres, J. A. (2007). Degradation of Reactive Black 5 by Fenton/UV-C and ferrioxalate/H2O2/solar light processes. Dyes and Pigments, 74, 622–629.

    Article  CAS  Google Scholar 

  • McDowell, E. M., & Trump, B. F. (1976). Histologic fixatives suitable for diagnostic light and electron microscopy. Archives of Pathology & Laboratory Medicine, 100, 405.

    CAS  Google Scholar 

  • Meyer, B., Ferrigni, N., Putnam, J., Jacobsen, L., Nichols, D. E., & McLaughlin, J. (1982). Brine shrimp: a convenient general bioassay for active plant constituents. Planta Medica, 45, 31.

    Article  CAS  Google Scholar 

  • Modi, H., Rajput, G., & Ambasana, C. (2010). Decolorization of water soluble azo dyes by bacterial cultures, isolated from dye house effluent. Bioresource Technology, 101, 6580–6583.

    Article  CAS  Google Scholar 

  • Moutaouakkil, A., Zeroual, Y., Zohra Dzayri, F., Talbi, M., Lee, K., & Blaghen, M. (2003). Purification and partial characterization of azoreductase from Enterobacter agglomerans. Archives of Biochemistry and Biophysics, 413, 139–146.

    Article  CAS  Google Scholar 

  • NCBI. 2012. http://www.ncbi.nlm.nih.gov/BLAST/Blast.cgi.

  • Ogugbue, C., Sawidis, T., Oranusi, N. (2011). Evaluation of colour removal in synthetic saline wastewater containing azo dyes using an immobilized halotolerant cell system. Ecological Engineering 37, 2056.

  • Ogugbue, C.J., Sawidis, T. (2011). Bioremediation and detoxification of synthetic wastewater containing triarylmethane dyes by Aeromonas hydrophila isolated from industrial effluent. Biotechnology Research International 2011, 1–11.

  • Palácio, S. M., Espinoza-Quiñones, F. R., Módenes, A. N., Oliveira, C. C., Borba, F. H., & Silva, F. G. (2009). Toxicity assessment from electro-coagulation treated-textile dye wastewaters by bioassays. Journal of Hazardous Materials, 172, 330–337.

    Article  Google Scholar 

  • Pandey, A., Singh, P., & Iyengar, L. (2007). Bacterial decolorization and degradation of azo dyes. International Biodeterioration and Biodegradation, 59, 73–84.

    Article  CAS  Google Scholar 

  • Patel, R., & Suresh, S. (2008). Kinetic and equilibrium studies on the biosorption of reactive black 5 dye by Aspergillus foetidus. Bioresource Technology, 99, 51–58.

    Article  CAS  Google Scholar 

  • Pinheiro, H., Touraud, E., & Thomas, O. (2004). Aromatic amines from azo dye reduction: status review with emphasis on direct UV spectrophotometric detection in textile industry wastewaters. Dyes and Pigments, 61, 121–139.

    Article  CAS  Google Scholar 

  • Rai, H. S., Bhattacharyya, M. S., Singh, J., Bansal, T., Vats, P., & Banerjee, U. (2005). Removal of dyes from the effluent of textile and dyestuff manufacturing industry: a review of emerging techniques with reference to biological treatment. Critical Reviews in Environmental Science and Technology, 35, 219–238.

    Article  CAS  Google Scholar 

  • Saratale, G.D., Chien, L.J. and Chang, J.S. (2011a) Enzymatic treatment of lignocellulosic wastes for anaerobic digestion and bioenergy production. In: Environmental anaerobic technology: applications and new developments. World Scientific, London, p. 279

  • Saratale, R., Saratale, G., Chang, J., & Govindwar, S. (2010). Decolorization and biodegradation of reactive dyes and dye wastewater by a developed bacterial consortium. Biodegradation, 21, 999–1015.

    Article  CAS  Google Scholar 

  • Saratale, R., Saratale, G., Chang, J., & Govindwar, S. (2011b). Bacterial decolorization and degradation of azo dyes: a review. Journal of the Taiwan Institute of Chemical Engineers, 42, 138–157.

    Article  CAS  Google Scholar 

  • Saratale, R., Saratale, G., Chang, J. S., & Govindwar, S. (2009a). Decolorization and biodegradation of textile dye Navy blue HER by Trichosporon beigelii NCIM-3326. Journal of Hazardous Materials, 166, 1421.

    Article  CAS  Google Scholar 

  • Saratale, R., Saratale, G., Chang, J. S., & Govindwar, S. (2009b). Ecofriendly degradation of sulfonated diazo dye CI Reactive Green 19A using Micrococcus glutamicus NCIM-2168. Bioresource Technology, 100, 3897–3905.

    Article  CAS  Google Scholar 

  • Saratale, R., Saratale, G., Kalyani, D., Chang, J. S., & Govindwar, S. (2009c). Enhanced decolorization and biodegradation of textile azo dye Scarlet R by using developed microbial consortium-GR. Bioresource Technology, 100, 2493–2500.

    Article  CAS  Google Scholar 

  • Seesuriyachan, P., Takenaka, S., Kuntiya, A., Klayraung, S., Murakami, S., & Aoki, K. (2007). Metabolism of azo dyes by Lactobacillus casei TISTR 1500 and effects of various factors on decolorization. Water Research, 41, 985–992.

    Article  CAS  Google Scholar 

  • Sasidharan, S., Darah, I., & Jain, K. (2008). In vivo and in vitro toxicity study of Gracilaria changii. Pharmaceutical Biology, 46, 413–417.

    Article  CAS  Google Scholar 

  • Sheth, N., & Dave, S. (2009). Optimisation for enhanced decolourization and degradation of Reactive Red BS CI 111 by Pseudomonas aeruginosa NGKCTS. Biodegradation, 20, 827–836.

    Article  CAS  Google Scholar 

  • Silveira, E., Marques, P., Silva, S., Lima-Filho, J., Porto, A., & Tambourgi, E. (2009). Selection of Pseudomonas for industrial textile dyes decolourization. International Biodeterioration and Biodegradation, 63, 230–235.

    Article  CAS  Google Scholar 

  • Singh, P., Sanghi, R., Pandey, A., & Iyengar, L. (2007). Decolorization and partial degradation of monoazo dyes in sequential fixed-film anaerobic batch reactor (SFABR). Bioresource Technology, 98, 2053–2056.

    Article  CAS  Google Scholar 

  • Talarposhti, A. M., Donnelly, T., & Anderson, G. (2001). Colour removal from a simulated dye wastewater using a two-phase anaerobic packed bed reactor. Water Research, 35, 425–432.

    Article  CAS  Google Scholar 

  • Tan, N., Borger, A., Slenders, P., Svitelskaya, A., Lettinga, G., Field, J. (2000). Degradation of azo dye Mordant Yellow 10 in a sequential anaerobic and bioaugmented aerobic bioreactor. Water Science and Technology, 337–344

  • Tan, N., Prenafeta-Boldu, F., Opsteeg, J., Lettinga, G., & Field, J. (1999). Biodegradation of azo dyes in cocultures of anaerobic granular sludge with aerobic aromatic amine degrading enrichment cultures. Applied Microbiology and Biotechnology, 51, 865–871.

    Article  CAS  Google Scholar 

  • Tony, B. D., Goyal, D., & Khanna, S. (2009). Decolorization of textile azo dyes by aerobic bacterial consortium. International Biodeterioration and Biodegradation, 63, 462–469.

    Article  CAS  Google Scholar 

  • van der Zee, F. P., Lettinga, G., & Field, J. A. (2001). Azo dye decolourisation by anaerobic granular sludge. Chemosphere, 44, 1169–1176.

    Article  Google Scholar 

  • van der Zee, F. P., & Villaverde, S. (2005). Combined anaerobic–aerobic treatment of azo dyes—a short review of bioreactor studies. Water Research, 39(8), 1425–1440.

    Article  Google Scholar 

  • Zhao, X., & Hardin, I. R. (2007). HPLC and spectrophotometric analysis of biodegradation of azo dyes by Pleurotus ostreatus. Dyes and Pigments, 73, 322–325.

    Article  CAS  Google Scholar 

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Acknowledgments

One of the authors (Ogugbue, C.J.) is thankful to the Academy of Science for the Developing World (TWAS) and the Universiti Sains Malaysia (USM) for awarding him the TWAS-USM Post Doctoral Fellowship.

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Correspondence to Norhashimah Morad.

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Hafshejani, M.K., Ogugbue, C.J. & Morad, N. Sequential Microaerophilic-Oxic Phase Mineralization of Azo Dyes by a Monoculture of Pseudomonas Aeruginosa Strain AWF Isolated from Textile Wastewater. Water Air Soil Pollut 224, 1672 (2013). https://doi.org/10.1007/s11270-013-1672-4

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