Abstract
The biodegradation and biosorption efficiency of an indigenous siderophores-producing bacterial community on azo dyes with immobilization in chitosan beads was evaluated in this study. 13 bacterial strains were isolated from textile wastewater streams. The bacterial strains were tested for the production of siderophores as well as their ability to decolorize toxic azo dyes in aqueous solution. Both qualitatively and quantitatively, all of the strains displayed high siderophores productivity. Furthermore, they displayed remarkable decolorization efficiency for azo dyes (Acid Black 1 and Reactive Black 5) in both free and immobilized form. The immobilization process was found not only to enhance the decolorization but also the degradation of azo dyes by the bacterial isolates. In a SEM micrograph, bacterial strains were immobilized, and the pores in chitosan bead to be trapped and adsorbed for dyes from synthetic wastewater. The extent of dye compounds degradation were examined using UV–visible and FTIR spectrophotometers on treated water samples and dye absorbed beads. After 72 h of incubation, the UV–visible analysis revealed that the bacterial community could significantly reduce both azo dyes in wastewater by 90% at 300 mgL−1 dyes initial concentration. FTIR study confirmed the bonds of these dyes were broken to form less toxic chemicals via the bacterial community immobilized in chitosan beads. The immobilized bacterial community thus demonstrated effective approach of azo dye biosorption and biodegradation.
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Introduction
Myanmar’s traditional textile industry is based mainly in the Mandalay region, which is a vital asset to the growth of the national economy. LeikSanKon village (sampling site) on the bank of DoukHtaWaddy River possesses many small scale textile mills. Despite their role in booming the economic development, these textile plants are lack of proper waste management system. As a result, their textile wastewater is discharged directly into nearby rivers or dumped into the soil.
According to the report by Carmen and Daniela (2012), during the dyeing process, up to 25% of textile dyes are lost and with up to 20% directly discharged into the environmental (soil and water) as components of aqueous effluents. In particular, the release to the aqueous environment of color-containing effluents is undesirable since many of the dyes including their derivatives are poisonous, carcinogenic or mutagenic to life forms (Suteu et al. 2009; Zaharia et al. 2009). Azo dyes and their degradation products are recalcitrant to complete biodegradation because of the complex structure and xenobiotic nature. These dyes are the most problematic pollutants of textile wastewaters (Lucas and Peres 2007). Efficient removal of azo dyes from waste effluents before environmental discharge was shown to be a major challenge (Khan and Malik 2016). Among the most widely used reactive type dyes, the Acid Black 1 (C.I. 20470) and the Reactive Black 5 (C.I. 20505) are important components of azo dye used in the textile industry. An indicator for chromatography and electrophoresis studies is one of the applications for Acid Black 1 (Green 1990).
A variety of physicochemical methods (such as adsorption, coagulation, membrane filtration, ozonation, electrochemical and radiolysis etc.) have traditionally been used for treating textile wastewater. Although some of these conventional processes are successful, they are hurdled by high costs, excessive consumption of chemicals and the subsequent waste generation (Saratale et al. 2011). Recently, advances in microbial and biotechnological research such as nano-bioremediation may present solutions to address these challenges, allowing for sustainable azo dye remediation (Marimuthu et al. 2020; Sharma et al. 2020). Biotechnology can therefore provide an opportunity for textile industry to minimize costs, protect the environment, resolve human health and safety and enhance wastewater treatment efficiency and functionality (Chen et al. 2007). Techniques such as immobilization of biodegradable, non-toxic microbes can be integrated into novel soil/water bioremediation methods for removal of various environmental pollutants.
Several investigators have tried to introduce microbial approaches into textile wastewater treatment (Georgiou and Aivasidis 2006). In this context, siderophores gained much attention in recent years given their possible applications in different areas of environmental science. Siderophores can bind a number of metals with a wide range of chemical structures and specific properties (Ahmed and Holmström 2014). Microbes capable of siderophores production and resistance to wastewater leachate have been identified (Michalska et al. 2020). Despite this, studies on the use of siderophores producing bacteria are relatively scarce. Past research has reported the metal sequestering property via siderophores-specific production by immobilized pure cultures, which was shown to perform better than non-immobilized pure cultures (Dao et al. 1999; Braud et al. 2006; Sharma and Johri 2003). Studies on siderophores-producing bacterial strains for dye decolorization are also scarce, although it is seen that immobilized siderophores-producing microbes can reduce reaction time significantly enhance decolorization efficiency, and provide effective dye removal at an industrial scale for the textile industry. Karnwal 2019 and Minussi et al. 2001 discussed the potential role of siderophores in the biodecolorization and detoxification of azo and synthetic dyes. Currently, immobilized microbial systems have several advantages over free systems. The area of application for microbial cell immobilization ranges from industrial to environmental processes. Microorganisms retained on a carrier can be used in continuous and semi-continuous treatment processes, resulting in significant cost savings due to biocatalyst regeneration, reduce environmental pollution by biodegrading many harmful compounds, while avoiding the biomass and liquid separation requirement given the immobilization (Park and Chang 2000; Mrudula and Shyam 2012; Martins et al. 2013). Chitosan meets the following requirements for wastewater treatment: insoluble, non-toxic, non-polluting, cheap, and containing potentially reactive amino functional groups that can increase the carrier's affinity with microorganisms (Martins et al. 2013).
This study aimed at the physiochemical and bacteriological evaluation of the effluents from traditional textile mills to investigate the bioremediation capacity of an indigenous siderophores-producing bacterial community in both free and immobilized form. These siderophores-producing bacterial strains were immobilized in chitosan beads as chitosan is inert, inexpensive, biocompatible, and nontoxic in nature. The experiments were carried out to decolorize two prominent azo dyes (Acid Black 1 and Reactive Black 5) at a laboratory scale.
Materials and methods
Dyes
All chemicals used were at analytical grade. Acid Black 1 (B1), cas no-1064-48-8 and Reactive Black 5 (B5), cas no-17095-24-8 were purchased from Heowns, China. A spectrophotometer ranging from 190 to 800 nm (double beam UV–Vis spectrophotometer, PHILES, Nanjing, China) was used to measure the concentration of dye in the samples, via absorption intensity at the maximum wavelength (λmax) of the dye.
Sample collections and physiochemical analysis
The textile wastewater and sludge samples from textile drainage canal around the dyeing mills were collected from local village viz. LeikSanKhon, Mandalay, Myanmar (Fig. 1). The physiological analysis was done to find the conductivity, pH, dissolved oxygen, and temperature of the samples. Samples were stored in sterile plastic vials, and refrigerated at 4 °C within 24 h of sampling for downstream analyses.
Isolation and identification of siderophores-producing bacteria
For the enrichment, isolation and screening of siderophores-producing bacteria, the following steps were taken: (i) wastewater sample was serially diluted with sterilized 0.9% NaCl (ii) 1 ml of the sample was transferred into 9 ml LB medium (iii) the culture was inoculated and incubated at 37 °C for 24–48 h and streaked on Chrome Azurol S (CAS) plates (Milagres et al. 1999) (iv) bacterial colonies which presented a clear zone around them on CAS medium were selected and further cultivated. Thirteen such bacterial strains with siderophores productivity were chosen for further research. Siderophores activity was calculated by mixing 0.5 ml of Chrome Azurol S (CAS) with 0.5 ml of the sample. Chrome Azurol S solution was prepared according to Schwyn and Neilands (1987). The same buffer used for the sample extraction was used to prepare a reference sample. At zero time and after 2 h of reaction at room temperature in the dark, the absorbance was measured at 630 nm. Positive reactions were estimated qualitatively by the decolorization in color (blue to colorless). The percentage of siderophores-type iron binding compounds was determined according to the equation:
where Ar = reference absorbance and As = sample absorbance.
The test was assumed negative when no blue color changes were detected.
In order to determine the tolerance of the isolates to dyes used in this research, 13 isolates were streaked on the plates with LB medium containing 50, 100, 200 mgL−1 of dyes (B1 and B5). Colonies of bacteria that exhibited the growth in the presence of dyes in the agar medium were picked and cultured. They were then preserved in 50% glycerol for further studies.
Furthermore, total genomic DNA was extracted from pure isolates to identify the bacterial strains using TIANamp Bacteria DNA Kit (DP302) (TIANGEN Biotech (Beijing) Co., Ltd.). The DNA was amplified using universal 16S rRNA primers 27F:5′-AGAGTTTGGATCMTGGCTCAG-3′ and 1492R:5′-CGGTTACCTTGTTA CGACTT-3′. The PCR predicted amplicon was approximately 1.5 kb. PCR reactions were performed in a 50 μl mixture containing 0.4 μM of each primer and 2 × Taq PCR master mix (Cat. #: R001AM), 1 μl of DNA template, adjusted to the final volume with sterilized double distilled water. PCR thermocycler (LifeEco) was used comprising 94 °C for 3 min following with 30 cycles at 94 °C for 30 secs, 55 °C as annealing temperature for 30 secs with an extension of 72 °C for 1 min followed by final extension temperature at 72 °C for 5 min. For further purification and downstream application, amplified PCR products were stored at − 20 °C. A 1.2% agarose gel electrophoresis loaded 5 μl of the PCR amplified product stained with Gold-View I Nuclear Staining Dyes (10000×) using Gene Ruler TMDSTM 15,000 DNA ladder (Cat. #: LM1161), and visualized under UV Transilluminator (CliNX). Products were analyzed and sequenced by ABI 3730 XL DNA Analyzer (Applied Biosystems, USA). Sequences have been aligned, verified and edited using Bioedit 7.2.0 (Hall 1999) software programs. NCBI BLAST determined the homology of the sequences.
Immobilization of isolated siderophores producing bacterial isolates
At room temperature, chitosan (4%) was dissolved in 1% (v:v) acetic acid with continuous stirring at 100 rpm for 25 min until it was clear., The resulting solution was then adjusted to pH 5 by adding NaOH or HCL (Ghadi et al. 2014). For the coating process, 10 ml of overnight culture broth was added to 10 ml of prepared chitosan solution. The biomass-chitosan mixture was applied drop-wise into a solution of 0.1 M NaOH using a 50 ml syringe, with constant stirring at 37 °C for 10 min, then washed several times with sterile distilled water until it reached pH 7. With sterile media, all measures were aseptically performed (Fierro et al. 2008).
Dye decolorization assay
Dye decolorization assay by free siderophores-producing bacterial isolates
Ten percent overnight cultured isolates were incubated for 72 h in 10 ml LB medium supplemented with 200 mgL−1 B5 and B1 dye. 2 ml of each experimental sample was then extracted in aseptic condition at a defined interval time (0, 1, 2, 4, 8, 12, 24, 48 and 72) hrs, and centrifuged for 10 min at 7500 rpm (Eppendorf 5810R). The supernatant was assayed spectrophotometrically by measuring the decrease in absorbance at the respective dyes λ-max (B1-617 nm and B5 599 nm). The control flasks as without bacterial cultures were tested under the same conditions. All these decolorization experiments were carried out in triplicate, and decolorization activity was expressed using the formula with regard to percent dye decolorization (Chen et al. 2003). The decoloration percent was spectrophotometrically determined by calculating the initial absorbance (before decoloration) and final absorbance (after decolorization).
Dye decolorization assay by immobilized siderophores-producing bacterial isolates
Both chitosan beads only and combined immobilized cells bead were introduced to 500 ml of synthetic dye wastewater medium in flasks containing dyes (50,100, 200, 300 mgL−1). Cultures were incubated at 28 °C and 175 rpm. Each flask was filled with 200 ml synthetic dye wastewater medium (Thomas et al. 2018). All flasks were incubated at 28 °C in an oscillatory shaker for 72 h, and the solution was analyzed. This decolorization activity was analyzed as described above.
Viability of isolates after decolorization
The immobilized chitosan beads were checked for the viability of isolates using LB medium plates (Fierro et al. 2008).
Conformational analysis of dye decolorization
Electron microscopy analysis
Scanning electron microscope (SEM) using Stereoscan (model S360 brand SEM – Leica Cambridge, Cambridge, UK) was used to examine the structure of chitosan beads before and after dye absorption. The freeze-dried beads were cut by cross-section. SEM was used to test their outer and inner structure. The scanning electron microscope was run with a magnification of ~ 250 and an increased voltage of 25 kV for the magnification to obtain high-resolution micrographs.
FTIR analysis for dye decolorization products
An additional dye biodegradation test was carried out to compare the activity of the immobilized consortium and chitosan beads. The dye absorbed chitosan beads were freeze dried and analyzed by FTIR (Bruker, TGA-IR, TENSOR 27). The spectra were collected within 450–4000 cm−1 of scanning range. The FTIR was first calibrated for background signal scanning and then screened for the experimental samples with control sample of pure potassium bromide (KBr). The results of the analysis were compared to the control dyes (B1 and B5).
Statistical analysis
All the quantitative findings are described as means ± standard deviations of triplicate analyses. Analysis of variance (ANOVA) was carried out, and possible statistical variations between experiments and control were evaluated with the Tukey’s test at a significance level of P < 0.05 using Minitab 17.1.0 (Minitab Pty, Sydney, Australia).
Results and discussion
Physiochemical conditions of textile wastewater samples
The temperature of the collected effluent was about 22.8 °C. The pH of the effluent was found to be alkaline, i.e., 9.46. Electric conductivity (EC) and Total dissolved solid (TDS) of the effluent were 6.75 msm−1 and 3660 mgL−1, respectively. Overall, it was observed that the Chemical oxygen demand (COD) of the effluent is about 1500 mgL−1. These results are in concordance with previous studies that have reported the physiochemical conditions of dye effluents to be high in color, pH, suspended solids, COD and Biochemical oxygen demand (BOD) (Yaseen and Scholz 2016; Sharma et al. 2007; Sekomo et al. 2012).
Isolation and identification of siderophores producing bacteria
A total of 13 different colonies were isolated on CAS media. Figure 2 illustrates the siderophores producing activity of these 13 isolates. Figure 2A shows the yellow color changes around such colonies and suggested the siderophores producing activity. Figure 2B showed the blue dye (CAS) decolorization activity of isolates at 600 nm. Figure 3 illustrates the siderophores production units produced by the 13 isolates at OD 1 (600 nm) showed high productivity with no statistical differences. Therefore, all the isolates have similar activity in siderophores production. Some environmental issues, such as heavy metal accumulation, rust reduction, bio fouling, dye degradation, waste treatment and bioleaching, can be addressed by siderophores (Sah and Singh 2015). Siderophores are considered to be effective agents in pulp treatment; with application toward bleached Kraft pulp (Bajpai 2004). Siderophores activity was linked with dye decolorization and degradation in our study.
Morphology of the isolates was analyzed under a light microscope. Based on this analysis and the 16 s rRNA gene sequencing results, the identity of the isolates are listed in Table 1. The 16S rRNA matches were three different Pseudomonas sp., three different Bacillus sp., two different Acinetobacter sp., Phaseolibacter sp., Comamonas sp., Stenotrophomonas sp., and Enterobacter sp.
Immobilization of isolated siderophores producing bacterial isolates
At room temperature, chitosan (4%) was dissolved in 1% (v:v) acetic acid with continuous stirring at 100 rpm for 25 min until it was clear. The resulting solution was then adjusted to pH 5 by adding NaOH or HCL (Ghadi et al.2014). For the coating process, 10 ml of overnight culture broth of each isolate was added to 10 ml of prepared chitosan solution (1:1), washed three times with distilled water and stored in 0.1 M phosphate buffer at 4 °C. The beads were able to maintain the stability. The number of beads obtained from 10 ml of 4% chitosan and 10 ml of suspension ranged from 170 to 250. These beads were of diameter 4 to 6 mm (Fig. 4). Our results are in concordance with previous studies where 1:1 ratio for immobilized chitosan and microbial culture gives stable beads (Le‐Tien et al. 2004; Verma et al. 2019).
Dye decolorization assay
Dye decolorization assay by free siderophores producing bacterial isolates
The ability of all free 13 isolates to decolorize the two azo textile dyes (B1 and B5) was investigated individually in order to assess their decolorization potential. In single culture experiment, all these 13 isolates have shown significant decolorization (90% at 200 mgL−1 dye concentration) for both dyes individually after 72 h of incubation. Decolorization process started to increase after 8 h of incubation as seen in Fig. 5A and B. The miximum absorbtion rate was found at 24 h of incubation. These results are in agreement with past work demonstrating the ability of siderophores from various fungal and bacterial strains as an alternative tool to treat industrial effluents (Goodell et al. 1997; DuraÂn et al. 1999). The efficient decolorization of sideraphores producing bacterial strains could be related to the fact that siderophores have high-affinity constants for various metals and many chemical complexes and possesses the decolorization capability by sequestering such complexes present in the dyes (Minussi et al. 2001).
Dye decolorization assay by immobilised siderophores producing bacterial isolates
Decolorization activity of 13 immobilized isolates analyzed by UV spectrophotometer and data were statistically analyzed by one way ANOVA. Synthetic wastewaters with varying dye concentrations were tested to compare their bio-sorption capacity. The results of dye decolorization and azo dye degrading activity are reported in Fig. 6A and B. Figure 7A and B showed the decolorization of synthetic textile effluents efficiency contaminated with B5 and B1 at different dye concentrations. Immobilization has been reported to be an effective way to improve decolorization capability in many previous studies (Oghenerobor et al. 2018; Khan and Banerjee 2010; Tony et al. 2009; Wang et al. 2009). Although non-immobilized dyes-degrading bacteria are potent enough to decolorize dyes, immobilization of pure cultures is more appropriate under real industrial applications (Zhou et al. 2019; Vikrant et al. 2018). More specifically, immobilized bacteria are more resistant to changing environmental stresses like toxic compounds, pH, temperature etc. Under such conditions, immobilization allows for stronger adsorption and biodegradation (Kurade et al. 2019; Wu et al. 2001). Thus our results are in concordance with the previous literature.
Viability of isolates after decolorization
Figure 8 showed the viability of 13 isolates at each stage of the experiments. It was observed that the immobilized bacterial isolates within the chitosan beads were viable in the post decolorization phase. This indicates that siderophores-producing bacterial strains in immobilized form are resistant to harsh growth conditions and thus are suitable for textile wastewater treatment. The authors have also been established by authors in previous studies (Ahmed et al. 2014; Rajkumar et al. 2010).
Conformational analysis of dye decolorization
Electron microscopy analysis
The polymerization and morphology of chitosan beads were studied using SEM. Figures 9 and 10 clearly show the layer of chitosan and the surface of the bead for the immobilization of bacterial strains. It was seen that the bacterial cells adhere firmly to the chitosan layers. It has increased cell density while not blocking the micropores of the beads. It has been reported in the previous literature that amino groups present on chitosan allow for covalent binding of material to be immobilized (Eberhardt et al. 2004; Cetinus et al. 2000). Apart from this, some authors have also given evidence of entrapment as a mode of immobilization in chitosan (Shentu et al. 2005; Zang et al. 2012). Conformational changes were not observed after dyes absorption, both in bacterial immobilized and empty chitosan beads in our study. Therefore, it could be postulated that the use of chitosan as immobilizing agent is as appropriate approach for the micropores of the beads to act as active sites for the dye adsorption.
Analysis for dye decolorization products
The FT-IR spectrum of both the dyes is shown in Fig. 11A and B with the position of peaks and corresponding functional units are explained.
The absorption spectrum of the synthetic dye B1 indicates a change in the O–H stretching after-treatment with bacterial community immobilized in chitosan beads. Along with this, an appearance of a peak at 2366 cm−1 after treatment indicates the formation of O= C=O stretching, while no such change was seen in dye treated with only chitosan beads. Similarly, the peak corresponding N=C=O stretching and CH2 bending was found to disappear in the dyes treated with immobilized chitosan beads. Also, the peak corresponding H–C–H stretching was found to disappear in the dyes treated with immobilized chitosan beads. Furthermore, the appearance of a bond at 2127 cm−1 in dye treated with immobilized chitosan beads indicates the formation of N=C=S, which is representative of the thiocyanate group. Similarly, appearance of S=O stretching on the treatment of dye with immobilized chitosan beads indicated the formation of sulfoxide during the decolorization process. Furthermore, the disappearance of peaks corresponding to C–C=C stretching, C=C stretching, and C–N stretching in the dye treated with immobilized chitosan beads is indicative of the effectiveness of the bacterial strains in converting the azo dyes to less toxic forms as N=N stretching disappeared after absorption. On the other hand, the effectiveness of the process also showed a shift in the spectrum at peaks corresponding to C–O–C stretching and C–H aromatic stretching by dye treated with immobilized chitosan beads.
The IR spectrum of the dye B5 post-treatment with only chitosan beads and bacteria immobilized chitosan beads was almost similar to that of the post-treatment IR spectrum of B1 dye. A minor variation was observed for the appearance of H–C–H stretching when dye was treated with bacteria immobilized chitosan beads. This is indicative that hydrocarbons were produced during the decolorization process of the dye B5. N=N stretching also disappeared for B5 after chitosan immobilized bacterial community absorption.
The IR spectrum for both the dyes has not reported the characteristic peak at 1620.21 cm−1 post-treatment with bacterial immobilized chitosan beads, which is representative of the absence of azo bond post treatment (Shah et al. 2012; Khan et al. 2014). The appearance of thiocaynate stretching is also a noteworthy aspect of the FTIR spectrum of both dyes post-treatment with bacterial immobilized chitosan beads. This is not the same as previous studies that reported thiocynate as an effective reducing agent for decolorization of various dyes like methylene blue. Other than this, a fission of aromatic rings peaks could be observed in the form of decreasing peak intensities within the low-frequency region (the region characteristic of the aromatic nature of azo dyes) of post-treatment spectra (Pérez-Calderón et al. 2018).
The corresponding UV visible spectra of both the dyes before and after treatment by bacterial immobilized chitosan beads also depicted a trend that validates the IR spectrum. It can be seen in Fig. 12A and B that the absorbance maxima of both dyes tends to decrease after the treatment. This demonstrates the decolorization of the dyes (B1 and B5). Our results are concordant to the previous literature where a decrease in the absorbance maxima of the dye post-treatment has been related to its decolorization or degradation (Roy et al. 2018; Mahmoud et al. 2017; Asad et al. 2007). Therefore, it is evident from the FTIR and the UV spectrum that the isolated siderophores producing bacterial strains are effective enough to convert dyes to less toxic forms.
Conclusion
This work investigated the decolorization of two Azo dyes, Acid Black 1 and Reactive Black 5, by siderophores-producing bacterial strains isolated from the textile effluent. 13 bacterial isolates were employed for this decolorization study. The decolorization assay comprised of estimation of the decolorization capability of the 13 isolates in the form of (i) pure culture and (ii) immobilized in chitosan beads. It was observed that in pure culture, all the 13 isolates have shown significant decolorization (90% at 300 mgL−1 dye concentrations) for both dyes after 72 h of incubation. Such a higher rate of decolorization was linked to the complex sequestering ability of siderophores. The immobilization process was found to enhance the decolorization process by providing a means of simultaneous absorption and decolorization of dyes by the bacterial strains. Besides this, the FTIR study confirmed the conversion of these dyes into less toxic forms by bacterial immobilized chitosan bead. Thus, it could be concluded that siderophores producing bacterial strains are an excellent alternative for decolorization of toxic recalcitrant dyes, and their immobilization would aid in the scale up of this process into the industrial level.
Data availability
All data and materials are included in this article.
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Authors are thankful to the financial support by the Research Start-Up Funds from Hainan University in China (KYQD_ZR2017212).
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TTW: conceptualization, experimental investigations, data interpretation, and writing of the original draft. PCF: supervision, data interpretation, reviewing, and editing of the original draft. TMS, HHE, NNW, KKS, WND, TKK: perform sampling, carry out experiments and experimental investigations. All authors read and approved the final version.
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We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work; there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the position presented in this paper.
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Win, T.T., Swe, T.M., Ei, H.H. et al. An evaluation into the biosorption and biodegradation of azo dyes by indigenous siderophores-producing bacteria immobilized in chitosan. Biodegradation 32, 697–710 (2021). https://doi.org/10.1007/s10532-021-09961-y
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DOI: https://doi.org/10.1007/s10532-021-09961-y