Abstract

Most currently employed textile effluent decolourization methods use physical and chemical processes where dyes do not get degraded instead concentrated or transferred into a solid phase. Therefore, further treatment processes are required to destroy dyes from the environment. In contrast, biological decolourization may result in degradation of the dye structure due to microbial activities and hence biological processes can be considered environmentally friendly. In the present study, bacterial strains with dye decolourization potential were isolated from the natural environment and their ability to decolourize four different reactive textile dyes was studied individually and in a bacterial consortium. The developed bacterial consortium composed with Proteus mirabilis, Morganella morganii and Enterobacter cloacae indicated more than 90% color removals for all four dyes and optimum decolourization of the dye mixture was observed at 40 °C and pH 7. The developed bacterial consortium decolourized 60% of dyes in textile industry effluent at 35 °C and pH 7 showing their ability to endure in highly complex and toxic environments and application in textile industry wastewaters.

INTRODUCTION

Textile dyes used in industry can be classified based on their structure as azo, anthraquinone, sulfur, indigoid, triphenylmethyl (trityl), and phthalocyanine derivatives (Forgacs et al. 2004) and depending on the application, as reactive, acid, direct, basic, mordant, disperse, sulphur, and vat dyes (Popli & Patel 2015). Out of these, reactive dyes are highly significant and the most widely used class of dyes which are especially used for the coloration of cotton fibers in textile industries (Chinta & Vijaykumar 2013).

Wet processing (dyeing) of textiles consumes large quantities of water and during processing, part of the dyes remains unfixed generating colored effluent. Discharge of these colored effluents into water bodies may result in reduction of light penetration through water and thus affect the photosynthetic activities of aquatic flora thereby severely affecting the food sources of aquatic organisms (Pereira & Alves 2012). Dyes are toxic to flora, fauna and humans and, further, degradation of dyes may deplete dissolved oxygen levels in water affecting aquatic organisms (Solís et al. 2012). Hence, textile industry is considered as one of the major contributors in environmental pollution and the second highest water polluter in the world (Kant 2011).

Different effluent treatment methods such as coagulation–flocculation, adsorption on activated carbon, membrane-filtration processes (nano filtration, electro dialysis, reverse osmosis) chemical oxidation methods (e.g. with H2O2, ozone), irradiation and advanced oxidation processes or electrochemical processes (e.g. electro oxidation, electro kinetic coagulation) are used in textile industries to treat colored effluent (Babu et al. 2007; Singh & Arora 2011; Pereira & Alves 2012). These physical and chemical effluent treatment methods have several drawbacks such as high cost (UV irradiation, chemicals for precipitation as well as for pH adjustments, electricity), problems associated with dewatering and disposing of generated sludge, high concentration of residual cation levels left in the supernatant, not effective for the decolourization of all dye types (Anjaneyulu et al. 2005).

The most widely used effluent treatment method, coagulation and flocculation (dos Santos et al. 2007); is effective for decolourization of sulphur and disperse dyes but not for reactive dyes due to their high water solubility (Singh & Arora 2011; Verma et al. 2012).

Effective decolourization of textile reactive dyes by different microorganisms such as P. mirabilis (Olukanni et al. 2010) and P. luteola (Chen 2002) have been reported in literature. Biological decolourization of textile dyes is mainly due to the change of dye structure with the degradation of bonds. Some bacterial species have ability to completely mineralize dyes (Olukanni et al. 2010) without producing secondary sludge with concentrated dye particles. Hence, this method can be considered a more environmentally friendly technique than chemical and physical methods for decolourization of textile dyes.

Even though biological methods have more benefits over physical and chemical treatment methods for dye decolourization, adaptation of dye decolourization microorganisms to textile industry effluent is challenging. Most of the reported studies have been conducted on decolourization of individual textile dyes by isolated microorganisms in synthetic medium. However, in this work, decolourization potential of four reactive textile dyes by microbial strains isolated from the natural environment and their applicability in industrial wastewater decolourization were investigated.

MATERIALS AND METHODS

Effluent sampling

Sludge containing effluent sample was collected from the oxidation ditch, of a local textile processing facility located in Colombo district, Sri Lanka. The sample was brought to the laboratory on an ice pack in a cooler box and stored at 4 °C until used.

Dyes and chemicals

Commercial grade Sumifix Supra Yellow EXF (Yellow EXF), Sumifix Supra Red EXF (Red EXF), Sumifix Supra Blue EXF (Blue EXF) and Cibacron Black WNN (Black WNN) dyes were obtained from a local textile dyeing industry (each of these dyes is a mixture of reactive dyes; structures of dyes except black WNN dye are not revealed due to trade secrets). According to the material safety data sheet, 60–70% of Black WNN dye is composed of sodium 4-amino-5-hydroxy-3,6-bis [[4-[[2-(sulfooxy)ethyl]sulfonyl]phenyl]azo]-2,7-napthalene disufonate (CAS number-17095-24-8) and its structure is given in Figure 1. Even though the structures of Sumifix Supra dyes are not available, they are reported as bifunctional reactive dyes containing aminochlorotriazine-sulphatoethylsulphone groups (Ghaly et al. 2014). All the chemicals used for media preparation were procured from Hardy diagnostics (USA) and MP Biomedicals (USA). Chemicals used for polymerase chain reaction (PCR) analysis were of molecular grade and purchased from Promega, USA.

Figure 1

Structure of major dye in Black WNN.

Figure 1

Structure of major dye in Black WNN.

Isolation of dye decolourizing microorganisms

The isolation method of microorganisms that have the ability to decolourize dyes has been reported elsewhere (Madhushika et al. 2019). Identification of these strains was done by conducting biochemical tests, considering the morphological characteristics and sequencing analysis of 16S rRNA gene.

16S rRNA sequencing analysis

A single colony of each selected bacterial strain was suspended in 20 μL of nuclease-free water separately in Eppendorf tubes. Each bacterial suspension was incubated for 20 min at 95 °C and centrifuged at 10,000 × g for 5 min. The supernatants were used as total genomic samples. The bacterial 16S rDNA gene was amplified from the total genomic DNA using universal primers 27F 5′ (AGA GTT TGA TCM TGG CTC AG) 3′ and 1492R 5′ (TAC GGY TAC CTT GTT ACG ACT T) 3′ (Integrated DNA Technologies, USA). The PCR conditions were 30 cycles at 95 °C denaturation for 30 s, annealing at 53.1 °C for 30 s and extension at 72 °C for 1 min, in addition, one cycle of extension at 72 °C for 5 min. The PCR product was purified by Wizard SV Gel and PCR clean up system (Promega, USA). Purified products were sent to Macrogen, Korea for sequencing. The resultant nucleotide sequences were analyzed by Blast-n site at NCBI server (www.ncbi.nih.gov/BLAST). Bacterial species were identified based on the blasting results.

Decolourization experiments

Mineral salt medium used for the decolourization studies was composed of 12.8 g/L Na2HPO4.7H2O, 3 g/L KH2PO4, 0.5 g/L NaCl, 1.0 g/L NH4Cl, 5.0 g/L yeast extracts and the pH was adjusted to 7. 100 mL of this medium was transferred to 250 mL Erlenmeyer flask and sterilized at 121 °C for 20 min. Dye solutions were filter sterilized with 0.2 μm membrane filters and mixed with the mineral salt medium to obtain final dye concentration of 50 mg/L. This dye containing mineral salt medium was used in all decolourization experiments unless otherwise mentioned.

Dye mixture was prepared by adding equal volumes of Yellow EXF, Red EXF, Blue EXF and Black WNN dye solutions having the same concentration and then mixing with sterilized mineral salt medium to obtain the final dye concentration of 50 mg/L.

Bacterial isolates (I1, I2, I3, I4 and I5) were pre-cultured in LB medium and incubated at 35 °C for 24 h. The sterilized mineral salt media containing each dye and dye mixtures were inoculated with 2% (v/v) (optical density adjusted to 0.3) of the inoculum and incubated at 35 °C under static (anoxic) conditions.

The bacterial consortium was developed by mixing equal volumes (optical density adjusted to 0.3) of 24 h grown cultures of I1, I3 and I4. 2% (v/v) of the constructed bacterial consortium was used as the inoculum where necessary.

5 mL samples were withdrawn from dye containing mineral salt medium at defined time intervals and centrifuged at 10,000 g (12,000 rpm) at 28 °C for 10 min. The supernatant was scanned at maximum absorbance wavelengths (λmax) of each dye under visible light in a spectrophotometer (UV-1800 Shimadzu spectrophotometer). Wavelengths of 422, 544, 606.5, 598 and 553 nm were considered as maximum absorbance wavelengths of Yellow EXF, Red EXF, Blue EXF, Black WNN and dye mixture, respectively. The uninoculated dye-free medium was used as the blank. All assays were performed in duplicate and compared with control (uninoculated dye containing medium).

Percentage dye decolourization was calculated by using Equation (1).
formula
(1)
where Ainitial is the absorbance before decolourization and Afinal is the absorbance of corresponding inoculated samples at a specific time. Each decolourization value is the mean of two parallel experiments.

Effect of temperature

Mineral salt medium containing dye mixture was inoculated with the bacterial consortium and incubated at 25, 30, 35, 40 and 45 °C temperatures to study the effect of temperature on decolourization of dyes. Samples were collected after 28 and 45 h of inoculation and evaluated for decolourization.

Effect of pH

In order to investigate the effect of pH on biological dye decolourization, the initial pH of the mineral salt medium was adjusted to 6, 7, 7.5, 8, and 9. Dye mixture containing samples were then inoculated with the bacterial consortium. Samples collected after 26 and 50 h incubations were used for the evaluation of percentage decolourization.

Textile effluent decolourization studies

Textile effluent samples for decolourization studies were obtained from two different textile processing companies (companies X and Y) in Sri Lanka. Effluent samples were collected from the inlet of the wastewater treatment plant prior to any treatment and the chemical oxygen demand (COD), biochemical oxygen demand (BOD), temperature and pH of the wastewater were recorded. Then pH of the effluent samples was adjusted to 7. Effluent samples were then sterilized by autoclaving at 121 °C for 20 min. Sterilized yeast extract (final concentration of 5 g/L) was added to 100 mL of effluent. Samples were inoculated with 2% (v/v) bacterial consortium. Absorbance values of the prepared samples were measured using the UV-visible spectrophotometer and percentage decolourization was calculated using Equation (1).

RESULTS AND DISCUSSION

Five bacterial strains that have the dye decolourization potential were selected from nutrient broth (test tube) screening. During screening, Yellow EXF was decolourized by strains I1, I3, I4, and I5, Red EXF by I1 and I4, Blue EXF by I1, I3 and I4 and Black WNN by I1, I2, I3 and I4. Based on 16srRNA gene sequencing analysis, each of these strains was identified (Table 1).

Table 1

Description of the isolated micro-organisms

CodeShapeGram stainingCatalaseBacterial species
I1 Rod Negative Positive Proteus mirabilis 
I2 Rod Negative Positive Escherichia fergusonii 
I3 Rod Negative Positive Morganella morganii 
I4 Rod Negative Positive Enterobacter cloacae 
I5 Short rod Negative Positive Acinetobacter baumannii 
CodeShapeGram stainingCatalaseBacterial species
I1 Rod Negative Positive Proteus mirabilis 
I2 Rod Negative Positive Escherichia fergusonii 
I3 Rod Negative Positive Morganella morganii 
I4 Rod Negative Positive Enterobacter cloacae 
I5 Short rod Negative Positive Acinetobacter baumannii 

Time-dependent decolourization of each dye (Yellow EXF, Red EXF, Blue EXF and Black WNN) by individual bacterial strains and consortium was studied in batch (in flasks) experiments. After 30 h incubation, 90% decolourization of Yellow EXF was indicated by I1 and bacterial consortium (Figure 2(a)). After 46 h incubation, I4 containing samples also indicated more than 94% decolourization. Compared to other strains, I5 indicated the lowest color removal.

Figure 2

Decolourization of (a) Yellow EXF, (b) Red EXF, (c) Blue EXF and (d) Black WNN dyes by isolated bacterial strains.

Figure 2

Decolourization of (a) Yellow EXF, (b) Red EXF, (c) Blue EXF and (d) Black WNN dyes by isolated bacterial strains.

After 72 h incubation, the highest percentage removal of Red EXF was exhibited by I1 (Madhushika et al. 2018). Samples decolourized with bacterial consortium showed slightly lower decolourization rates at early stages compared to I1 however, reached 94% decolourization at 72 h (Figure 2(b)). During the first 24 h incubation, color removal by I4 was low, but decolourization percentage increased with time and 89% reduction was observed after 72 h.

Blue EXF decolourization was more effective with bacterial consortium than with individual bacterial strains (Figure 2(c)). From the identified individual strains, I1 indicated the highest color removal of 83% after 72 h incubation.

As shown in Figure 2(d), Black WNN was effectively decolourized by bacterial isolates as well as the bacterial consortium and obtained more than 90% removal of color after 72 h incubation. However, overall, highest decolourization was exhibited by bacterial consortium and the lowest performance was by I3.

Biological decolourization of textile dyes are mainly due to breakage of dye structures by enzymatic activity of micro-organisms. As reported in the literature, enzymes such as azo reductases, laccase and veratryl alcohol oxidase produced by bacteria (Olukanni et al. 2010) are involved in the degradation of azo dyes. In a bacterial consortium, different bacterial strains may secrete various enzymes to attack different subgroups of dye particles (Phugare et al. 2011) and, further, some strains may catabolize the intermediate products produced by other strains.

Decolourization potential of Yellow EXF, Red EXF, Blue EXF, Black WNN and dye mixture by strain I1 was discussed elsewhere (Madhushika et al. 2019). In the current study, a comparative analysis on dye decolourizing ability of individual bacterial strains and the bacterial consortium was conducted. Out of the selected bacterial strains, I1 was able to decolourize all four dyes effectively and was able to decolourize Yellow EXF and Red EXF dyes more rapidly than by the bacterial consortium. However, the decolourization of Blue EXF and Black WNN dyes were more effective with bacterial consortium than the individual bacterial strains. Dye mixture decolourization studies conducted with the best performing strain I1 showed 72% of decolourization after 46 h incubation where bacterial consortium indicated 83% decolourization. Hence, utilization of bacterial consortia in the decolourization of a mixture of dyes or industrial textile effluents is more effective compared to individual strains.

According to literature, azo dyes are biologically degraded due to the breakage of the azo bond in the dye structure which is the chromophore group that results in the color of the dye molecule. As azo dyes are electron-deficient compounds, electrons need to be provided for the cleavage of azo bond (Chen et al. 1999). Under anaerobic or oxygen-limited conditions, azo dyes behave as the final electron acceptor of the bacterial electron transport chain (Pandey et al. 2007) and fulfill the requirement of electrons for the degradation of the dye. Because of this, high color removals can be observed under static conditions. However, under aerobic or shaking conditions where oxygen concentrations in the medium is high, oxygen will accept electrons more effectively than azo dyes resulting less color removals.

Out of the five isolated bacterial strains, Acinetobacter baumannii is an aerobic bacterium, whereas all the other four strains are facultative anaerobes. During this study, dye decolourization experiments were conducted under static conditions where oxygen concentrations in the medium was low. This oxygen-limited conditions may negatively affect the growth of aerobic bacteria, Acinetobacter baumannii than the other bacterial strains. This could be the reason for the observed low percentage color removals by A. baumannii in decolourization of Yellow EXF dye. However, when decolourization studies were conducted under shaking conditions, A. baumannii indicated only 3% decolourization of Yellow EXF dye (results not shown). Even though high cell growth was observed, dye decolourization was not effective under shaking conditions. As the growth and existence of A.baumannii was not possible under oxygen-limited conditions, this strain was omitted when developing the bacterial consortium.

Within the initial 28 h, the highest color removal of the dye mixture by the bacterial consortium was observed in samples incubated at 35 °C (Figure 3(a)). However, after 45 h incubation, the highest dye decolourization was detected in samples incubated at 40 °C. All samples showed more than 70% decolourization after 45 h incubation.

Figure 3

Effect of (a) temperature and (b) pH on decolourization of the dye mixture by the developed bacterial consortium.

Figure 3

Effect of (a) temperature and (b) pH on decolourization of the dye mixture by the developed bacterial consortium.

As shown in Figure 3(b), dye mixtures of pH 7, 7.5 and 8 indicated the highest color removal after 26 h incubation with the bacterial consortium. However, after 50 h, the highest percentage decolourization was observed in the culture of pH 7. Samples in which the pH was adjusted to 10 indicated the lowest color reductions.

According to the obtained results, the temperature and the pH conditions of mineral salt medium containing dye mixture have influenced the color removal rates. Different degrees of decolourization were observed when the pH of the medium varied from 6 to 10 and the incubation temperature varied from 25 to 45 °C. The effect of temperature and pH on the growth and enzymatic activities of cells could be the reason for observed variations. These enzymatic activities have a great influence on cellular activities and consequently on dye decolourization. The highest dye decolourization was observed at temperature 40 °C and at pH 7, which is the most favorable condition for the growth of considered bacteria.

During the current study, effective dye decolourization was observed throughout the considered temperature range of 25–45 °C, however, considerable colour reduction was not observed in the samples incubated at pH 10. Loss of cell viability and denaturation of dye decolourizing enzymes at higher pH conditions could be the reason for this behavior.

Characteristics of textile industry effluents used in this study are given in Table 2.

Table 2

Characteristics of textile industry effluents

Effluent characteristicsEffluent XEffluent YTypical ranges reported in literatureReferences
Temperature (oC) 45 48 35–45 Yaseen & Scholz (2019), Ghaly et al. (2014), Upadhye & Joshi (2012)  
pH 9.7 10 6–10 Yaseen & Scholz (2019), Ghaly et al. (2014), Upadhye & Joshi (2012)  
COD (mg/L) 850 902 150–12,000 Yaseen & Scholz (2019), Ghaly et al. (2014), Upadhye & Joshi (2012)  
BOD (mg/L) 445 200 80–6,000 Yaseen & Scholz (2019), Ghaly et al. (2014)  
Effluent characteristicsEffluent XEffluent YTypical ranges reported in literatureReferences
Temperature (oC) 45 48 35–45 Yaseen & Scholz (2019), Ghaly et al. (2014), Upadhye & Joshi (2012)  
pH 9.7 10 6–10 Yaseen & Scholz (2019), Ghaly et al. (2014), Upadhye & Joshi (2012)  
COD (mg/L) 850 902 150–12,000 Yaseen & Scholz (2019), Ghaly et al. (2014), Upadhye & Joshi (2012)  
BOD (mg/L) 445 200 80–6,000 Yaseen & Scholz (2019), Ghaly et al. (2014)  

The maximum absorbance of the effluent obtained from company X was observed at 521 nm wavelength. After the biological treatments, a clear shift of UV-visible spectrum of the effluent sample was observed due to reductions in absorbance values, indicating the dye decolourization (Figure 3(a)).

Time-dependent decolourization studies conducted with the bacterial consortium for effluents obtained from company X indicated 60% decolourization within 138 h at 521 nm (Figure 5). However, UV-visible spectrum of effluent obtained from company Y did not show any peak in the visible range of the spectrum (Figure 4(b)). In textile dyeing industries, a large number of different dyes are simultaneously used (for different fabrics) and all of these dyes get mixed with the wastewater. The UV-visible spectrum for a dye mixture is the resultant absorbance of all absorbing functional groups of the dyes present in the effluent. Hence, it is not possible to identify a maximum absorbance wavelength for most textile dyeing effluents and these absorbance values can vary with the change of effluent composition

Figure 4

UV-visible spectrum of company (a) X and (b) Y effluents before and after biological treatments.

Figure 4

UV-visible spectrum of company (a) X and (b) Y effluents before and after biological treatments.

Figure 5

Decolourization of company X and Y effluents by bacterial consortium.

Figure 5

Decolourization of company X and Y effluents by bacterial consortium.

Hence, for the calculation of percentage decolourization of company Y effluent, three wavelengths 436, 525 and 620 nm were selected as representative points to cover the visible range following ISO 7887:2011 standard (ISO 7887 2011). Color reductions of 34%, 46% and 61% were observed for effluent obtained from company Y at 436, 525 and 620 nm wavelengths, respectively, after 24 h incubation (Figure 5). However, further considerable color reductions were not observed in this effluent, even with 138 h incubation.

Textile industry effluent may contain large quantities and varieties of chemical substances such as salts, detergents, and organic acids (Hessel et al. 2007). High salt concentrations and toxicity of these chemical substances may negatively affect microbial growth. Hence, use of biological decolourization techniques for textile effluent is considered to be a difficult task. However, during this study, the developed bacterial consortium was able to remove 60% color of the effluent obtained from company X within 138 h (Figure 5). Effluent collected from company Y also indicated color reductions on all three considered wavelengths within the first 24 h incubation, however, further considerable reductions were not observed thereafter (Figure 5). Company Y is a sewing thread manufacturing company and prominently uses disperse and vat dyes for the dyeing process. Company X is a weft-knitted fabric manufacturing company widely use reactive textile dyes in their processing. So based on the decolourization results obtained, it can be considered that the developed bacterial consortium have the ability to decolourize textile effluents that consist of different types of dyes.

The ability of different bacterial strains to decolourize synthetic dye solutions are widely reported in literature. However, a limited number of publications report about the bacteria which have the ability to decolourize textile effluents (Agarry & Ajani 2011; Valli Nachiyar et al. 2014). Among them also very few have directly use textile effluent for the decolourization studies without dilutions. However, in the current study, textile effluent was directly used without dilution and was able to decolourize successfully. This implies the capability of the developed bacterial consortium to withstand the toxicity of industrial effluent.

Two textile processing companies considered in this study use chemical coagulation and flocculation technique for the decolourization of effluent like many other textile industries. Further, most of the textile dyeing industries already use conventional aerobic treatment techniques for the reduction of COD and BOD loads of the effluents. Introduction of anaerobic treatment units prior to aerobic treatment will be more economically feasible and environmentally friendly than the currently employed dye decolourization techniques. Moreover, anaerobic systems have the ability to reduce effluent COD values (Somasiri et al. 2008) in addition to dye decolourization, hence will result in low COD loads on the aerobic treatment unit which will ultimately reduce the hydraulic retention time in the aerobic reactor. However, in-depth investigation is necessary in lab and pilot-scale reactors to evaluate the compatibility of the method with particular industrial effluent and this work is being done under this project.

Yeast extract was used as the carbon source or primary substrate in the current research. In addition to providing energy and carbon required for microbial growth, primary substrate behaves as an electron donor and supplies electrons required for the reductive cleavage of the N = N bond in azo dyes resulting decolourization (Solís et al. 2012).

Generally, dyes and small quantities of other organic matter present in textile effluents are not sufficient for the growth of anaerobic bacteria and therefore effective decolourization cannot be obtained (Saratale et al. 2011). In this work too, a significant colour reduction in textile effluents (from both effluents, X and Y) was not observed when the decolourization experiments were conducted without yeast extract. Therefore, yeast extract was added during effluent decolourization experiments.

However, the requirement of external substrate depends on the composition of the effluent (if the particular effluent contains sufficient amounts of organic compounds such as starch then the requirement of external substrate would be low).

CONCLUSIONS

Out of the isolated strains, five bacterial strains indicated dye decolourization potential. However, bacterial consortium can be considered as more effective when decolourizing mixture of dyes or industrial effluents. Out of the individual strains, Proteus mirabilis indicated the best decolourization. Positive outcomes achieved in this study for decolourization of textile effluents by the bacterial consortium can effectively be utilized for implementing biological decolourization of industrial wastewater.

ACKNOWLEDGEMENTS

Authors gratefully acknowledge the financial support provided by the Senate Research Committee [grant number SRC/CAP/15/03]; University of Moratuwa, Sri Lanka. Authors would also like to thank Mrs I. K. Athukorala and Mr B. Karunathilaka for their assistance in laboratory work.

CONFLICT OF INTEREST

The authors have declared no conflict of interest.

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