Abstract
Different types of microorganisms are capable of degrading azo dyes due to their high metabolic potentials. However, many of them cannot be used as degrading agents due to the harsh conditions of dye-polluted environments. Here, halophilic and halotolerant microorganisms can be the best candidates for a practical biodecolorization process as they are able to grow easily at high concentrations of salts. In addition, some of them can tolerate the presence of other stress factors such as toxic oxyanions and heavy metals which are so common in industrial wastewaters. In recent years, several studies have been focused on halophilic and halotolerant microorganisms and their abilities for decolorization of azo dyes. For example, Shewanella putrefaciens was determined to be capable of the complete removal of Reactive Black-5, Direct Red-81, Acid Red-88 and Disperse Orange-3 (all 100 mg l−1) within 8 h in the presence of 40 g l−1 NaCl. Another halophilic example is Halomonas sp. GTW which has shown a remarkable performance in the removal of different azo dyes within 24 h in the presence of 150 g l−1 NaCl. Although these approaches need to be studied in more detail, some studies have designed different types of fermentation processes and even specific fermentors to provide a practical methodology for industrial wastewater remediation. Sequential anaerobic EGSB (expanded granular sludge blanket) and aerobic reactor was the result of an important attempt to design an effective approach to large-scale biodecolorization.
Similar content being viewed by others
References
Amoozegar MA, Ghasemi A, Razavi MR, Naddaf S (2007) Evaluation of hexavalent chromium reduction by chromate-resistant moderately halophile, Nesterenkonia sp. strain MF2. Process Biochem 42:1475–1479
Amoozegar MA, Ashengroph M, Malekzadeh F, Razavi MR, Naddaf S, Kabiri M (2008) Isolation and initial characterization of the tellurite reducing moderately halophilic bacterium, Salinicoccus sp. strain QW6. Microbiol Res 163:456–465
An H, Qian Y, Gu X, Tang WZ (1996) Biological treatment of dye wastewaters using an anaerobic-oxic system. Chemosphere 33:2533–2542
Anliker R (1979) Ecotoxicology of dyestuffs – a joint effort by industry. Ecotoxicol Environ Saf 3:59–74
Asad S, Amoozegar MA, Pourbabaee AA, Sarbolouki MN, Dastgheib SMM (2007) Decolorization of textile azo dyes by newly isolated halophilic and halotolerant bacteria. Bioresour Technol 98:2082–2088
Balan DSL, Monteneiro RTR (2001) Decolorization of textile indigo dye by ligninolytic fungi. J Biotechnol 89:141–145
Benigni R, Passerini L (2002) Carcinogenicity of the aromatic amines: from structure-activity relationships to mechanisms of action and risk assessment. Mutat Res 511(3):191–206
Boer CG, Obici L, Souza CG, Peralta RM (2004) Decolourization of synthetic dyes by solid state cultures of Lentinula (Lentinus) edodes producing manganese peroxidase as the main lignolytic enzyme. Bioresour Technol 94:107–112
Brigé A, Motte B, Borloo J, Buysschaert G, Devreese B, Van Beeumen JJ (2008) Bacterial decolorization of textile dyes is an extracellular process requiring a multicomponent electron transfer pathway. Microb Biotechnol 1:40–52
Brown MA, DeVito SC (1993) Predicting azo dye toxicity. Crit Rev Environ Sci Technol 23:249–324
Brown D, Hamburger B (1987) The degradation of dyestuffs, part III, Investigations of their ultimative biodegradability. Chemosphere 16:1539–1553
Brown D, Laboureur P (1983) The aerobic biodegradability of primary aromatic amines. Chemosphere 12:405–414
Carliell CM, Barclay SJ, Naidoo N, Buckley CA, Mulholland DA, Senior E (1994) Anaerobic decolorisation of reactive dyes in conventional sewage treatment processes. Water SA 20:341–344
Chen X, Xu M, Wei J, Sun G (2010) Two different electron transfer pathways may involve in azoreduction in Shewanella decolorationis S12. Appl Microbiol Biotechnol 86:743–751
Chudgar RJ (1985) Azo dyes. In: Kroschwitz JI (ed) Kirk-Othmer encyclopedia of chemical technology, 4th edn. Wiley, New York, pp 821–875
Chung KT, Stevens SE, Cerniglia CE (1992) The reduction of azo dyes by the intestinal microflora. Crit Rev Microbiol 18:175–190
Clarke A, Anliker R (1980) Organic dyes and pigments. In: The handbook of environmental chemistry. Springer Berlin, pp 181–215
Correia VM, Stephenson T, Judd SJ (1994) Characteristics of textile wastewaters. Environ Technol 15:917–929
DasSarma S, Arora P (2002) Halophiles. In: Encyclopedia of life sciences. Nature, London 8:458–466
De Baere LA, Devocht M, Assche PV, Verstraete W (1984) Influence of high NaCl and NH4Cl salt levels on methanogenic associations. Water Res 18:543–648
Dong X, Zhou J, Liu Y (2003) Peptone–induced biodecolorization of Reactive Brilliant Blue (KN-R) by Rhodocycus gelatinosus XL-1. Process Biochem 39:89–94
Feigel BJ, Knackmuss HJ (1993) Syntrophic interactions during degradation of 4-aminobenzenesulfonic acid by a two species bacterial culture. Arch Microbiol 159:124–130
Fitzgerald SW, Bishop PL (1995) Two stage anaerobic/aerobic treatment of sulfonated azo dyes. J Environ Sci Health A 30:1251–1276
Georgiou D, Metallinou C, Aivasidis A, Voudrias E, Gimouhopoulos K (2004) Decolorization of azo-reactive dyes and cotton-textile wastewater using anaerobic digestion and acetate-consuming bacteria. Biochem Eng J 19:75–79
Ghosh DK, Mandal A, Chaudhuri J (1992) Purification and partial characterization of two azoreductases from Shigella dysenteriae type 1. FEMS Microbiol Lett 77:229–233
Ghosh DK, Ghosh S, Sadhukhan P, Mandal A, Chaudhuri J (1993) Purification of two azoreductases from Escherichia coli K12. Indian J Exp Biol 31:951–954
Gill M, Strauch RJ (1984) Constituents of Agaricus xanthodermus Genevier: the first naturally endogenous azo compound and toxic phenolic metabolites. Z Naturforsch 39(c):1027–1029
Glässer A, Liebelt U, Hempel DC (1992) Design of a two-stage process for total degradation of azo dyes. DECHEMA Biotechnol Conf 5(B):1085–1088
Grau P (1991) Textile industry wastewater treatment. Water Sci Technol 24(1):97–103
Guo J, Zhou J, Wang D, Tian C, Wang P, Salah Uddin M (2008a) A novel moderately halophilic bacterium for decolorizing azo dye under high salt condition. Biodegradation 19:15–19
Guo J, Zhou J, Wang D, Yang J, Li Z (2008b) The new incorporation bio-treatment technology of bromoamine acid and azo dyes wastewaters under high-salt conditions. Biodegradation 19:93–98
Hao OJ, Kim H, Chaing PC (2000) Decolorization of wastewater. Crit Rev Environ Sci Technol 30:49–505
Harmer C, Bishop P (1992) Transformation of azo dye AO-7 by wastewater biofilms. Water Sci Technol 6:627–636
Haug W, Schmidt A, Nörtemann B, Hempel DC, Stolz A, Knackmuss HJ (1991) Mineralization of the sulfonated azo dye Mordant Yellow 3 by a 6-aminonaphthalene-2-sulfonate-degrading bacterial consortium. Appl Environ Microbiol 57:3144–3149
Hong Y, Xu M, Guo J, Xu Z, Chen X, Sun G (2007a) Respiration and growth of Shewanella decolorationis S12 with an azo compound as the sole electron acceptor. Appl Environ Microbiol 73(1):64–72
Hong Y, Chen X, Guo J, Xu Z, Xu M, Sun G (2007b) Effects of electron donors and acceptors on anaerobic reduction of azo dyes by Shewanella decolorationis S12. Appl Microbiol Biotechnol 74:230–238
Hong Y, Guo J, Xu Z, Mo C, Xu M, Sun G (2007c) Reduction and partial degradation mechanisms of naphthylaminesulfonic azo dye amaranth by Shewanella decolorationis S12. Appl Microbiol Biotechnol 75:647–654
Ince H, Tezcanli G (1999) Treatability of textile dye-bath effluents by advanced oxidation: preparation for reuse. Water Sci Technol 40:183–190
Jeckel M (1997) Wastewater treatment in the textile industry. In: Kornmüller A (ed) Treatment of wastewaters from textile processing. Schrift Biol Abwass 9 TU Berlin, pp 3–12
Jiang H, Bishop PL (1994) Aerobic biodegradation of azo dyes in biofilms. Water Sci Technol 29:525–530
Junkins R (1982) Textile wastes, case history: pretreatment of textile wastewater. In: proceedings of the International conference on industrial waste 37. Ann Arbor Science Purdue University, pp 139–146
Kabiri M, Amoozegar MA, Tabebordbar M, Gilany K, Hosseini Salekdeh G (2009) Effects of Selenite and Tellurite on Growth, Physiology, and Proteome of a Moderately Halophilic Bacterium. J Proteome Res 8:3098–3108
Kalyani DC, Telke AA, Dhanve RS, Jadhav JP (2009) Ecofriendly biodegradation and detoxification of Reactive Red 2 textile dye by newly isolated Pseudomonas sp. SUK1. J Hazard Mater 163:735–742
Kertell RC, Hill FG (1982) Textile dyehouse wastewater treatment: a case history. In proceedings of the International conference on industrial waste 37. Ann Arbor Science Purdue University, pp 147–156
Khalid A, Arshad M, Crowley DE (2008a) Accelerated decolorization of structurally different azo dyes by newly isolated bacterial strains. Appl Microbiol Biotechnol 78:361–369
Khalid A, Arshad M, Crowley DE (2008b) Decolorization of azo dyes by Shewanella sp. under saline conditions. Appl Microbiol Biotechnol 79:1053–1059
Kodam KM, Soojhawon I, Lohande PD, Gawai KR (2005) Microbial decolorization of reactive azo dyes under aerobic conditions. World J Microbiol Biotechnol 21:367–370
Krull R, Hempel DC, Metzen P, Alfter P (2000) Konzept zur technischen Umsetzung einer zwiestufigen anoxischen und erobe Textilabwasserbehandlung. Chem Ing Tech 72:1113–1114
Kudlich M, Bishop P, Knackmuss HJ, Stolz A (1996) Synchronous anaerobic and aerobic degradation of the sulfonated azo dye Mordant Yellow 3 by immobilized cells from a naphthalenesulfonate- degrading mixed culture. Appl Microbiol Biotechnol 46:597–603
Kudlich M, Hetheridge MJ, Knackmuss HJ, Stolz A (1999) Autoxidation reactions of different aromatic ortho-aminohydroxynaphthalenes which are formed during the anaerobic reduction of sulfonated azo dyes. Environ Sci Technol 33:896–901
Larson AR, Weber EJ (1994) Reaction mechanisms in environmental organic chemistry. Lewis, USA
Le Borgne S, Dayanira Paniagua D, Vazquez-Duhalt R (2008) Biodegradation of organic pollutants by halophilic bacteria and archaea. J Mol Microbiol Biotechnol 15:74–92
Locher HH, Thurnheer T, Leisinger T, Cook AM (1989) 3-Nitrobenzenesulfonate, 3-aminobenzenesulfonate, and 4-aminobenzenesulfonate as sole carbon sources for bacteria. Appl Environ Microbiol 55:492–494
Lourenço ND, Novais JM, Pinheiro HM (2006) Kinetic studies of reactive azo dye decolorization in anaerobic/aerobic sequencing batch reactors. Biotechnol Lett 28:733–739
Maguire RJ, Tkacz RJ (1991) Occurence of dyes in the Yamaska River, Québec. Water Pollut Res J Can 26:145–161
Maier J, Kandelbauer A, Erlacher A, Cavaco-Paulo A, Gubitz G (2004) A new alkali-thermostable azoreductase from Bacillus sp. strain SF. Appl Environ Microbiol 70:837–844
Manu B, Chauhari S (2003) Decolorization of indigo and azo dyes in semicontinuous reactors with long hydraulic retention time. Process Biochem 38:1213–1221
Margesin R, Schinner F (2001) Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles 5:75–83
Meyer U (1981) Biodegradation of synthetic organic colorants. In: Leisinger T, Cook AM, Hutter R, Nuesch J (eds) Microbial degradation of Xenobiotics and recalcitrant compounds. FEMS Symposium 12. Academic, London, pp 371–385
Moosvi S, Kehaira H, Madamwar D (2005) Decolorization of textile dye reactive violet 5 by a newly isolated bacterial consortium RVM 11.1. World J Microbiol Biotechnol 21:667–672
Moser D, Nealson K (1996) Growth of the facultative anaerobe Shewanella putrefaciens by elemental sulfur reduction. Appl Environ Microbiol 62:2100–2105
Moutaouakkil A, Zeroual Y, Dzayri FZ, Talbi M, Lee K, Blaghen M (2003) Purification and partial characterization of azoreductase from Enterobacter agglomerans. Arch Biochem Biophys 413:139–146
Myers CR, Carstens BP, Antholine WE, Myers JM (2000) Chromium (VI) reductase activity is associated with the cytoplasmic membrane of anaerobically grown Shewanella putrefaciens MR-1. J Appl Microbiol 88:98–106
Namasivayam C, Yamuna RT (1992) Removal of Congo Red from aqueous solutions by biogas waste slurry. J Chem Tech Biotechnol 53:153–157
Nealson K, Saffarini D (1994) Iron and manganese in anaerobic respiration: environmental significance, physiology, and regulation. Annu Rev Microbiol 48:311–343
Nigam P, Banat IM, Singh D, Merchant R (1996) Microbial process for the decolorization of textile effluent containing azo, diazo and reactive dyes. Process Biochem 31:435–442
Nörtemann B, Baumgarten J, Rast HG, Knackmuss HJ (1986) Bacterial communities degrading amino- and hydroxynaphthalenesulfonates. Appl Environ Microbiol 52:1195–1202
Nörtemann B, Kuhm AE, Knackmuss HJ, Stolz A (1994) Conversion of substituted naphthalenesulfonates by Pseudomonas sp. BN6. Arch Microbiol 161:320–327
O’Neill C, Hawkes FR, Hawkes DL, Lourenco ND, Pinheiro HM, Delee W (1999) Color in textile effluents sources, measurement, discharge consents and simulation. J Chem Technol Biotechnol 74:1009–1018
O’Neill C, Lopez A, Esteves S, Hawkes FR, Hawkes DL, Wilcox S (2000a) Azo-dye degradation in an anaerobic-aerobic treatment system operating on simulated textile effluent. Appl Microbiol Biotechnol 53:249–254
O’Neill C, Hawkes FR, Hawkes DL, Esteves S, Wilcox SJ (2000b) Anaerobic-aerobic biotreatment of simulated textile effluent containing varied ratios of starch and azo dye. Water Res 34:2355–2361
Ohe T, Watanabe Y (1986) Degradation of 2-naphthylamine-1-sulfonic acid by Pseudomonas strain TA-1. Agric Biol Chem 50:1419–1426
Oren A (2002) Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. Ind Microbiol Biotechnol 28:56–63
Ozdemir G, Pazarbasi B, Kocyigit A, Omeroglu EE, Yasa I, Karaboz I (2008) Decolorization of Acid Black 210 by Vibrio harveyi TEMS1, a newly isolated bioluminescent bacterium from Izmir Bay, Turkey. World J Microbiol Biotechnol 24:1375–1381
Pagga U, Brown D (1986) The degradation of dyestuffs. Part II. Behav dyestuffs aerobic biodegradation tests. Chemosphere 15:479–491
Platzek T, Lang C, Grohmann G, Gi US, Baltes W (1999) Formation of carcinogenic aromatic amine from an azo dye by human skin bacteria in vitro. Hum Exp Toxicol 18:552–559
Rafii F, Cerniglia CE (1993) Comparison of the azoreductase and nitroreductase from Clostridium perfringens. Appl Environ Microbiol 59:1731–1734
Ràfols C, Barceló D (1997) Determination of mono- and disulphonated azo dyes by liquid chromatography-atmospheric pressure ionization mass spectrometry. J Chromatogr 777:177–192
Rajaguru P, Kalaiselvi K, Palanivel M, Subburam V (2000) Biodegradation of azo dyes in a sequential anaerobic-aerobic system. Appl Microbiol Biotechnol 54:268–273
Ramalho PA, Paiva S, Cavaco-Paulo A, Casal M, Cardoso MH, Ramalho MT (2005) Azo reductase activity of intact Saccharomyces cerevisiae cells is dependent on the Fre1p component of plasma membrane ferric reductase. Appl Environ Microbiol 71:3882–3888
Razo-Flores E, Luijten M, Donlon BA, Lettinga G, Field JA (1997) Complete biodegradation of the azo dye azodisalicylate under anaerobic conditions. Environ Sci Technol 31:2098–2103
Reife A, Freeman HS (2000) Pollution prevention in the production of dyes and pigments. Text Chem Color Am Dyes Report 32:56–60
Reisch MS (1996) Asian textile dye makers are a growing power in changing market. Chem Eng News Jan 15:10–12
Riu J, Schönsee I, Barceló D (1998) Determination of sulfonated azo dyes in groundwater and industrial effluent by automated solid-phase extraction followed by capillary electrophoresis/ mass spectrometry. J Mass Spectrom 33:653–663
Salah Uddin M, Zhou J, Qu Y, Guo J, Wang P, Zhao LH (2007) Biodecolorization of azo dye acid red B under high salinity condition. Bull Environ Contam Toxicol 79:440–444
Saltikov CW, Cifuentes A, Venkateswaran K, Newman DK (2003) The ars detoxification system is advantageous but not required for As (V) respiration by the genetically tractable Shewanella species strain ANA-3. Appl Environ Microbiol 69:2800–2809
Sani RK, Banerjee UC (1999) Decolorization of triphenylmethane dyes and textile and dyestuff effluent by Kurthia sp. Enzyme Microb Technol 24:433–437
Seshadri S, Bishop PL, Agha AM (1994) Anaerobic/aerobic treatment of selected azo dyes in waste water. Waste Manage 14:127–137
Shaul GM, Holdsworth TJ, Dempsey CR, Dostal KA (1991) Fate of water soluble azo dyes in the activated sludge process. Chemosphere 22:107–119
Sosath F, Libra JA (1997) Biologische Behandlung von synthetischen Abwässern mit Azofarbstoffen. Acta Hydrochim Hydrobiol 25:259–264
Stolz A (2001) Basic and applied aspects in the microbial degradation of azo dyes. Appl Microbiol Biotechnol 56:69–80
Supaka N, Juntongjin K, Damronglerd S, Delia ML, Strehaiano P (2004) Microbial decolorization of reactive azo dyes in a sequential anaerobic–aerobic system. Chem Eng J 99:169–176
Suzuki Y, Yoda T, Ruhul A, Sugiura W (2001) Molecular cloning and characterization of the gene coding for azoreductase from Bacillus sp. OY1–2 isolated from soil. J Biol Chem 276:9059–9065
Tan NCG (2001) Integrated and sequential anaerobic/aerobic biodegradation of azo dyes. Dissertation, University of Wageningen
Tan N, Prenafeta-Boldú FX, Opsteeg JL, Lettinga G, Field JA (1999) Biodegradation of azo dyes in cocultures of anaerobic granular sludge with aerobic aromatic amine degrading enrichment cultures. Appl Microbiol Biotechnol 51:865–871
Tan NCG, Borger A, Slender P, Svitelskaya AV, Lettinga G, Field JA (2000) Degradation of azo dye Mordant Yellow 10 in a sequential anaerobic and bioaugmented aerobic bioreactor. Water Sci Technol 42:337–344
Tan NC, van Leeuwen A, van Voorthuizen EM, Slenders P, Prenafeta-Boldú FX, Temmink H, Lettinga G, Field JA (2005) Fate and biodegradability of sulfonated aromatic amines. Biodegradation 16:527–537
Taskin M, Erdal S (2010), Reactive dye bioaccumulation by fungus Aspergillus niger isolated from the effluent of sugar fabric-contamined soil.Toxicol Indust Health. doi:10.1177/0748233710364967
Thurnheer T, Köhler T, Cook AM, Leisinger T (1986) Orthanilic acid and analogues as carbon sources for bacteria: growth physiology and enzymic desulphonation. J Gen Microbiol 132:1215–1220
Thurnheer T, Cook AM, Leisinger T (1988) Co-culture of defined bacteria to degrade seven sulfonated aromatic compounds: efficiency, rates and phenotypic variations. Appl Microbiol Biotechnol 29:605–609
Tincher WC, Robertson JR (1982) Analysis of dyes in textile dyeing wastewater. Text Chem Color 14:269–275
Ventosa A, Nieto JJ (1995) Biotechnological applications and potentialities of halophilic microorganisms. World J Microbiol Biotechnol 11:85–94
Ventosa A, Quesada E, Rodriguez-Valera F, Ruiz-Berraquero F, Ramos-Cormenzana A (1982) Numerical taxonomy of moderately halophilic Gram-negative rods. J Gen Microbiol 128:1959–1968
Ventosa A, Nieto JJ, Oren A (1998) Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol Rev 62:504–544
Verma P, Madamwar D (2005) Decolorization of Azo dyes using Basidiomycete strain PV 002. World J Microbiol Biotechnol 21:481–485
Wade R, DiChristina T (2000) Isolation of U (VI) reduction-deficient mutants of Shewanella putrefaciens. FEMS Microbiol Lett 184:143–146
Wang H, Zheng XW, Su JQ, Tian Y, Xiong XJ, Zheng TL (2009) Biological decolorization of the reactive dyes Reactive Black 5 by a novel isolated bacterial strain Enterobacter sp. EC3. J Hazard Mater 171:654–659
Weber EJ, Stickney VC (1993) Hydrolysis kinetics of Reactive Blue 19-vinyl sulfone. Water Res 27:63–67
Xu M, Guo J, Sun G (2007) Biodegradation of textile azo dye by Shewanella decolorationis S12 under microaerophilic conditions. Appl Microbiol Biotechnol 76:719–726
Zimmermann T, Kulla HG, Leisinger T (1982) Properties of purified orange azoreductase, the enzyme initiating azo dye degradation by Pseudomonas KF46. Eur J Biochem 129:197–203
Zimmermann T, Gasser F, Kulla HG, Leisinger T (1984) Comparison of two bacterial azoreductases acquired during adaptation to growth on azo dyes. Arch Microbiol 138:37–43
Zollinger H (1987) Azo dyes and pigments, in color chemistry: synthesis, properties and applications of organic dyes and pigments. VCH, New York, pp 92–100
Zollinger H (1991) Color chemistry. VCH, Weinheim
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Amoozegar, M.A., Hajighasemi, M., Hamedi, J. et al. Azo dye decolorization by halophilic and halotolerant microorganisms. Ann Microbiol 61, 217–230 (2011). https://doi.org/10.1007/s13213-010-0144-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13213-010-0144-y