Abstract
An investigation was conducted to assess the ability of three species of brown-rot fungi to decolorize and transform methyl orange dye. Methyl orange was decolorized in a potato dextrose agar medium by Fomitopsis pinicola, Gloeophyllum trabeum, and Daedalea dickinsii at different concentrations of 50, 75, and 100 mg L−1. Based on the values of the decolorization index, the highest methyl orange decolorization was found approximately 91% by F. pinicola, followed by D. dickinsii and G. trabeum of 82% and 76%, respectively, at a concentration of 50 mg L−1. F. pinicola had the highest methyl orange transformation with percent decolorization values of approximately 97%, followed by D. dickinsii and G. trabeum of 93% and 67%, respectively, after a 14-day incubation period in potato dextrose broth. F. pinicola transformed methyl orange into six metabolic products: compounds 3, 6, 7, 8, 9, and 10, while G. trabeum transformed methyl orange into five metabolic products: compounds 1, 2, 3, 4, and 5. Among brown-rot fungi, D. dickinsii had more metabolic products, with compounds 3, 4, 6, 11, 12, 13, 14, 15, 16, 17, and 18. Based on the identification of metabolic products, novel bio-transformation was proposed that brown-rot fungi initially transformed methyl orange via three pathways: (1) demethylation, (2) desulfonylation, and (3) hydroxylation. This study indicated that brown-rot fungi can be used to decolorize and transform methyl orange dye as well as proposed novel bio-transformation of methyl orange by brown-rot fungi.
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Introduction
The production of synthetic dyes has increased with the progression of consumerism, with most being used in textile industries. It was estimated that approximately 10–15% of dyes do not bind to the fibers during the coloring process and are therefore discharged into the environment (Camargo and Morales 2013). Azo dyes are the most important synthetic dyes, containing at least one azo group as the color-producing group, attached to substituted benzene or naphthalene rings. Azo dyes are classified as the most recalcitrant, persistent, and resistant dyes to the degradative environmental activities because of their chemical stability and versatility (Gutowska et al. 2007; Thao et al. 2013; Saroj et al. 2014). Apart from causing esthetic problems, most azo dyes have substantial toxic effects to the environment as well as humans. Methyl orange (MO) has been reported as a type of azo dye that is soluble in water, easily absorbed into the skin and inhaled, as well as a potential mutagenic and carcinogenic agent (Rafii et al. 1997; Wu et al. 2008; Sudha et al. 2014). Since the discovery of the harmful effects of MO (Shah et al. 2013; Bazrafshan et al. 2014; Grizca and Setyo 2018), a process of degradation of this dye is now required.
Some chemical and physical methods have been used and developed for the degradation of azo dyes, such as reductive degradation (Bigg and Judd 2001; Bokare et al. 2008), ozonation (Liakou et al. 1997; Yildirim et al. 2011), adsorption (Abramian and El-Rassy 2009; Roy et al. 2013), electrochemical (Ramirez et al. 2013), photocatalysis (Chen et al. 2011; Singla et al. 2014), and the Fenton reaction (Chacón et al. 2006; Peternel et al. 2007; Gomathi et al. 2009). The Fenton reaction is an effective technology with a catalytic oxidation process using hydrogen peroxide (H2O2) and ferrous ions (Fe2+) mixtures to produce hydroxyl radicals (·OH) as the current strongest oxidant known in biological systems for the destruction of a large number of hazardous and organic pollutants (Fenton 1894; Koenigs 1974; Wood 1994; Zhu et al. 2014). The treatment of azo dyes using the Fenton reaction has been reported previously (Chacón et al. 2006; Peternel et al. 2007; Gomathi et al. 2009); however, this method has a relatively high cost in practice and has the potential to destroy other environmental substances.
Biodegradation using microorganisms, especially fungi, is one of the most effective, cheap, and environmentally friendly methods for degrading some pollutants—including dyes (Purnomo 2017). Brown-rot fungi (BRF) have the biological Fenton reaction capable of generating hydroxyl radicals (·OH) that are able to degrade cellulose and hemicellulose effectively, as well as several xenobiotic compounds, such as 2,4,6-trinitrotoluene (Newcombe et al. 2002), chlorophenol (Schlosser et al. 2000), fluoroquinolone antibiotics (Wetzstein et al. 1997; 1999), aldrin and dieldrin (Purnomo et al. 2017a), DDT (Purnomo et al. 2017b; Sariwati et al. 2017; Sariwati and Purnomo 2018; Setyo et al. 2018), and dyes (Gomaa et al. 2010; Rizqi and Purnomo 2017). In our previous studies, three species of BRF, namely Fomitopsis pinicola, Gloeophyllum trabeum, and Daedalea dickinsii showed the greatest abilities in degrading DDT in liquid media (Purnomo et al. 2008; 2010c) as well as in contaminated soil (Purnomo et al. 2011a), with the Fenton reaction being used in the degradation mechanism (Purnomo et al. 2011b). In the current study, the ability of these BRF in degrading MO was investigated and compared with the characterization of the major metabolic products, and clarification of the degradation pathway also included. This was the first report on the bio-transformation of MO by BRF.
Materials and methods
Chemicals
Methyl orange (MO, C14H14N3NaO3S, molecular weight 327.34 g mol−1) was purchased from SAP Chemicals, while methanol, n-hexane, acetone, and N,N-dimethylformamide (DMF) were purchased from Wako Pure Chemical Industries (Osaka, Japan).
Fungi
The brown-rot fungi used in this study were F. pinicola NBRC8705, G. trabeum NBRC6509, and D. dickinsii NBRC31163 (NITE Biological Resource Center, NBRC; Chiba, Japan). These fungi were maintained on potato dextrose agar (PDA; Difco, Detroit, MI, USA) incubated at 30 °C as stock cultures.
Decolorization of MO in solid agar media
PDA was used for the solid agar media test, which had a varying MO concentration (0, 50, 75, and 100 mg mL−1, Jayasinghe et al. 2008). The mycelium of BRF (diameter 1 cm) were inoculated into the PDA medium containing MO and then incubated at 30 °C for 14 days. The mycelium (DM) diameter growth and the zone of color change (ZCC) on the agar plates were measured after the incubation period. The ability of BRF to decolorize MO was determined as the decolorization index (DI) using the following equation:
Biodegradation of MO in liquid media
The biodegradation of MO using BRF in PDB medium was performed in vivo. One plug (diameter 1 cm) of mycelia of stock cultures of BRF from a PDA plate was inoculated into 10 mL of potato dextrose broth (PDB; Difco, Detroit, MI, USA) in a 100-mL Erlenmeyer flask, which pre-incubated statically at 30 °C for 7 days.
After pre-incubation for 7 days, MO (final concentration: 50 mg L−1) was added to the cultures and incubated at 30 °C. The degradation of MO was monitored after 0, 7, and 14 days of treatments. The cultures were placed in 15-mL Falcon tubes and centrifuged at 4000 rpm for 10 min to obtain the biomass and supernatant, measured using a spectrometer UV–VIS at wavelength 400–650 nm in which the max wavelength of MO was 465 nm, while the rest were stored for metabolite product identification. For control, the cultures were performed without the addition of BRF. Percent degradation was calculated based on the equation:
where Abs0 and Abst are control and treatment absorbances, respectively.
Identification of metabolic products
The supernatant was analyzed using liquid chromatography–time-of-flight–mass spectrometry (LC–ToF–MS) to determine the metabolite products, and the electrospray ionization (ESI) had a mass range of 50–500 m/z. The column used was AcclaimTM RSLC 120 C18 2.1 × 100 mm with a particle size of 2.2 μm. The mobile phase was methanol to water at a ratio of 99:1 for 3 min, with a speed flow rate of 0.2 mL min−1 and 61:39 for 7 min with a rate of 0.4 mL min−1.
Statistical analysis
The results are presented as the average of triplicate measurements. Any statistically significant differences between or within groups during the MO transformation were determined by the t test, which a confidence level of 5% (P < 0.05) (Purnomo et al. 2010a; b, 2013, 2014).
Results and discussion
The Fenton chemical reaction had been used as an effective method for decolorizing azo dyes (Chacón et al. 2006; Peternel et al. 2007; Gomathi et al. 2009); however, it is relatively expensive and considered destructive to other environmental substances. Therefore, the biological Fenton reaction from BRF may be useful as a cheaper, environmentally friendly method. Previously, F. pinicola, G. trabeum, and D. dickinsii had been reported for their ability to degrade DDT by involving the Fenton reaction (Purnomo et al. 2008; 2010c; 2011a). In this study, bio-decolorization and bio-transformation of MO by these BRF were investigated and compared.
The decolorization of MO by BRF on a PDA medium was evaluated using PDA’s agar plate containing MO in different concentrations (final concentration 50, 75, 100 mg L−1), which was used as the initial screen to verify whether BRF could decolorize MO, as well as to determine its optimal concentration. The concentration of MO below 50 mg L−1 and above 100 mg L−1 produced vague and thick colors, respectively, thus making observation quite difficult. Previously, the same various concentrations (final concentration 50, 75, 100 mg L−1) were used to evaluate the decolorization of methylene blue (MB) by brown-rot fungus D. dickinsii (Rizqi and Purnomo 2017). The diameter growth mycelium (DM) and the zone of color change (ZCC) were used to evaluated the decolorization index (DI) that defines the ability of BRF in decolorizing MO. Based on the DM values, every tested BRF did not show a significant difference (P < 0.05) in growth in the PDA medium containing MO in all variation concentrations, except G. trabeum which grew in PDA containing 100 mg L−1 (Table 1). Through comparing the control medium (PDA without addition MO), it was found that the growth of all BRF did not show any significant differences (Table 1), indicating that MO was not toxic for BRF. Vasdev (2011) reported that the growth of six species of white-rot fungi (WRF) was not affected by the presence of dyes in the medium, implying that some fungi are able to tolerate and decolorize dyes for growth. Pycnoporus coccineus, Fomes fomentarius, Stereum ostrea, and Pycnoporus cinnabarinus have good mycelial growth in a medium containing MB, but they could not degrade methylene blue (MB) (Jayasinghe et al. 2008).
During a 5-day incubation period, the color of MO (orange) changed to red as a result of changes in the structure. These changes occurred due to variations in the pH of the PDA medium, which became acidic (Del Nero et al. 2005). It has been known in advance that the BRF produces some organic acids, such as oxalic acid (Takao 1965; Espejo and Agosin 1991). The low pH encouraged BRF to produce hydroxyl radical from the Fenton reaction (Akamatsu et al. 1992; Dutton and Evans 1996). After the 5-day incubation period, the red color began to decolorize. G. trabeum showed significant differences in decolorizing MO in various concentrations: the higher the concentration of MO, the lower the obtained decolorized zone was (Table 1). The highest decolorized zone was shown at an MO concentration of 50 mg L−1; however, F. pinicola did not show a significant difference in decolorizing, as well as D. dickinsii except at 100 mg L−1 concentration where it showed the lowest one (Table 1).
The ID values of each BRF in different concentrations of MO are shown in Table 1. In general, the higher MO concentration in the PDA medium, the lower the ID values obtained. G. trabeum showed significant differences in ID values of approximately 76, 70, and 56% in MO concentrations of 50, 75, and 100 mg L−1, respectively (Table 1). D. dickinsii did not show significant differences in the ID values except at an MO concentration of 100 mg L−1 that showed the lowest ones. F. pinicola also did not show significantly different ID values in all variation of MO concentration. These results indicate that at higher concentrations, BRF needs more activity to decolorize MO. In general, an MO concentration of 50 mg L−1 showed the highest BRF ID values, with F. pinicola showing the best BRF to decolorize MO with approximately 91% ID, followed by D. dickinsii and G. trabeum of 82% and 76%, respectively. Previously, D. dickinsii could decolorize MB with the highest ID value (92%) at 50 mg L−1 of MB (Rizqi and Purnomo 2017). Zeng et al. (2015) reported the same trend indicating that dye concentration has a negative effect on the decolorization percentage. It is assumed that high concentrations of dye result in slower decolorization rates. The Kocuria rosea (MTCC 1532) bacterium showed 100% decolorization of the MO (50 mg L−1) medium containing yeast extract (Parshetti et al. 2010), while Aeromonas sp. DH-6 reached nearly 100% decolorization of MO (100 mg L−1) after a 12 h incubation (Du et al. 2015). Based on this screening, 50 mg L−1 was selected as the concentration of MO in the liquid medium test.
Figure 1 illustrates the absorbance profile of MO during degradation by BRF, when MO was added to the pre-culture of all BRF (0 day), the absorbance of MO was decreased, and the orange color changed to red, indicating a transformation in structure due to the acid condition, where organic acids were formed during the pre-incubation of BRF. Besides producing organic acids, BRF may produce some secondary metabolites as well as the Fenton reaction to produce hydroxyl radicals during pre-incubation (Takao 1965; Espejo and Agosin 1991; Akamatsu et al. 1992; Dutton and Evans, 1996; Del Nero et al. 2005; Purnomo et al. 2008; 2010c; 2011a; Wahyuni et al. 2016). The results had a similar tendency in the degradation of MO in the PDA medium. Among BRF, the F. pinicola pre-culture showed the highest degradation at 0-day incubation, indicating that it is able to produce more organic acid or enzymes (Fig. 1c). On the other hand, the D. dickinsii pre-incubation culture showed the lowest degradation at 0-day incubation, suggesting that this fungus may produce a smaller amount of organic acids. During the degradation of MO for both 7 and 14 days, the MO absorbances were decreased slightly (Fig. 1), suggesting a degradation by BRF. The highest absorbance of MO was obtained at a wavelength of 465 nm, which was used to determine the degradation rate quantitatively by measuring percentage decolorization (PD).
Table 2 highlights the percentage decolorization (PD) and biomass dry weight of BRF during degradation. All of the BRF showed significant different weights, the longer the incubation times were, the higher the biomass was obtained. In each BRF, the higher biomass and PD values obtained indicated that biomass has a direct influence during MO degradation by the production of higher metabolic products or enzymes. G. trabeum showed the highest biomass, followed by F. pinicola and D. dickinsii of approximately 26, 25, and 23 mg, respectively, over the 14-day incubation period. G. trabeum, however, showed the lowest degradation rate at 67%, whereas F. pinicola showed the highest at 97% during the 14 days. This indicated that the quantity of biomass was not only the factor affecting the degradation rate, but also the type of fungus. Even though the F. pinicola and D. dickinsii biomasses were lower than G. trabeum biomass, they had a higher ability to degrade MO. Generally, it was assumed that the ability of BRF to degrade MO may be associated with the ability to produce extracellular enzymes (Singh et al. 2015; Wahyuni et al. 2017) and hydroxyl radicals generated by the Fenton reaction (Purnomo et al. 2008, 2010a, 2011b) (Fig. 1). However, to confirm the involvement of extracellular enzymes and the Fenton reaction in the degradation process, further investigation is needed.
LC–TOF/MS analysis showed that each BRF produced different metabolic products (Table 3), with most transforming MO via demethylation and hydroxylation as the main reaction. G. trabeum transformed MO into five metabolic products, namely 4-{[3-hydroxy-4-(methylamino)phenyl] diazenyl} benzenolate (m/z 242, compound 1), 4-{[4-(methylideneamino)phenyl] diazenyl} benzenolate (m/z 255, compound 2), 4-[(4-aminophenyl) diazenyl] benzene sulfonate (m/z 276, compound 3), 4-{[4-(dimethylamino)-3-hydroxyphenyl] diazenyl} benzene sulfonate (m/z 320, compound 4), and 4-[(4-amino-3,5-dihydroxyphenyl) diazenyl]-3-hydroxybenzene sulfonate (m/z 324, compound 5). On the other hand, F. pinicola transformed MO into six metabolic products, namely 4-{[4-(dimethylamino) phenyl] diazenyl} benzenolate (m/z 240, compound 6), 4-[(4-aminophenyl) diazenyl] benzene sulfonate (m/z 276, compound 3), 4-[(4-amino-3-hydroxy phenyl) diazenyl] benzene sulfonate (m/z 292, compound 7), 4-[(4-amino-3-hydroxy phenyl) diazenyl]-3-hydroxy benzene sulfonate (m/z 308, compound 8), 4-{[3-hydroxy-4-(methylamino)phenyl] diazenyl}3-hydroxy benzene sulfonate (m/z 322, compound 9), and 4-{[4-(dimethylamino)-3-hydroxy phenyl] diazenyl}-3-hydroxy benzene sulfonate (m/z 336, compound 10). Among the BRF, D. dickinsii had more metabolic products and the hydroxylation was more dominant over demethylation. The metabolic products of MO by D. dickinsii were N,N-dimethyl-4-phenyl diazenylaniline (m/z 225, compound 11), 4-{[4-(dimethylamino)phenyl] diazenyl} benzenolate (m/z 240, compound 6), 4-(phenyldiazenyl) benzene sulfonate (m/z 261, compound 12), 4-[(4-aminophenyl)diazenyl] benzene sulfonate (m/z 276, compound 3), 4-{[4-(dimethylamino)-3-hydroxyphenyl]diazenyl} benzene sulfonate (m/z 320, compound 4), 4-{[4-(dimethylamino)-3,5-dihydroxyphenyl]diazenyl} benzene sulfonate (m/z 336, compound 13), 4-{[4-(dimethylamino)-2,3,5-trihydroxyphenyl]diazenyl} benzene sulfonate (m/z 352, compound 14), -{[4-(dimethylamino)-2,3,5-trihydroxyphenyl]diazenyl}-3-hydroxybenzene sulfonate (m/z 368, compound 15), 4-{[4-(dimethylamino)-2,3,5-trihydroxyphenyl]diazenyl}-2,5-dihydroxybenzene sulfonate (m/z 384, compound 16), 4-{[4-(dimethylamino)-2,3,5-trihydroxyphenyl]diazenyl}-2,3,5-trihydroxybenzene sulfonate (m/z 400, compound 17), and 4-{[4-(dimethylamino)-2,3,5,6-tetrahydroxyphenyl]diazenyl}-2,3,5,6-tetrahydroxybenzene sulfonate (m/z 432, compound 18).
Some studies have reported that different mechanisms may be involved in the biodegradation of azo dyes such as enzymatic and non-enzymatic, as well as combinations of these mechanisms (Jadhav et al. 2008; Ayed et al. 2010). Among the enzymatic mechanisms, the involvement of laccase and azoreductase was often reported (Seesuriyachan et al. 2007; Parshetti et al. 2010; Ayed et al. 2010; Levin et al. 2012). Laccase is believed to be involved in the oxidation of the sulfonated side, while azoreductase is responsible for the reductive cleavage of the azo bridge (Jadhav et al. 2008; Ayed et al. 2010). Some metabolites (compounds 1, 2, 6, 11) were also detected as oxidation products of the sulfonated sides of MO, suggesting that laccase may be involved in the MO transformation by BRF. Some studies had reported laccase activity from G. trabeum (D’Souza et al. 1996), D. dickinsii (Mahmood et al. 2017), and F. pinicola (Park and Park 2014); however, since all of the identified metabolites of MO biodegradation by BRF were not products from the cleavage of the azo bridge, it is suggested that azoreductase is not involved in the MO biodegradation by BRF.
Based on the identification metabolites, MO degradation pathways were proposed (Fig. 2), by G. trabeum via three pathways: (1) demethylation to compound 3, followed by hydroxylation to compound 5, (2) desulfonylation that followed demethylation to compound 2, hydroxylation to compound 1, and (3) hydroxylation to compound 4. Also, F. pinicola transformed MO via three pathways: (1) demethylation to compound 3, followed by hydroxylation reactions to compounds 7 and 8, (2) hydroxylation to compound 10, followed by demethylation to compound 9, and (3) desulfonylation to compound 6. On the other hand, D. dickinsii also transformed MO via three pathways: (1) demethylation to compound 3, followed by deamination to compound 12, (2) desulfonylation to compound 6, followed by reduction to compound 11, and (3) hydroxylation to compound 4, then followed by several hydroxylation to compounds 13, 14, 15, 16, 17, and 18. Thus, BRF initially transformed MO via three pathways: (1) demethylation, (2) desulfonylation, and (3) hydroxylation.
Conclusion
The present study clarified that BRF can decolorize and transform MO in PDA and PDB media. F. pinicola was concluded to be the best among BRF in decolorizing MO with DI by approximately 91% in the PDA medium and to transform MO with approximately 97% of PD in the PDB medium, after a 14-day incubation. Based on the identification of metabolic products, BRF initially transformed MO via three pathways: (1) demethylation, (2) desulfonylation, and (3) hydroxylation. This is the first report regarding MO transformation that indicates BRF can be used to decolorize and transform the MO dye.
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This work was supported by the competency-based research Grant No. 1/E/KPT/2018 from the Directorate General of Strengthening Research and Development, Ministry of Research, Technology and Higher Education, Indonesia.
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Purnomo, A.S., Mauliddawati, V.T., Khoirudin, M. et al. Bio-decolorization and novel bio-transformation of methyl orange by brown-rot fungi. Int. J. Environ. Sci. Technol. 16, 7555–7564 (2019). https://doi.org/10.1007/s13762-019-02484-3
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DOI: https://doi.org/10.1007/s13762-019-02484-3