Chemosphere xxx (2014) xxx–xxx

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Technical Note

Decolorization and degradation of xenobiotic azo dye ReactiveYellow-84A and textile effluent by Galactomyces geotrichum

http://dx.doi.org/10.1016/j.chemosphere.2014.02.0090045-6535/� 2014 Elsevier Ltd. All rights reserved.

⇑ Corresponding author at: Department of Soil Science, Institute of Agricultureand Life Sciences, Gyeongsang National University, Jinju 660-701, South Korea. Tel.:+82 10 28203722.

E-mail address: tatobawaghmode@gmail.com (T.R. Waghmode).

Please cite this article in press as: Govindwar, S.P., et al. Decolorization and degradation of xenobiotic azo dye Reactive Yellow-84A and textile effluGalactomyces geotrichum. Chemosphere (2014), http://dx.doi.org/10.1016/j.chemosphere.2014.02.009

Sanjay P. Govindwar a, Mayur B. Kurade b, Dhawal P. Tamboli c, Akhil N. Kabra d, Pil Joo Kim e,Tatoba R. Waghmode a,e,⇑a Department of Biochemistry, Shivaji University, Kolhapur 416 004, Indiab Department of Biology, Hong Kong Baptist University, Kowloon, Hong Kongc Department of Environmental Engineering, Kyungpook National University, Daegu, South Koread Department of Environmental Engineering, Yonsei University, Wonju, South Koreae Institute of Agriculture and Life Sciences, Gyeongsang National University, Jinju 660-701, South Korea

h i g h l i g h t s

� G. geotrichum efficiently degrade azo dye as well as textile effluent.� Azo reductase was found to be the key enzyme in the degradation process.� Decolorization was improved by addition of waste agricultural residue in media.� HPTLC, FTIR and GCMS analysis were carried out to characterize degraded metabolites.

a r t i c l e i n f o

Article history:Received 5 December 2013Received in revised form 8 February 2014Accepted 10 February 2014Available online xxxx

Keywords:G. geotrichum MTCC 1360BiodegradationReactive Yellow-84AAzo reductaseLaccaseDecolorization

a b s t r a c t

Galactomyces geotrichum MTCC 1360 exhibited 86% decolorization of azo dye Reactive Yellow-84A(50 mg L�1) within 30 h at 30 �C and pH 7.0 under static condition. Examination of azoreductase, laccaseand tyrosinase enzyme activities confirmed their prominent role in Reactive Yellow-84A degradation.Considerable reduction of COD (73%) and TOC (62%) during degradation of the dye was indicative of con-version of complex dye into simple products, which were further analyzed by HPLC, FTIR, GC–MS andHPTLC. The degradation products were identified as 4(5-hydroxy, 4-amino cyclopentane) sulfobenzeneand 4(5-hydroxy cyclopentane) sulfobenzene by GC–MS. In addition, when G. geotrichum was appliedto decolorize textile effluent, it showed 85% of true color removal (ADMI removal) within 72 h, along witha significant reduction in TOC and COD. Phytotoxicity studies revealed the less toxic nature of degradedReactive Yellow-84A as compared to original dye.

� 2014 Elsevier Ltd. All rights reserved.

1. Introduction

Azo dyes are one of the oldest industrially synthesized organiccompounds characterized by presence of azo bond (AN@NA) andare widely utilized as coloring agents in textile, leather, cosmetic,paint, plastic, paper, and food industries (Hsueh and Chen, 2007;Khalid et al., 2008). Disposal of azo dyes from dyestuff synthesisand textile processing industry into the water resources causesreduction in water transparency and oxygen solubility (Lodatoet al., 2007; Corso and Almeida, 2009) and shows a negative impact

on germination and growth of plant species, that imbalances theecological function. So removal of textile dyes from the effluent be-fore its disposal in the water bodies is very important.

In the last few decades, several physicochemical methods havebeen developed for removal of dye from textile effluent, but thesemethods are not suitable due to the production of large amounts oftoxic sludge, aromatic amines, and secondary waste products(Alhassani et al., 2007). Numerous biotechnological approacheshave been suggested to overcome the problem of physiochemicaltreatment methods using microorganisms for the treatment of tex-tile dyes and industry effluent as microorganisms play crucial rolesin the mineralization of xenobiotic compounds (Kurade et al.,2012). The biodegradation of textile dyestuff is used widely be-cause of their cost effective, ecofriendly nature, and as well as pro-duces less toxic and/or non-toxic compounds (Wang et al., 2008).

ent by

2 S.P. Govindwar et al. / Chemosphere xxx (2014) xxx–xxx

Such bioremediation includes the use of fungal, yeast and bacterialcultures for the removal of dye from textile effluent (Stajic et al.,2006; Zhao et al., 2006; Waghmode et al., 2012a). In many circum-stances, the formed metabolites after degradation of textile azodyes show toxic or mutagenic effect (Phugare et al., 2011). There-fore, it is necessary to measure the toxicity of aromatic pollutantand their metabolites in order to assess the feasibility of the bio-degradation technique. Phytotoxicity assay of dyes and metabo-lites on seeds of Phaseolus mungo and Sorghum vulgare have beenreported for pollution monitoring (Kabra et al., 2011).

Being a mostly consumable azo dye, Reactive Yellow-84A (RY-84A) is responsible for severe pollution, as the unbound dye duringtextile processing is being discharged into water reservoirsthrough the effluent. Unfortunately, very few studies have reportedthe degradation of dye RY-84A by physicochemical aspects (Kochet al., 2002; He et al., 2007; Barka et al., 2010), while there is onlya single report on the biodecolorization of azo dye RY-84A byExiguobacterium sp. RD3 (Dhanve et al., 2009). Moreover, enzymesassociated with the decolorization or degradation of RY-84A inyeast species and the identification of metabolites by bioanalyticaltechniques have not been scrutinized before. The present studyevaluates the potential of using Galactomyces geotrichum MTCC1360 in the degradation and detoxification of the azo dye RY-84Aand investigates possible degradation pathways via enzyme stud-ies, FTIR and GC–MS analysis. The study also includes the effectof physicochemical parameters, carbon and nitrogen sources onthe dye decolorization potential of G. geotrichum. This study alsoassesses the toxicity of the dye and its metabolites based on phy-totoxicity using common agricultural crop seeds.

2. Materials and methods

2.1. Microorganisms and culture conditions

G. geotrichum MTCC 1360 was obtained from Microbial TypeCulture Collection, Chandigarh, India. The pure culture was main-tained on the malt extract agar at 4 �C. The composition of malt ex-tract medium (g L�1) was: malt extract, 3.0; yeast extract, 3.0;peptone, 5.0 and glucose, 10 for the decolorization studies.

2.2. Dyes and chemicals

The textile dye RY-84A, and effluent were obtained from localtextile industry, Ichalkaranji, India. DAB (3030-diaminobenzidinetetra hydrochloride) and riboflavin were purchased from Sigma(St. Louis, MO, USA). Remaining chemicals were obtained fromHi-media Laboratories and Sisco Research Laboratory, India. Allchemicals used were of the highest purity available and of analyt-ical grade.

2.3. Decolorization experiment and physicochemical parameters

Decolorization of RY-84A (50 mg L�1) was carried out understatic as well as shaking conditions at 30 �C in Erlenmeyer flaskscontaining 100 mL malt extract medium by G. geotrichum. Alldecolorization experiments were performed in triplicate anddecolorization was expressed in terms of percentage. Effect of dif-ferent pH (3-11) on the decolorization performance was studied byadjusting different pH of pre-grown culture medium by 1 N HCland 1 N NaOH before dye addition. Effect of temperature on thedecolorization performance was studied by incubating pre-grown(at 30 �C) culture at different temperatures (10–50 �C) after thedye addition. Aliquot (4 mL) of culture supernatant was withdrawnduring decolorization process and decolorization was monitoredby using UV–Vis spectrophotometer (Hitachi U 2800, Tokyo, Japan)

Please cite this article in press as: Govindwar, S.P., et al. Decolorization and degGalactomyces geotrichum. Chemosphere (2014), http://dx.doi.org/10.1016/j.che

at 420 nm at respective pH and temperature treatment. No changewas observed in the wavelength during the decolorization processdue to different pH and temperature adjustment. The potential ofG. geotrichum to tolerate higher concentrations of RY-84A (100–500 mg L�1) was also checked. Reduction in COD and TOC wasdetermined by using previously reported methods (Waghmodeet al., 2012a).

2.4. Effect of carbon, nitrogen sources and agricultural wastes ondecolorization

Bushnell Haas medium (BHM) is a mineral salt medium used forthis particular study to check the dye decolorization efficiency ofmicroorganism in the presence of different carbon and nitrogensubstrates. BHM composed of (g L�1) (MgSO4, 0.2; KH2PO4, 1.0;K2HPO4, 1.0; CaCl2, 0.02, FeCl3, 0.05; NH4NO3, 1.0) supplementedwith yeast extract (0.5) to study the effect of carbon (glucose,starch) and nitrogen (yeast extract, ammonium chloride, urea, pep-tone) sources at the concentration of 5.0 g L�1 on the decoloriza-tion of RY-84A (50 mg L�1). In addition to effect of syntheticcarbon and nitrogen sources, agricultural waste extracts werestudied on decolorization of RY-84A in BHM medium (5 mL extractof 10 g L�1 boiled agricultural residue).

2.5. Decolorization of textile effluent

G. geotrichum was tested to degrade textile effluent. For thispurpose, we prepared two types of textile effluent combinationwith malt extract medium including 80 mL effluent with 20 mLmalt extract medium (named as Type 1) and 60 mL effluent with40 mL malt extract medium (named as Type 2). The flasks wereinoculated with 24 h grown culture of G. geotrichum (approxi-mately 2 g wet wt) and kept for decolorization at 30 �C for 72 h un-der static condition. Decolorization of the textile effluent wascalculated by using American Dye Manufacturer’s Institute (ADMI3WL) tristimulus filter method (Kurade et al., 2012). Also degrada-tion was characterized by COD and TOC measurement afterdecolorization.

2.6. Preparation of cell-free extract

G. geotrichum was grown in the malt extract medium for 24 hand the biomass collected by filtration through Whatmann filterpaper No 1. The mycelium was then suspended in 50 mM sodiumphosphate buffer (pH 7.4) and sonicated based on a 60 amplitudeoutput, at 4 �C with 12 strokes of 30 s, each at 1 min intervals.The sonicated cells were centrifuged (4 �C, at 9000 rpm for25 min) and supernatant used as the source of intracellular en-zymes. A similar procedure was used to determine the enzymeactivities after RY-84A decolorization.

2.7. Enzyme analysis

The enzyme activities were assayed spectrophotometrically incell free extract and culture supernatant at room temperature(25 �C). Laccase, tyrosinase, azoreductase, NADH-DCIP reductase,and riboflavin reductase activities were determined according tothe procedure reported earlier (Tamboli et al., 2010a; Waghmodeet al., 2012b). One unit of enzyme activity was defined as amountof enzyme required to reduce 1 lM of substrate min�1 mg�1

protein.

2.8. Biodegradation analysis

The decolorization of RY-84A was monitored by using UV–Visspectrophotometer (Hitachi U 2800, Tokyo, Japan). The biomass

radation of xenobiotic azo dye Reactive Yellow-84A and textile effluent bymosphere.2014.02.009

Table 1Effect of carbon, nitrogen sources and agricultural waste on decolorization of RY-84Aby G. geotrichum MTCC 1360.

Media Decolorization (%)

BHM 16BHM + Wheat bran 75BHM + Wood shaving 16BHM + Rice husk 15BHM + Bagasse 13BHM + Glucose 66BHM + Glucose + Yeast extract 77BHM + Glucose + Ammonium chloride 87BHM + Glucose + Urea 19BHM + Urea 13BHM + Urea + Yeast extract 79BHM + Peptone 12BHM + Peptone + Yeast extract 60BHM + Starch 2BHM + Ammonium chloride 18

BHM – Bushnell Haas medium.

S.P. Govindwar et al. / Chemosphere xxx (2014) xxx–xxx 3

was removed after decolorization extracted with ethyl acetate;metabolite extracted with ethyl acetate dried over anhydrous Na2-

SO4 and dissolved in methanol and used for further analysis. HPTLCanalysis was performed by using HPTLC system (CAMAG,Switzerland) (Waghmode et al., 2012a). HPLC analysis was carriedout (Waters model 2690) on a C18 column (symmetry,4.6 mm � 250 mm) by isocratic method with 10 min run time(Phugare et al., 2011). FTIR analysis was done in the mid IR regionof 400–4000 cm�1 with 16 scan speed (Saratale et al., 2009). Theidentification of metabolites was carried using a QP2010 GC/MS(Shimadzu, Japan) (Kabra et al., 2011).

2.9. Phytotoxicity study

The degraded RY-84A after 30 h of decolorization was extractedwith ethyl extract, dried over anhydrous Na2SO4 and dissolved indistilled water to make a final concentration of 1000 mg L�1. Alsooriginal dye RY-84 was directly dissolved in distilled water to makethe 1000 mg L�1 concentration. Ten seeds of P. mungo and S. vulg-are plants were sown into a plastic sand pot with daily watering(5 mL) of original RY-84A (1000 mg L�1) and degraded RY-84A(1000 mg L�1) after 30 h treatment. Control set was carried outusing distilled water at the same time. Germination and lengthof shoot and root were recorded after 6 d.

Table 2Enzyme activities in G. geotrichum MTCC 1360 at (0 h) and 30 h of RY-84Adegradation.

Enzyme 0 h (beforedecolorization)

30 h (afterdecolorization)

Laccasea 0.07 ± 0.05 0.211 ± 0.03*

Intracellulartyrosinasea

1408 ± 451 1660 ± 342

Extracellulartyrosinasea

1217 ± 111 NA

NADH-DCIPreductaseb

183 ± 11 75 ± 1.8*

Riboflavin reductasec 14.3 ± 0.2 4.3 ± 1.2Azo reductased 5.5 ± 0.4 5.5 ± 1.4

Values are mean of three experiments ± SEM.a Enzyme unit is min�1 mg�1 protein.b Enzyme unit is lg of DCIP reduced min�1 mg�1 protein.c Enzyme unit is lg of riboflavin reduced min�1 mg�1 protein.d Enzyme unit is lM of methyl red reduced min�1 mg�1 protein.

* Significantly different from control cells at P < 0.001 by one-way ANOVA withTukey Kramer comparison test.

3. Results and discussion

3.1. Decolorization of RY-84A and physicochemical parameters

The G. geotrichum showed 86% decolorization of RY-84A(50 mg L�1) within 30 h, at 30 �C and pH 7.0 under static condi-tions, with a significant reduction in COD (73%) and TOC (62%).The G. geotrichum only showed 24% of degradation at shaking con-dition (120 rpm). The less decolorization in shaking conditionmight be due to the competition of oxygen and azo compoundsfor the reduced electron carriers under aerobic condition (Kuradeet al., 2011). Therefore, further study was continued at static con-dition. The decolorization of RY-84A was found at broader pH (3-11), and temperature (10–50 �C) range, but the optimum pH andtemperature were found to be 7.0 and 30 �C respectively. The pHwas slightly changed after 30 h of decolorization for respectivepH treatment, but the decolorization was due to microbial actionand not because of change in pH. This was confirmed by runningabiotic control (without G. geotrichum) during the decolorizationprocess. The G. geotrichum showed 77% of RY-84A decolorizationat 100 mg L�1 concentration and at 500 mg L�1 concentration itshowed 44% decolorization within 30 h.

3.2. Effect of carbon and nitrogen sources and agricultural waste

Biodegradation activity of G. geotrichum greatly varied accord-ing to the type of carbon and nitrogen sources used in the BHMmedium. In BHM medium (control), 16% decolorization of RY-84A was observed at 72 h. In an attempt to enhance decolorizationin control medium, the medium was supplemented with extra car-bon and nitrogen sources and extracts of agricultural residues (Ta-ble 1). It was found that wheat bran showed 75% decolorization.Also Tamboli et al. (2010b) showed the significant removal ofdye in the presence of agricultural residue in basal medium bySphingobacterium sp. ATM. Certain components present in wheatbran might be acting as an electron donor for the reduction ofazo dye. The medium supplemented with glucose showed 66%decolorization, whereas urea, peptone, starch and ammoniumchloride showed less decolorization which was very similar to con-trol. The BHM containing glucose in combination with ammonium

Please cite this article in press as: Govindwar, S.P., et al. Decolorization and degGalactomyces geotrichum. Chemosphere (2014), http://dx.doi.org/10.1016/j.che

chloride and yeast extract showed 87% and 77% of decolorizationrespectively, whereas glucose in combination with urea showed19% decolorization of RY-84A. Urea alone showed 13% of decolor-ization, but in combination with yeast extract it showed 79% decol-orization. Also peptone in combination with yeast extract showed60% decolorization. This showed concerted action of carbon andnitrogen sources in decolorization of RY-84A. An earlier studyreported that glucose and yeast extract act as electron donors forfaster decolorization of dye (Chen et al., 2003).

3.3. Enzymatic analysis

Induction of various enzymes during decolorization gives addi-tional insights into decolorization mechanism and supports the ac-tive role of microorganisms in the biodegradation process. Thesignificant induction in laccase (201%) and intracellular tyrosinase(78%) during decolorization of RY-84A by G. geotrichum as com-pared with control (before decolorization) (Table 2). No extracellu-lar tyrosinase activity was observed after decolorization. Previousstudy reported the involvement of laccase in textile dye degrada-tion (Tamboli et al., 2010a). Also azo reductase, NADH-DCIPreductase and riboflavin reductase showed their involvement inthe RY-84A decolorization. Azo reductase activity remainedconstant during decolorization, while NADH-DCIP reductase andriboflavin reductase showed 144% and 225% of reduction in activityafter decolorization as compared to control (before decolorization).

radation of xenobiotic azo dye Reactive Yellow-84A and textile effluent bymosphere.2014.02.009

Fig. 1. HPTLC chromatogram (a) and 3-D image profile (b) of original dye RY-84A(A) and its degraded RY-84A (B) obtained after decolorization by G. geotrichumMTCC 1360.

4 S.P. Govindwar et al. / Chemosphere xxx (2014) xxx–xxx

The earlier report confirms the role of azo reductase in degradationof dyes (Parshetti et al., 2010).

3.4. Decolorization of textile effluent

Tamboli et al. (2010a) showed the degradation of textile efflu-ent by Sphingobacterium sp. ATM, while Telke et al. (2010) usedPseudomonas sp. SU-EBT for degrading textile effluent. Textileeffluent decolorization varies with concentration of effluent inmixture of medium and effluent. The time required for decoloriza-tion decreases with less concentration (Type-2) of effluent in

Fig. 2. Proposed pathway and GC–MS chromatogram for the

Please cite this article in press as: Govindwar, S.P., et al. Decolorization and degGalactomyces geotrichum. Chemosphere (2014), http://dx.doi.org/10.1016/j.che

culture medium and increases with high concentration of effluent(Type-1) used. The COD and TOC were found to be higher for un-treated effluent than the treated effluent. The G. geotrichumshowed 43% of ADMI removal, along with 24% of COD and 16% ofTOC reduction for the Type 1 combination and Type 2 combinationshowed 85% ADMI removal as well as 58% of COD and 42% of TOCreduction.

3.5. Biodegradation analysis

The spectrophotometric analysis of degraded RY-84A culturesupernatant showed significant reduction in absorbance at420 nm as compared to original dye. HPTLC analysis of degradedRY-84A indicates different degradation pattern of dye (Fig. 1aand b). The differences in retardation factor values of original RY-84A (0.69) and degraded RY-84A (0.62, 0.78) indicates degradationof dye (Fig. 1a). HPLC of original dye showed major peak at reten-tion time 3.0 min and four minor peaks at different retention times,while degraded RY-84A showed three peaks at the different reten-tion time of 2.3, 2.7, 2.9 min which confirms the degradation of RY-84A.

Comparison of the FTIR spectrum of original dye and the de-graded RY-84A revealed the biodegradation of dye RY-84A by G.geotrichum. The FTIR analysis of RY-84A revealed the presence ofaromatic compound at 1490 cm�1, azo bond (N@N) at1614 cm�1, CH3 vibration at 1365 cm�1, OAH stretching at3471 cm�1, presence of sulfonic acid at 1041 cm�1 and1190 cm�1 indicates the nature of dye was sulfonated aromaticcompound. Also 673 cm�1 indicates the presence of halides (CACl).Whereas, the analysis of degraded RY-84A showed, amines as N-Hstretching at 3269 cm�1, CAH stretching at 2958 cm�1, C@Cstretching at 1450 and 1666 cm�1, benzene ring at 829 cm�1 andpresence of sulfonic group (S@O stretch) at 1041 and 1230 cm�1.

RY-84A after degradation by G. geotrichum MTCC 1360.

radation of xenobiotic azo dye Reactive Yellow-84A and textile effluent bymosphere.2014.02.009

Table 3Phytotoxicity of RY-84A (1000 mg L�1) and degraded RY-84A (1000 mg L�1) after 30 h of degradation by G. geotrichum MTCC 1360 for the Phaseolus mungo and Sorghum vulgare.

Observation Phaseolus mungo Sorghum vulgare

Distilled water RY-84A Degraded RY-84A Distilled water RY-84A Degraded RY-84A

Germination (%) 100 80 100 90 40 70Shoot length (cm) 10.24 6.40 8.29 1.89 0.72 0.84

±0.08 ±0.11* ±0.09$ ±0.03 ±0.01* ±0.01$

Root length (cm) 8.55 2.17 3.46 6.64 0.94 2.88±0.09 ±0.10* ±0.03$ ±0.03 ±0.02* ±0.01$$

Data was analyzed by one-way ANOVA Test and mentioned values are the mean of ten germinated seeds of three sets SEM (±).* Seeds germinated in RY-84A are significantly different from the seeds germinated in plain water at P < 0.001.

$ Seeds germinated in degraded RY-84A are significantly different from the seeds germinated in RY-84A at P < 0.05, when compared by Tukey Kramer Multiple comparisontest.

$$ Seeds germinated in degraded RY-84A are significantly different from the seeds germinated in RY-84A at P < 0.001 when compared by Tukey Kramer Multiple comparisontest.

S.P. Govindwar et al. / Chemosphere xxx (2014) xxx–xxx 5

Disappearance of peak at 1614 cm�1 for an azo group clearly indi-cates the breaking of azo bond by azoreductase.

The GC–MS analysis showed the probable cleavage productsproduced during the RY-84A biotransformation. On the basis ofinduction of various enzymes and mass spectrum analysis, the pos-sible RY-84A biodegradation pathway adapted by G. geotrichum isas illustrated in Fig. 2. The first step in the decolorization RY-84Acould include the cleavage of azo bond by the action of azo reduc-tase enzyme leading to the formation two intermediates [I] and[II]. Intermediate [I] was identified as 4(5-hydroxy, 4-amino cyclo-pentane) sulfobenzene (Retention time (Rt), 22.7, m/z-256). Fur-ther the deamination of intermediate [I] yields intermediate [III]identified as 4(5-hydroxy cyclopentane) sulfobenzene (Rt. 28.5,m/z-244).

3.6. Phytotoxicity study

The degraded RY-84A showed less or negligible inhibitory effecton shoot and root length of P. mungo and S. vulgare as compared tooriginal RY-84A (Table 3). Similar results were observed during thedecolorization study of Direct Orange 39 with P. aeruginosa strainBCH (Jadhav et al., 2010).

4. Conclusion

G. geotrichum can be used for the degradation of recalcitrantdyes as well as textile effluent. This organism tolerates 500 mg L�1

of dye concentration. Enzymatic studies indicate an important roleof azoreductase and laccase in biotransformation. Phytotoxicitystudy revealed less toxic nature of the degraded RY-84A as com-pared to original RY-84A. Our results indicate that G. geotrichumhas great potential towards textile dye degradation.

Acknowledgement

This study was supported by a grant from the BK 21 PLUS Pro-gram, division of applied life sciences, Republic of Korea andDepartment of Biotechnology, New Delhi, India.

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radation of xenobiotic azo dye Reactive Yellow-84A and textile effluent bymosphere.2014.02.009