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International Biodeterioration & Biodegradation 63 (2009) 582–586

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International Biodeterioration & Biodegradation

journal homepage: www.elsevier .com/locate/ ib iod

Eco-friendly biodegradation of a reactive textile dye Golden YellowHER by Brevibacillus laterosporus MTCC 2298

Sushama S. Gomare*, Dhawal P. Tamboli, Anuradha N. Kagalkar, Sanjay P. GovindwarDepartment of Biochemistry, Shivaji University, Vidhyanagar, Kolhapur 416004, India

a r t i c l e i n f o

Article history:Received 22 January 2009Received in revised form14 March 2009Accepted 25 March 2009Available online 26 April 2009

Keywords:Golden Yellow HERBrevibacillus laterosporusBiodegradationPhytotoxicity

* Corresponding author. Tel.: þ91 231 2609152; faxE-mail address: sushamabiochemist@gmail.com (S

0964-8305/$ – see front matter � 2009 Elsevier Ltd.doi:10.1016/j.ibiod.2009.03.005

a b s t r a c t

Brevibacillus laterosporus MTCC 2298 showed 87% decolorization of Golden Yellow HER within 48 hunder static condition at the concentration 50 mg l�1; however no significant change in the decolor-ization performance was observed under shaking condition. Decolorization performance was maximum(74%) at the pH 7.0 and 30 �C. TLC and HPLC analysis confirmed the biodegradation of Golden Yellow HER.Biodegradation pathway was proposed using GC–MS and FTIR spectral analysis. Mainly elected metab-olites are the 2,5-Dichloro-4 (3-hydrazino-2-hydroxy cyclopentylamino-) dibenzene-sulfonic acid (peak1, m/z ¼ 526), 4-(3-hydrazino-2-hydroxy cyclopentylamino)-benzene-sulfonic acid (peak 2, m/z ¼ 455),4-(3-amino-2-hydroxy-cyclopentylamino)-benzene-sulfonic acid and 5-amino-cyclohex-3-ene-sulfonicacid (peak 3, m/z ¼ 183). Phytotoxicity results suggested that degradation products of Golden Yellow HERare non-toxic to the common crops such as Sorghum vulgare and Phaseolus mungo. Also, degradationproducts are non-toxic to B. laterosporus as well as ecologically important bacteria like Pseudomonasaeruginosa and Azotobacter vinelandii.

� 2009 Elsevier Ltd. All rights reserved.

1. Introduction

More than 2000 structurally different azo dyes are currently inuse (Vijaykumar et al., 2007). Sulfonated azo dyes representa large group that gives diverse colors. Depending on the class ofthe dyes, their loss in wastewaters can range from 2% of theoriginal concentration for basic dyes to as high as 50% for reactivedyes (O’Neill et al., 1999; Tan et al., 2000; Boer et al., 2004).Various physical (Astrid et al., 2004; Anastasios et al., 2005;Theodora et al., 2006), chemical (Kabita et al., 2001) and biolog-ical treatments (Bustard et al., 1998; Hao et al., 2000; Robinsonet al., 2001) have been reported to remove colors from dye con-taining wastewater. Environmental biotechnology relies upon thepollutant degrading capacities of naturally occurring microbialconsortium in which bacteria play central role (Liu and Suffita,1993).

Number of microorganisms has been studied for their ability todecolorize a wide range of commercially available textile dyes (Jinqiand Houtian, 1992; Kim et al., 1995; Parikh and Madamwar, 2005;Parshetti et al., 2007). The features like omnipotence, faster growth,facultative nature and high adaptability are the desirable qualitiesof bacterial community for the bioremediation. Brevibacillus

: þ91 231 2691533..S. Gomare).

All rights reserved.

laterosporus strains are eco-friendly, since they have been studiedfor biological control (Edmar et al., 2004). B. laterosporus MTCC2298 showed the potential for the degradation of various azo dyesincluding Golden Yellow HER (Gomare and Govindwar, 2009).Present study was undertaken to confirm the biodegradation ofa commonly used reactive textile dye Golden Yellow HER by B.laterosporus. Also, analytical techniques such as TLC and HPLC, FTIRand GC–MS have been performed for the concrete conclusion.

2. Materials and methods

2.1. Microorganisms and culture conditions

B. laterosporus MTCC 2298 was obtained from Microbial TypeCulture Collection, Chandigarh, India. Pseudomonas aeruginosaNCIM 2036 and Azotobacter vinelandii NCIM 2821 were obtainedfrom NCIM, National Chemical Laboratory, Pune, India. All thebacterial strains were maintained routinely on the nutrient slantscontaining (g l�1): NaCl, 5.0; bacteriological peptone, 5.0; yeastextract, 2.0; beef extract, 1.0 and agar–agar 15.0 at 4 �C.

2.2. Dyes and chemicals

A textile dye Golden Yellow HER was obtained from YashwantTextile Processing, Ichalkaranji, Kolhapur, India. Remaining all

S.S. Gomare et al. / International Biodeterioration & Biodegradation 63 (2009) 582–586 583

chemicals were obtained from Hi-media Laboratories Pvt. Ltd.,Mumbai, India.

2.3. Decolorization experiments, physicochemical parameters andenzyme assays

B. laterosporus culture grown for 36 h (an exponential phase)was used for the dye decolorization. Decolorization was carried outunder static condition at 30 �C using 250 ml Erlenmeyer flasks.Aliquot (5 ml) withdrawn after decolorization was centrifuged(4000 � g for 20 min) and residual dye content in the supernatantwas measured according to the procedure reported earlier byGomare and Govindwar (2009). Effect of shaking condition on thedecolorization performance was studied by using an orbital shakeradjusted at 30 �C and 150 rpm. Pre-grown (under static condition)culture was kept on the shaker after dye addition. Effect of pH onthe decolorization performance was studied by adjusting differentpH (pH 3.0, 5.0, 7.0, 9.0 and 11.0) of the pre-grown culture beforedye addition. Effect of temperature on the decolorization perfor-mance was studied by incubating pre-grown (at 30 �C) culture atdifferent temperatures (5, 15, 30 and 45 �C) after the dye addition.Flasks were incubated at respective temperatures for 30 min beforeaddition of dye. Effect of repeated dye addition on the decoloriza-tion performance was studied by the repeated addition of dye(50 mg l�1) into a batch culture (100 ml) after every 48 h andremoval of dye during each cycle was monitored. All the decolor-ization experiments were carried out in triplicate. Lignin peroxi-dase, laccase, tyrosinase, aminopyrine N-demethylase, MGreductase and DCIP reductase activities were determined usingprocedures reported from our laboratory (Gomare and Govindwar,2009). Lignin peroxidase, laccase and tyrosinase activities wereassayed by monitoring the formation of propanaldehyde fromn-propanol, oxidized ABTS from ABTS and catechol quinone fromcatechol respectively. NADH–DCIP reductase and MG reductaseactivities were determined by monitoring reduction of DCIP andmalachite green respectively. Aminopyrine N-demethylase activitywas determined by measuring formaldehyde liberated by usingNash reagent (Gomare and Govindwar, 2009).

2.4. Extraction of degradation products

Biomass was removed after decolorization (10 000 � g at 4 �Cfor 20 min) and supernatant was extracted for degradation prod-ucts with an equal volume of ethyl acetate. The ethyl acetate extractwas evaporated in vacuum over anhydrous Na2SO4 and dried. Thedried sample was dissolved in 2 ml HPLC grade methanol and usedfor analytical studies.

Fig. 1. Comparison of the FTIR spectra of control dye Golden Yellow HER and itsdegradation products extracted after 48 h.

2.5. Analytical techniques

Thin layer chromatogram was obtained on the pre-coatedsilica gel plates with mobile phase containing methanol and spotswere visualized in an iodine chamber. HPLC analysis was carriedout at 30 �C by using Water Model 2487 equipped with dual lUV–Vis detector (set at 379 nm) and C18 column (symmetry,4.6 � 250 mm). Samples (10 ml) injected to separate dye productsat the flow rate 0.5 ml min�1 using an isocratic mobile system i.e.methanol for 10 min. FTIR spectral analysis was carried out in themid IR region of 400–4000 cm�1 with 16-scan speed (PerkinsElmer 783 Spectrophotometer). GC–MS analysis was carried outusing a Hewlett Packard 989 B MS Engine, equipped withintegrated gas chromatograph and an HP1 column (30 m long and0.25 mm id).

2.6. Toxicity studies

Toxicity effects of control dye and its degradation products werestudied for two important crops such as Sorghum vulgare andPhaseolus mungo. Toxicity of control dye studied at differentconcentrations and a concentration (0.1 g l�1) showing inhibitoryeffect on the growth of seeds was selected for further studies. Tenseeds of each crop allowed germinating in a filter paper beddedpetriplate with daily watering of 5.0 ml solutions (i.e. control dye/its degradation product). Simultaneously, a control set with theplain water supply was carried out. Toxicity effect was measured interms of percent germination and lengths of plumule and radicalafter 6 days. Relative seed germination, relative root elongation andgermination index (GI) were calculated by the formulae (Gomareet al., in press) as given below:

Relative seed germination ð%Þ

¼ No: of seeds germinated in the extractNo: of seeds germinated in the dye control

� 100

Relative root elongation ð%Þ

¼ Mean root elongation in the extractMean root elongation in the dye control

� 100

Germination index ðGIÞ

¼ ð% Seed germinationÞ � ð% Root elongationÞ100

Microbial toxicity studies carried out for the bacterial strainexploited for the decolorization i.e. B. laterosporus as well asa phosphate solubilizing bacterium P. aeruginosa and a nitrogenfixing bacterium A. vinelandii. The nutrient medium containing 1.5%agar was used for plating. Toxicity of control dye studied atdifferent concentrations and the concentration (1.0 g l�1) showingdistinct zone of inhibition was selected for further studies. Toxicityeffect was measured in terms of zone of inhibition (diameter in cm)after 24 h incubation at 30 �C.

3. Results and discussion

3.1. Decolorization of Golden Yellow HER and physicochemicalparameters

Literature survey revealed that there are no reports on thebacterial decolorization of Golden Yellow HER or the biological

Fig. 2. Gas chromatogram of degradation products of the Golden Yellow HER extractedafter 48 h.

S.S. Gomare et al. / International Biodeterioration & Biodegradation 63 (2009) 582–586584

treatment of textile effluents containing this widely used textiledye. B. laterosporus decolorized 87% of Golden Yellow HER within48 h under static condition; however decolorization performanceremained unchanged under shaking condition. Recently, acceler-ated decolorization of structurally different azo dyes by newlyisolated bacterial strains has reported, where, shaking increasedthe time required for complete decolorization of dye compared tothat which was required under static conditions (Khalid et al.,2008). The pH of culture medium of B. laterosporus at the time ofdye addition was 8.0. B. laterosporus showed maximum decolor-ization of Golden Yellow HER by the bacterial culture withoutadjusting the pH; however, decolorization was more than 60% inthe broader range of pH (i.e. 5.0–9.0). No change in pH of themedium observed during dye decolorization. Decolorization ofGolden Yellow HER by B. laterosporus was 62, 72, 74, 67, and 57%within 48 h at the pH 3.0, 5.0, 7.0, 9.0, and 11.0 respectively.Maximum decolorization of azo dyes by Pseudomonas sp. has beenreported between the pH 6.0 and 9.0 (Mali et al., 2000). Maximumrate of decolorization was between pH 7.0 and 8.5; however furtherincrease in pH caused decrease in the decolorization rate (Moosviet al., 2005). B. laterosporus exhibited maximum decolorization at30 �C whereas, about 60% dye removal observed even at 45 �C.Decolorization of Golden Yellow HER by B. laterosporus was 22, 43,86, and 64% within 48 h at 5, 15, 30, and 45 �C respectively. Nodecolorization was observed by the autoclaved cells or abioticcontrol. The dye decolorization activity of consortium NBNJ6 wasincreased with the increase in incubation temperature from 25 to37 �C and further increase in temperature resulted in the marginalreduction in decolorization activity (Junnarkar et al., 2006). Declinein decolorization activity at higher temperature can be attributed tothe loss of cell viability or to the denaturation of the enzymes(Pearce et al., 2003). Klebsiella pneumoniae RS-13 exhibited decol-orization of methyl red at temperatures varying from 23 to 37 �C,whereas decolorization was completely inhibited at 45 �C (Wongand Yuen, 1996). Degradation products formed and saturated in theculture medium may affect the cell viability and decolorizationactivity. B. laterosporus exhibited the ability to decolorize about 80%

Table 1GC–MS data of the Golden Yellow HER degradation products extracted after 48 h.

PeakNo.

RT m/z (percent relative intensity of the predominant ions flagged in the

1. 21.042 43 (73), 57 (27), 73 (27), 83 (47), 107 (7), 113 (100), 139 (10), 141 (33), 16341 (20), 353 (7), 377 (7), 399 (7), 411 (7), 427 (10), 441 (7), 479 (7), 4

2. 21.733 43 (64), 57 (64), 82 (7), 85 (93), 98 (7), 113 (100), 131 (93), 141 (43), 156(25), 327 (7), 343 (14), 356 (14), 369 (14), 384 (7), 399 (7), 412 (7), 42

3. 23.433 55 (13), 68 (19), 70 (6), 86 (75), 98 (6), 112 (6), 126 (6), 140 (13), 155 (4. 25.067 53 (56), 69 (50), 70 (56), 85 (50), 100 (56), 121 (38), 134 (50), 141 (100), 1

281 (63), 300 (31), 313 (63), 331 (56), 345 (31), 355 (75), 371 (56), 387(38), 538 (25).

of the Golden Yellow HER up to repeated V cycles of the dyeadditions and then declined up to 75% in the cycle VI. Moosvi et al.(2005) found that 93, 94 and 68% decolorization of Reactive Violet 5in the cycle I (40 h), II (24 h) and III (24 h) respectively by thebacterial consortium RVM-11.1.

3.2. Analysis of Golden Yellow HER degradation products

Thin layer chromatogram of control dye and its degradationproducts extracted after 48 h showed different spots having Rfvalue 0.98 and 0.91 respectively (data not shown). The HPLC ofcontrol dye showed a single peak at retention time 1.593, whereastwo peaks of the degradation products extracted after 48 h at theretention time 2.299 and 2.453 (data not shown). Overall findingssuggested biotransformation of the dye. The degradation productsof Golden Yellow HER are analyzed by FTIR analysis. FTIR spectrumof control dye displayed a peak at 3431 cm�1 for NeH stretch,a peak at 2924 cm�1 for CH3 stretch, a peak at 1574 cm�1 foreN]Ne stretch, a peak at 1487 cm�1 for ring vibrations, a peak at671 cm�1 for CeH bend, a peak at 1188 cm�1 for SO2 stretch whereas peaks at 1082, and 1039 cm�1 for CeN stretch as well as a peak at615 cm�1 for CeCl stretch suggested aromatic azo nature of the dyeand confirmed its chemical structure (Fig. 1). In recent years,vibrational spectroscopies such as Fourier transform infrared (FTIR)(Goodacre et al., 2000; Oberreuter et al., 2002) have been devel-oped for analyzing characteristics of the different samples. FTIRspectrum of degradation products displayed the peaks at 3241,1330, and 1106 cm�1 suggested the formation of NeNe disubsti-tuted sulfonamides from the parent dye molecules. Disappearanceof a peak at 1574 cm�1 for an azo stretch clearly indicated thebreaking of azo bond by B. laterosporus that would be an essentialand foremost step for the color removal. A peak at 1236 cm�1 forCeN stretch of AreNHeR suggests the formation of aromatic aminederivatives (Fig. 1).

Gas chromatogram (Fig. 2) of the degradation products extrac-ted after 48 h detected existence of four different intermediates.Table 1 illustrates the mass spectral analysis of degradationproducts. Fig. 3 illustrates proposed pathway for the degradation ofGolden Yellow HER by B. laterosporus. Recently, significant induc-tion of lignin peroxidase (156%), aminopyrine N-demethylase(120%), NADH–DCIP reductase (76%) and MG reductase (40%)during the decolorization of Golden Yellow HER by B. laterosporushas been reported (Gomare and Govindwar, 2009) which suggeststheir involvement in the degradation of Golden Yellow HER. Weassumed that parent dye molecule firstly undergo demethylation toform 2,5-Dichloro-4 (3-hydrazino-2-hydroxy cyclopentylamino-)dibenzene-sulfonic acid (peak 1, m/z ¼ 526) that would be facili-tated by aminopyrine N-demethylase. This intermediate moleculefurther undergo reduction to form 4-(3-hydrazino-2-hydroxycyclopentylamino)-benzene-sulfonic acid (peak 2, m/z ¼ 455) thatwould be facilitated by reductases. This molecule further cleavedinto 4-(3-amino-2-hydroxy-cyclopentylamino)-benzene-sulfonic

fragmentation pattern)

6 (13), 176 (7), 184 (27), 208 (20), 223 (7), 248 (7), 278 (7), 297 (10), 312 (13), 330 (7),92 (7), 511 (7), 526 (7).(14), 173 (7), 184 (29), 203 (7), 231 (7), 244 (7), 257 (7), 269 (7), 284 (7), 299 (7), 315

7 (14), 439 (7), 455 (21).6), 180 (100), 183 (6).55 (38), 177 (50), 191 (100), 208 (63), 212 (100), 228 (13), 240 (38), 257 (50), 267 (38),

(44), 397 (25), 409 (25), 425 (63), 445 (25), 455 (56), 472 (38), 485 (31), 495 (25), 523

SO2Na

N=N OH

H3C NH

Cl

Cl SO2Na

Golden Yellow HER (m/z = 538)

+ 2HCH3

SO2Na

N N OH

NH

Cl

Cl SO2Na

.

H

H

2 Cl -

SO2Na

N N OH

NH

SO2Na

H

H

NH2

SO2Na

+OH

NH

SO2Na

H2N

NH2

SO2Na

+ OHH2N

Mineralization

(Peak 3, m/z = 183)

(ND)

(Peak 2, m/z = 455)

(Peak 1, m/z = 526)

(Peak 3, m/z = 183)

.ND = Not detected in GC-MS

Fig. 3. Proposed pathway of Golden Yellow HER degradation by the B. laterosporusMTCC 2298.

Table 3Toxicity of Golden Yellow HER and its degradation products extracted after 48 h(1.0 g l�1) for the bacteria B. laterosporus, P. aeruginosa and A. vinelandii.

Bacteria Diameter of zone of inhibition (cm)

Golden Yellow Degradation products

B. laterosporus MTCC 2298 0.60 � 0.05 0.20 � 0.05*P. aeruginosa NCIM 2036 0.40 � 0.05 NIA. vinelandii NCIM 2821 1.10 � 0.05 0.30 � 0.05*

NI ¼ No zone of inhibition was observed.Values are the mean of three sets SEM (�). Data was analyzed by one-way ANOVATest. Bacterial inhibition due to the degradation products is significantly differentfrom the control dye at *P < 0.001 when compared by Tukey Kramer MultipleComparison Test.

S.S. Gomare et al. / International Biodeterioration & Biodegradation 63 (2009) 582–586 585

acid and 5-amino-cyclohex-3-ene-sulfonic acid (peak 3, m/z¼ 183)that would be facilitated by peroxidase. The 4-(3-amino-2-hydroxy-cyclopentylamino)-benzene-sulfonic acid would furthercleaved into the 3-amino-cyclohex-3-ene-sulfonic acid and

Table 2Toxicity of Golden Yellow HER and its degradation products extracted after 48 h (0.1 g l�

Parameters Sorghum vulgare

Plain water Golden Yellow Degradation pro

Germination (%) 100 50 90Plumule (cm) 4.99 � 0.47 0.63 � 0.09* 3.03 � 0.37**Radical (cm) 2.29 � 0.39 0.48 � 0.07* 2.12 � 0.28***

Values are the mean of ten germinated seeds of three sets SEM (�). Data was analyzsignificantly different from the seeds germinated in plain water at *P < 0.001 and the sgerminated in control dye at **P < 0.01, ***P < 0.001 when compared by Tukey Kramer

2-amino-cyclopentanol. The 2-amino-cyclopentanol mineralizedby the B. laterosporus. This is the first report on the biodegradationpathway of the Golden Yellow HER.

3.3. Toxicity of Golden Yellow HER and its degradation products

Table 2 illustrates significantly different lengths of plumule andradical of the seeds of S. vulgare and P. mungo grown in the water,control dye and its degradation products. Seed germination andplant growth bioassays are the most common techniques used toevaluate the phytotoxicity (Kapanen and Itavaara, 2001). Seedgermination has been regarded as a less sensitive method than rootlength (Fuentes et al., 2004). Phytotoxicity results of the presentstudy suggested that degradation products of Golden Yellow HERwere non-toxic to the common crops such as S. vulgare and P.mungo. Relative seed germination and relative root elongation of S.vulgare were 180 and 441% respectively; whereas that of P. mungowas 111 and 397% respectively. However, germination index of S.vulgare and P. mungo was 794 and 441 respectively.

Table 3 illustrates significantly different zone of inhibition ofB. laterosporus, P. aeruginosa and A. vinelandii against the controldye and its degradation products. Microbial toxicity resultssuggested non-toxic nature of degradation products for theecologically important bacteria like B. laterosporus, P. aeruginosaand A. vinelandii.

4. Conclusions

B. laterosporus decolorized 87% of Golden Yellow HER within48 h under static condition at the dye concentration 50 mg l�1. B.laterosporus showed maximum decolorization of Golden YellowHER by the bacterial culture without adjusting the pH of culturemedium. The optimum temperature for the decolorization ofGolden Yellow HER was 30 �C. Phytotoxicity results suggested thatdegradation products of Golden Yellow HER are non-toxic to thecommon crops such as S. vulgare and Phaseolus mungo and toecologically important bacteria like B. laterosporus, P. aeruginosaand A. vinelandii. Overall findings suggested need to exploit this

1) for the S. vulgare and P. mungo.

Phaseolus mungo

ducts Plain water Golden Yellow Degradation products

100 90 1007.88 � 0.54 4.42 � 0.62* 10.45 � 0.88***1.87 � 0.24 0.68 � 0.22* 2.70 � 0.29***

ed by one-way ANOVA Test. Seeds germinated in control Golden Yellow HER areeeds germinated in degradation products are significantly different from the seedsMultiple Comparison Test.

S.S. Gomare et al. / International Biodeterioration & Biodegradation 63 (2009) 582–586586

strain for further studies on the environmental friendly dyeremoval.

Acknowledgements

Authors are thankful to Department of Science and Technology,Govt. of India, New Delhi, India for funding the research work andYashwant Textile Processing, Ichalkaranji, Kolhapur, India forproviding the textile dyes.

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