Biodegradation of synthetic textile dyes by Mn … of synthetic textile dyes by Mn dependent peroxidase produced by Phanerochaete chrysosporium Rina D. Koyani, Sharma. R.K, Kishore

INTERNATIONAL JOURNAL OF ENVIRONMENTAL SCIENCES Volume 5, No 3, 2014

© Copyright by the authors - Licensee IPA- Under Creative Commons license 3.0

Research article ISSN 0976 – 4402

Received on August 2014 Published on November 2014 652

Biodegradation of synthetic textile dyes by Mn dependent peroxidase

produced by Phanerochaete chrysosporium Rina D. Koyani1, Sharma. R.K2, Kishore S. Rajput1

1- Department of Botany, Faculty of Science, The Maharaja Sayajirao University of Baroda, Vadodara 390002, India.

2- Department of Applied Chemistry, Faculty of Technology and Engineering, The Maharaja Sayajirao University of Baroda, Vadodara

[email protected] doi: 10.6088/ijes.2014050100059

ABSTRACT

Invention of permanent and un-removable dyes created a revolution in textile industries but at the same time posed a severe problem of ground water contamination due to their recalcitrant nature and its release in rivers. This problem can be resolved by application of ligninolytic enzymes produced by white rot fungus. Therefore, a wild strain of Phanerochaete

chrysosporium growing on dead wood logs collected from Girnar Forest (Gujarat, India) was evaluated for its biodecolourisation and biodegradation of common textile dyes (i.e. Reactive Golden yellow HRNL, Reactive yellow FG, Reactive orange 2R, and Reactive magenta HB). On the 11th day of inoculation, complete disappearance of all dyes except Reactive Yellow FG (which took only 9 days) was observed on solid and liquid medium. Growth media supplemented with different carbon and nitrogen sources enhanced the rate of decolourisation. Among them, dextrose and asparagine were found to be the best carbon and nitrogen sources respectively to boost up the rate of decolourisation. Visual decolourisation of dyes does not prove its degradation; therefore, breakdown of different bonds within dyes structure was confirmed by FTIR analysis of all dyes after treating with partially purified Manganese Peroxidase enzyme (52.8 kDa molecular weight) extracted from P. chrysosporium through solid state fermentation.

Keywords: Bioremediation, Dye degradation, Textile dyes, Mangnase peroxidise, Phanerochaete

1. Introduction

A demand for the higher production of synthetic dyes is directly related with the development of textile industries and degradation of the environment by releasing the effluent directly to the nature. According to Zollinger (1987), about 7×105 tons of dyes are produced every year worldwide, from which 280,000 tons of dyes are discharged as effluents by textile industries (Shah et al. 2012). Among them, azo dyes are the largest and very common group of dyes preferred by textile industries due to their amenable nature and they can be made to bind most synthetic as well as natural textile fibres (Selvam et al. 2003). Therefore, extermination of these dyes from the environment demands the cost effective and eco-friendly technique. Various technologies have been investigated in last two decades; however, these dyes are not readily removed or degraded from water by conventional wastewater treatment systems (Shaul et al. 1991). Another alternative i.e. bioremediation has been emerged as the most desirable and eco-friendly approach for the degradation of many pollutants in the waste water (Shararia et al. 2013). However, the efficiency of every fungus varies with respect to its ability to produce particular ligninolytic enzyme (peroxidases or laccase) having specified

Biodegradation of synthetic textile dyes by Mn dependent peroxidase produced by Phanerochaete

chrysosporium

Rina D. Koyani, Sharma. R.K, Kishore S. Rajput International Journal of Environmental Sciences Volume 5 No.3, 2014

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molecular weight. The pioneer production of ligninolytic peroxidases were recorded from P.

chrysosporium by earlier worker (Glenn and Gold 1983; Kuwahara et al. 1984) on the basis of decolourisation of dyes. Subsequently, several studies were carried out on the production of lignin and manganese peroxidases from P. chrysosporium, and its potential to degrade xenobiotic compounds including high molecular weight Poly Aromatic Hydrocarbons (Wariishi et al. 1989; Valli and Gold 1991; Armenante et al. 1994; Bumpus 1995; Moldes et

al. 2003; Alam et al. 2009; Koyani et al. 2013).

Many of the earlier studies on P. chrysosporium are based on liquid media under controlled conditions in laboratory. However, in the present investigation, we have tried to mimic the natural (field) conditions by cultivating it on different agro-industrial wastes as a Solid State Fermentation (SSF) media. Moreover, SSF is the most economical process for ligninolytic enzyme production (Mielgo et al. 2002; Koyani et al. 2013) and not only helps to overcome the problem of agricultural waste management but also leads to value added products. The cellulose, hemicelluloses and lignin present in the agricultural waste induces the ligninolytic enzyme production which is the plausible source for some industrial processes like biopulping and biobleaching, and of course for the bioremediation of wide range of xenobiotics compounds.

Our earlier study on P. chrysosporium has described degradation of Reactive Yellow MERL, Reactive Red ME4BL, Reactive Red HE8B, Reactive Black B, Reactive Golden Yellow HR, and Reactive Violet 5R. In the present study, Reactive Golden yellow HRNL, Reactive yellow FG, Reactive orange 2R, and Reactive magenta HB were utilised to study the degradation ability of wild strain of P. chrysosporium collected from the Girnar forest. Decolourisation and degradation of dyes were confirmed FTIR analysis of treated dyes.

2. Materials and method

2.1 Microorganism and growth media

Number of white rot fungal strains isolated and purified from fungal fruiting bodies and infected wood samples collected from the different forests of Gujarat state (India). They were screened by Bavendam test (Bavendam 1928) for the production of various lignin peroxidases from which a wild strain of P. chrysosporium was selected for the present study.

Initially, isolation of fungi was carried out by using various media to optimize the growth conditions, where Malt Extract Agar (MEA) medium was found to be most suitable for the rapid growth. Pure culture of Phanerochaete chrysosporium was revived regularly on freshly prepared media at the interval of every 15 days and maintained at 4 °C. Molecular identification of the strain was attained through Chromous Biotech Pvt. Ltd., Bangalore (India). On the basis of generated sequence, the fungus was identified as P. chrysosporium and the sequence was submitted to NCBI Gene Bank with accession number AB361645.

2.2 Chemicals

Malt Extract powder, Agar agar powder, dextrose, sucrose, fructose, maltose and lactose were procured from Himedia (India). Potassium di-hydrogen orthophosphate (KH2PO4), Di-potassium hydrogen orthophosphate (K2HPO4), Acetic acid, and different nitrogen sources (ammonium sulphate, sodium nitrate, sodium nitrite, urea and asparagine) were supplied by Qualigens Fine Chemicals Ltd., India. All the other chemicals used were commercially available products of analytical grade.


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Reactive textile dyes used in the study were kindly provided by Krishnakant Textile Industry (Gujarat, India). Dyes were selected on the basis of their structural diversity and frequency of use in the textile industries.

2.3 Decolourisation experiments

Dye decolourisation experiments in both solid and liquid media were evaluated on Malt Extract Agar (MEA) and Malt Extract Broth (MEB) respectively. Sterilized media supplemented with five different concentrations (10, 50, 100, 250 and 500 mg L-1) of dye were inoculated with actively growing culture of P. chrysosporium. The decolourisation efficiency on both solid and liquid medium was assessed by visual disappearance of colours from the plates and monitoring the decrease in the absorbance against the initial absorbance of control with a UV–visible spectrophotometer (Perkin-Elmer, USA) respectively. Detailed methodology is described in our earlier study (Koyani et al., 2013).

2.4 Effect of carbon and nitrogen sources on decolourisation

Five different sources of carbon (dextrose, sucrose, fructose, maltose and lactose) and nitrogen (Ammonium sulphate, Urea, Asparagine, Sodium nitrate and Sodium nitrite) were added to the medium to examine their influence on decolourisation as co-substrates (10 g L-1 concentration). Effect of these carbon and nitrogen sources on solid plate decolourisation was checked by measuring growth and decolourisation zone (cm) in two perpendicular directions of the plates at an interval of every 2 days. In case of liquid decolourisation, medium without any of the supplement was used as blank, whereas media with dyes and carbon/nitrogen sources but without inoculums were used as control. Decolourisation potential of the fungal isolates was measured at an interval of every 3 days using UV-visible spectrophotometer (Perkin-Elmer, USA) and percent decolourisation was calculated as per standard equation (Saratale et al., 2006).

2.5 Determination of enzymatic activity

Production of ligninolytic enzymes were supported by solid state fermentation (SSF). Among different agro-industrial substrates used for determining maximum enzyme production, wheat straw was found as the most appropriate substrate. Detailed methodology for optimization of solid substrates, inoculum size, incubation time, and enzyme production, their harvesting, assay, partial purification and molecular weight determination is mentioned elsewhere (Koyani et al., 2013).

2.6 Biodegradation analysis by FTIR (Fourier Transform Infrared Spectroscopy)

Decolourisation values achieved through the spectrophotometric measurements were checked by FTIR analysis to confirm the degradation of the compound. The samples prepared as the mixture of 10 ml of dye (10 mg L-1concentration) treated with 500 µl of partially purified enzyme were dried at room temperature and processed for the FTIR analysis by KBr pellet method using Shimadzu 8400, at 10-4 resolution and 30 scan.

3. Results and discussion

3.1 Microorganisms and growth media


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Collection of fungal fruiting bodies and infected wood logs were followed by isolation and purification of the selected strains and subjected to Bavendam test. Bavendam reaction showing the complete browning of the malt agar medium enriched with 1% tannic acid (Bavendam 1928), distinguished the white rot fungi. Among which P. chrysosporium (GenBank accession no. AB361645) was appropriately selected for the present study.

3.2 Solid plate decolourisation

The identification of potent species for dye decolourisation requires a screening method based on the direct measurement of substrate transformation such as colour removal (Field et

al., 1993). Dye decolourisation by fungi during growth on solid medium has been widely employed to identify the ligninolytic potential and ability to degrade xenobiotic compounds by Basidiomycetes (Shah and Nerud 2002; Wesenberg et al., 2003; Machado et al., 2006). In the present study, the growth tolerance and decolourising potential of P. chrysosporium was examined for the four diverse reactive textile dyes i.e. Reactive Golden yellow HRNL, Reactive yellow FG, Reactive orange 2R, and Reactive magenta HB. Dye decolourisation ability of the fungus depends upon the structure, type and the concentration of the dyes used. Therefore in the present investigation, four dyes representing different visible wavelength of absorbance (λmax) i.e. 408, 422, 481, and 558 were tested at five different concentrations (10, 50, 100, 250 and 500 mg L-1) and demonstrated for gradual disappearance of dyes from the plates. P. chrysosporium decolourised all the four tested dyes without inhibiting the mycelial growth up to the concentration of 100 mg L-1 but exceeding concentration gradually affected the growth as well as decolourisation rate. The dye decolourisation rate i.e. time required for the decolourisation, also varied according to the complexity of the dye (Figure 1, 2). In the present study, it was measured as the decolourisation zone from 3rd to 11th days of inoculation, where Reactive Yellow FG is decolourised completely after 9th day of inoculation while other three dyes were reached to their complete disappearance after 11th day of incubation (Figure 3). It indicates that Reactive yellow FG is structurally less complex than other three treated dyes.

Figure 1: Solid plate decolourisation of textile dyes. Reactive Golden Yellow HRNL (A: Control, B: Treated with P. chrysosporium); Reactive Yellow FG (C: Control, D: Treated with P. chrysosporium) at five different concentrations (10, 50, 100, 250 and 500 mg L-1-

from right to left).


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Figure 2: Solid plate decolourisation of textile dyes. Reactive Orange 2R (A: Control, B:

Treated with P. chrysosporium), and Reactive Magenta HB (C: Control, D: Treated with P.

chrysosporium) at five different concentrations (10, 50, 100, 250 and 500 mg L-1 from right to left).

Figure 3: On plate decolourisation measured as decolourisation zone (cm) against different

incubation time interval (days) treated with P. chrysosporium.

3.3 Liquid decolourisation

The azo dyes are recalcitrant for decolourisation and could be decolourised to a limited extent (Revankar and Lele 2007), in the present study liquid decolourisation method was also followed in search of confirm conclusion regarding decolourisation and degradation potential of P. chrysosporium. The decolourisation conducted in the liquid media was observed for complete disappearance of all four tested dyes in the flask containing 10 mg L-1 dye concentration. Although dyes with the different structures decolourized at different rate, P.

chrysosporium exhibited gradual vanishing of dye colour and ultimately complete decolourisation at 11th day of incubation (Figure 4). Evaluation for decolourisation was also measured as % decolourisation through comparative absorbance of control and treated dye


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solutions (Figure 5). Different concentration ranging from 10 to 500 mg L-1 was checked for their complete decolourisation in order to consider P. chrysosporium as efficient degrader of all four tested dyes (data not shown). Although, high concentration of dyes may show the toxic effect on fungi, in the present study concentration up to 500 mg L-1 of reactive dyes showed no inhibitory effect on the growth of the fungus.

Figure 4: Liquid decolourisation of Reactive Golden Yellow HRNL (A); Reactive Yellow FG (B); Reactive Orange 2R (C), and Reactive Magenta HB (D) at 10 mg L-1concentration (Control on right and treated on left) by P. chrysosporium after 9 days of incubation.

Figure 5: Percent decolourisation obtained at different time interval (days) using P.

chrysosporium.

Figure 6A Figure 6B

Figure 6: Influence of five different carbon sources on solid plate (A) and liquid decolourisation (B) inoculate with P. chrysosporium.


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Figure 7A Figure 7B

Figure 7: Effect of different nitrogen sources on decolourisation; on plate decolourisation (A) and liquid decolourisation (B).

3.4 Influence of carbon and nitrogen sources on decolourisation

There are no unanimous opinions regarding the effect of carbon and nitrogen sources. Available literature indicates that it may enhance (Dahiya et al., 2001; Machado et al., 2006), inhibit (Leatham and Kirk 1983; Tatarko and Bumpus 1998) or may not show any effect (Mester and Field 1997; Gianfreda et al., (1999) on of enzyme activity and dye degradation. Addition of supplementary nutrient sources i.e. five different carbon and nitrogen sources influences the decolourisation rate. After the addition of carbon sources (i.e. dextrose, fructose, sucrose, maltose and lactose) in the solid as well as in liquid decolourising media, dextrose was proved more competent than all other carbon sources tested in case of both the decolourisation methods (Figure 6), which is contrary to other reports (Knapp and Newby 1995; Özsoy et al., 2001; Eichlerova et al., 2006) which did not show any direct relationship between the carbon sources and decolourisation. In support to the present study, Dahiya et al., (2001) reported glucose as the best carbon source for supporting decolourisation. Supplementation of nitrogen sources in the growth media also play important role in the process of dye decolourisation (Moldes et al., 2004). This may be because; the nitrogen concentration in the culture medium influences the growth of fungi (Machado et al., 2006). In the present study, media was supplemented with various nitrogen sources (Ammonium sulphate, Urea, Asparagine, Sodium nitrate and Sodium nitrite) where aspargine was more supportive and conducive source for solid and liquid decolourisation than rest of the tested sources. In contrast, sodium nitrite was examined as effective growth inhibitor (Figure 7). In support of sodium nitrite as an inhibitor, there are reports that suppression of enzyme activity and inhibition of degradation is reported due to high nitrogen concentration by earlier researchers (Leatham and Kirk 1983; Tatarko and Bumpus 1998). On the other hand, Mester and Field (1997) and Gianfreda et al., (1999) noticed that some of the white rot fungi do not show any effect of carbon and nitrogen sources on ligninolytic enzyme production in the expected trend. Present study indicates that each fungal species respond specific to individual source of carbon and nitrogen.

3.5 Determination enzyme activity

The production of ligninolytic enzymes using the appropriate medium is crucial factor for the success of optimum enzyme production and their input in degradation (Koyani et al., 2013). Among different agro-industrial wastes verified for the optimum enzyme production by P.


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chrysosporium, wheat straw was the best supportive solid fermentative media and produced 607.35 IU mL-1 of Manganese peroxidase with 52.8 kDa molecular weight after 9th day of incubation period (data given elsewhere, Koyani et al., 2013). Gupte et al., (2007) observed the highest production of manganese peroxidase (20.2 IU mL-1) after 10 days of incubation with P. chrysosporium in media containing wheat straw, which is very less compared to the present report. Even the Molecular weight of MnP obtained from P. chrysosporium is recorded 46 kDa (Glenn and Gold 1985; Rüttimann-Johnson et al., 1994; Matsubara et al., 1996; Takano et al., 2004), while our study represents 52.8 kDa of molecular weight.

3.6 Fourier Transform Infrared Spectroscopy (FTIR) analysis of treated dyes

The difference between decolourisation of structurally different dyes is not easy to explain (Eichlerova et al. 2006); therefore, biodegradation of dye structure was analysed by FTIR, which pave the way towards understanding the structural changes occur during degradation of all tested reactive textile dyes. Spadaro et al., (1992) also reported that P. chrysosporium is capable of mineralizing a variety of toxic azo dyes and concluded that the mineralization of aromatic rings in azo dyes is dependent on the nature of ring substituent. If compared with control, FTIR spectra of all four tested dyes treated with partially purified enzyme exhibit the shifting of the peaks from their specific region reflecting the particular group i.e. ─N─H, ─N=N, ─C─H, ─SO2 to another positions which indicate the degradation of dyes (Figure 8A-D).

Figure 8A Figure 8B

Figure 8C Figure 8D

Figure 8: Comparison of the FTIR spectra of control dyes i.e. Reactive Golden Yellow HRNL (A); Reactive Yellow FG (B); Reactive Orange 2R (C), and Reactive Magenta HB

(D) and their degradation products extracted after 48 hours of reaction with partially purified enzyme produced by P. chrysosporium.


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4. Conclusion

Phanerochaete chrysosporium is a potential fungus that degrades Reactive Golden yellow HRNL, Reactive yellow FG, Reactive orange 2R, and Reactive magenta HB within 11 days of inoculation. Supplement of growth media with different sources carbon and nitrogen revealed dextrose and aspargine as best enhancer of the dye decolourisation process. On the basis of present study, it appears that each fungal species respond specific to individual source of carbon and nitrogen. Some of the sources of carbon or nitrogen may act as inducer while other may suppress or may not show any effect on the enzyme activity and its production. FTIR analysis of treated dyes showed shift in the peak value which confirms the biodegradation potential of P. Chrysosporium for very commonly used reactive textile dyes.

Acknowledgement

Authors gratefully acknowledge Council of Scientific and Industrial Research (CSIR), Government of India for financial support to carry out the present work. We are also thankful to the Editor, International Journal of Biodeterioration and Biodegradation for permitting us to reuse the enzyme data.

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Biodegradation of synthetic textile dyes by Mn … of synthetic textile dyes by Mn dependent peroxidase produced by Phanerochaete chrysosporium Rina D. Koyani, Sharma. R.K, Kishore