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Bioresource Technology 91 (2004) 69–75 Decolorization of reactive azo dyes by Cunninghamella elegans UCP 542
Bioresource Technology 91 (2004) 69–75 Decolorization of reactive azo dyes by Cunninghamella elegans UCP 542

Bioresource Technology 91 (2004) 69–75

Bioresource Technology 91 (2004) 69–75 Decolorization of reactive azo dyes by Cunninghamella elegans UCP 542 under

Decolorization of reactive azo dyes by Cunninghamella elegans UCP 542 under co-metabolic conditions

S.T. Ambroosio

a , G.M. Campos-Takaki a,b, *

a Doutorado em Ciee^ncias Bioloo gicas, Universidade Federal de Pernambuco, 50670-420 Recife-Pernambuco, Brazil b Departamento de Qu ıımica e Nuu cleo de Pesquisas em Ciee^ncias Ambientais, Universidade Catoo lica de Pernambuco, 50050-590 Recife-Pernambuco, Brazil

Received 9 September 2002; received in revised form 15 May 2003; accepted 16 May 2003

Abstract

The inappropriate disposal of dyes in wastewater constitutes an environmental problem and can cause damage to the ecosystem. Alternative treatments have been reported that fungi are particularly effective in the decolorization of textile effluents. The decol- orization of dyes with different molecular structures by Cunninghamella elegans was evaluated under several media conditions. The decolorization procedures consisted of adding 72 h of mycelium into the culture medium containing either orange or reactive black or reactive red or a mixture of these dyes in the presence or absence of sucrose and/or peptone. The decolorization profile was highly dependent upon the incubation time, the molecular structure of the dye and presence or absence of co-substrates. The presence of sucrose or both sucrose and peptone significantly increased the decolorization of the solutions, however, the presence of only the nitrogen source suppressed it. The ultraviolet spectra of the solutions before and after decolorization suggested the occurrence of biodegradation in addition to the biosorption of the dyes. All tested dyes, except for the reactive black, caused inhibition of res- piration of Escherichia coli, which suggested that toxic metabolites were produced. 2003 Elsevier Ltd. All rights reserved.

Keywords: Zygomycetes; Biodegradation; Biosorption; Textile dyes; Toxicity

1. Introduction

The reactive azo dyes are characterized by the pres- ence of a nitrogen–nitrogen double bond (–N@N–), namely the azo group, which is bound to aromatic groups. Usually during the textile processing, around 30–70% of the amount of the dye used is hydrolyzed and eliminated into the wastewater (Bumpus, 1995). In order to meet the criteria necessary for industrial applications, these dyes present a diversity of colors, molecular structures and resistance to fading upon ex- posure to light, water and many chemical compounds (Correia et al., 1994). These required criteria thus yield compounds that cause serious environmental pollution problems. As a result of the environmental legislation, industries are being forced to treat dye contaminated their effluents (Robinson et al., 2001). Due to their ge- netic diversity and metabolic versatility, microorganisms

* Corresponding

32714043.

author.

Tel.:

+55-81-32164017;

fax:

+55-81-

E-mail address: takaki@unicap.br (G.M. Campos-Takaki).

0960-8524/$ - see front matter 2003 Elsevier Ltd. All rights reserved.

doi:10.1016/S0960-8524(03)00153-6

have become a viable alternative to remediate the pollu- tion problem caused by reactive azo dyes (Alexander, 1994). Currently, bioremediation is becoming important because it is cost effective, environmentally friendly, and pro- duces less sludge (Banat et al., 1996; Robinson et al., 2001). Many bacteria are able to degrade azo reactive dyes aerobically and anaerobically (Tan et al., 1999); how- ever, in many cases the metabolic products, usually aro- matic amines (Hu, 2001), are toxic or even more toxic than the starting azo dyes. Phanerochaete chrysosporium has been reported to efficiently degrade azo reactive dyes such as Orange II, Congo red e Tropaeolim (Cripps et al., 1990). In addition, it has recently been demon- strated that peroxidases (LiP and MnP), phenoloxidases (laccases), and dioxygenases can act on specific recalci- trant pollutants by precipitation or transforming them into other products, thus allowing for a possible better final treatment (Dur aan and Esposito, 2000). It has been shown that some species of Basidiomy- cetes such as Phlebia tremellosa (Kirby et al., 2000), Irpex lacteus, Pleurotus ostreaus (Novotn yy et al., 2001) and Trametes modesta (Nyanhongo et al., 2002), can

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S.T. Ambr oosio, G.M. Campos-Takaki / Bioresource Technology 91 (2004) 69–75

play an important role in the azo dyes decolorization, despite the fact that the detailed biochemical pathways underlying the fungal degradation are not yet well un- derstood (Banat et al., 1996; Slockar and Le Marechal, 1998; Zheng et al., 1999). In addition, it has also been demonstrated that fungi can utilize dye chemical sub- stances such as aniline, as the sole source of carbon and nitrogen (Emtiazi et al., 2001). Consequently, the effi- ciency of the decolorization process can be improved by the addition of suitable co-substrates in the culture medium (Sumathi and Manju, 2000; Panswad and Luangdilok, 2000), significantly reducing the costs of the process (Kapdan et al., 2000). Studies on nonligninolytic fungi metabolizing dyes are minimal, and only recently, has there been a report that Cunninghamella elegans ATCC 36112 was able to metabolize 85% of the triphenylmethane dye malachite green after 24 h of incubation. The mechanism of this degradation process by C. elegans is yet to be elucidated; however, this fungus is capable of metabolizing a wide range of compounds, particularly by demethylation and oxidation (Cha et al., 2001). The main objective of the present study was to examine the decolorization of three reactive azo dyes and their mixture by mycelium of C. elegans in presence or absence of carbon and/or nitrogen sources, as well as the determination of the toxicity of dyes after the action of the fungus by reduction of Escherichia coli respiration.

2. Methods

2.1. Microorganism and dyes

C. elegans UCP 542 was isolated from mangrove sediment collected in the City of Rio Formoso, Per-

nambuco State, Brazil by Gomes et al. (2000). The iso- lation and identification of strain are according to O Donnell (1979). The culture was maintained on Sab- ouraud dextrose agar at 4 C and deposited in Culture Collection of Nucleus of Resource in Environmental Sciences, Catholic University of Pernambuco, Recife, PE, Brazil. Selected features of the azo dyes studied are presented in Table 1. The azo dyes C.I. reactive black-5 and C.I. reactive red-198 were provided by the Suape T^eextil Co., located in the City of Cabo, Pernambuco, Brazil, and the orange II (C.I.15510) was obtained from Sigma (Sigma-Aldrich Corporation, St. Louis, Missouri, USA). Solutions of these dyes were prepared by dissolving a given amount of the powder in distilled water and then added to the medium in order to yield solutions with final concentrations of 0.025 mM for the pure dyes and 0.034 mM for the mixture of dyes.

2.2. Culture conditions

The fungal cultures were grown in 250 ml Erlenmeyer flasks using spore suspensions (3.8 · 10 8 spores/ml) into 95 ml of Sabouraud broth medium sterilized at 121 C for 15 min (Hansen et al., 1995). For the decolorization experiments, 72 h old fungal mycelium was inoculated in modified Sabouraud broth media (Lacaz et al., 1991) in Table 2. Sucrose was used rather than glucose, as a more economical substitute (Kapdan et al., 2000). The pH of the medium was adjusted to 5.8 before sterilization and the culture was incubated in an orbital shaker at 150 rpm and 28 C. Aliquots were removed after 12, 24, 48, 72, 96, 120 and 168 h. Controls of the experiments were designed to perform under the same conditions de- scribed earlier without the fungi. All experiments were

Table 1 Structure of azo dyes and their respective wavelength maximum absorption ( k max )

Dyes

k max (nm)

Chemical structure

 

Orange II

485

NaO 3 S

OH N N
OH
N
N
 

Reactive black 5

597

 

NaO

3

SOCH

2

CH

2

O S

2

N N
N
N

NaO S

3

OH NH 2 N N SO 3 Na
OH
NH 2
N
N
SO 3 Na

SO CH

2

2

CH OSO Na

2

3

Reactive red 198

517

H 3 C NH SO 3 Na N OH NH N N N N Cl
H 3 C
NH
SO 3
Na
N
OH
NH
N
N
N
N
Cl
SO 3 Na
Na O 3 S

S.T. Ambr oosio, G.M. Campos-Takaki / Bioresource Technology 91 (2004) 69–75

71

Table 2 Composition of media used in the dye decolorization experiments

Components a

Medium

I

II

III

IV

Peptone (10 g/l) Sucrose (20 g/l) KH 2 PO 4 (0.5 g/l) Dye

X

X

X

X

XXXX

X

X

X

X

a X denotes the presence of the component.

performed in triplicate and each treatment had four replicates.

2.3. Color reduction measurements

Absorbance measurements were performed with a UV–VIS spectrophotometer (Spectronic Genesis, model 2-Spectronic Instruments Inc., USA). The wavelengths for the measurements were set at the values presented in Table 1 as k max for the pure dyes, and at 511 nm for the mixture. Dye concentration was calculated from an absorbance x concentration calibration curve. All cali- bration curves yielded a linear range 0.005–0.025 mM/l and a linear regression coefficient at least 0.99.

2.4. Assessment of acute toxicity

The toxicity tests were performed at the Biological Chemistry Laboratory of University of Campinas (S~aao Paulo, Brazil). The indicator organism, E. coli ATCC 25922, was provided by Culture Collections of Tropical Fundation Andr ee Tosello (University of Campinas, S~aao Paulo, Brazil). The bioassay was based on the inhibition of respiration of the bacteria by pollutant and was carried out on a clear supernatant after fungal treatment in comparison to the toxicity of controls. The assay in- volves the incubation of E. coli cultures at 37 C with known amounts of the pollutant (solution-dyes). When the CO 2 concentration produced by microbial respira- tion reached 0.5 mmol/l, 45 ml of the cultures of the E. coli was transferred into several flasks and each one received 5 ml of one sample withdrawn at a selected time. As a control, 5 ml of distilled water was introduced in one the flasks and the CO 2 production monitored every 20 min using flow injection analysis (FIA). The test is described in detail in Moraes et al. (2000).

2.5. Statistical analysis

To evaluate the influence of the media components upon the decolorization of dye solutions the ANOVA, analysis of variance of the data, was performed, which involved the pre-treatment of the data by the arcsine function, namely, arcsine (x=100), with x being the original data. The main factors analyzed were the dye

structure, culture media, incubation period, and the in- teraction among them. The means of the significantly different main effects were compared by the Duncan s test at the 5% level using the Statistica program (Statsoft Inc., 1997).

3. Results and discussion

The azo reactive dyes black-5, red-198, orange II were chosen for this study since they are widely used

in the cotton textile industry in Brazil and throughout

the world. Four different media have been used in order to establish the most suitable conditions for decolorization of solutions containing dyes and their mixture by the mycelium of C. elegans. This fungus was capable of decolorizing all dyes and the respective combinations in all media were studied. The ANOVA analysis of the data indicated that the decolorizations were statistically significant (P < 0:05) for all media and dyes (Fig. 1). For simplicity, representative values presented data pooled, and the distinction between the averages was indicated by combination of different letters. These results showed that for this particular fungus the decolorization of the dyes solutions could be selec- tively supported by the media composition. For in- stance, the medias I and III were more appropriate for decolorization of the orange II dye, whereas medium II and IV were more suitable for decolorization of reactive red and mixture of dyes. In addition, the mixture de- colorization was strongly dependent upon the medium respectively used in the procedure. The decolorization produced by the fungus was highly selective despite the

fact that all dyes process the same azo-stilbene moiety.

A relationship between the selectivity induced by the

medium and the molecular structure of the dyes might be established if it is consider that medias I and III contain carbon sources leading to a significant (P < 0:05) increase of the biomass (50% and 70%, respec- tively). Consequently the metabolism and the biosorp- tion of the orange II dye should be preferred, since it is the poorest on carbon source, as well as the smallest molecule, its small steric hindrance should allow for a better biosorption. It should however be noted that the relationship between the molecular structure of the dyes and their decolorization by fungal treatment is still not clearly established (Knapp et al., 1995). Quantitatively, it was observed that in the presence of sucrose and peptone (medium I), the decolorization of orange II was nearly 83% after 96 h, whereas the de- colorization of the other dyes not as significant (Fig. 1A). Conversely, in the presence of peptone as the sole source of organic nitrogen (medium II) the decoloriza- tion was not satisfactory, since the most significant de- colorization (48% after 72 h) was achieved for the

72

S.T. Ambr oosio, G.M. Campos-Takaki / Bioresource Technology 91 (2004) 69–75

Medium II 0.65 1.0 a Medium I a 0.60 0.9 0.55 a a a 0.8
Medium II
0.65
1.0
a
Medium I
a
0.60
0.9
0.55
a
a
a
0.8
0.50
0.45
0.7
b
b
0.40
a
b
b
0.6
b
b
a
a
0.35
b
b
c
0.5
ab
0.30
c
b
a
ab
ab
b
bc
a
0.4
0.25
b
b
ab
c
b
c
bc
b
a
b
ab
0.20
d
d
c
0.3
b
ab
a
a
a
a
0.15
c
0.2
c
ab
a
0.10
b
ab
ab
0.1
b
b
b
0.05
0.0
0.00
12
24
72
96
168
12
24
48
72
96
120
168
48
120
(A)
Time (hours)
(B)
Time (hours)
Medium III
Medium IV
1.4
a
1.0
a
a
a
a
1.2
0.8
a
a
1.0
a
a
b
c
0.6
0.8
a
a
a
a
a
b
b
a
a
a
0.6
ab
b
b
b
b
b
b
b
0.4
b
b
ab
0.4
ab
b
b
b
bc
b
bc
c
b b
a
0.2
0.2
b
a
b
c
b
d
a
a
b
b
c
c
c
0.0
0.0
12
24
48
72
96
120
168
12
24
48
72
96
120
168
(C)
Time (hours)
(D)
Time (hours)
Fig. 1. Effect of medium composition I decolorization of the dyes orange II (j), reactive black ( ), reactive red (
542. The letters indicate average values which are statistically different at P ¼ 0:05, using the Duncan test.
) and mixture (
) by C. elegans
Decolorization (%)
Decolorization (%)
Decolorization (%)
Decolorization (%)

reactive red (Fig. 1B). These results showed that the presence of peptone interfered in the color removal of the azo dye, as has already been reported (Tatarko and Bumpus, 1998; Zheng et al., 1999; Fu and Viraragha- van, 2001) concerning the color removal reduction due to the presence of inorganic nitrogen, such as ammo- nium ions. Satisfactory decolorization was obtained for all dyes in the medium III, which contained only sucrose (Fig. 1C). Comparisons with medium I, which contained sucrose and peptone, exhibited distinct behaviors. The decolorization of orange II was slightly greater as well as faster for medium III (88% after 96 h of incubation), since it was significant just after 48 h of incubation. These differences can be interpreted as a negative in-

terference of peptone (medium I), as observed in me- dium II (peptone only). For comparison, a medium without sucrose and peptone (medium IV) was used and a distinct behavior for the decolorization was observed (Fig. 1D). In this medium, the decolorization of orange II (10%), reactive black (40%) and mixture of dyes (40%) was slight even after 72 h of incubation when compared with media containing sucrose. However, a significant decoloriza- tion for the reactive red dye (80%) was achieved after 120 h of incubation. These results thus showed that the medium composition was important for the decolor- ization of dyes by this fungus treatment and that selec- tive decolorization can be obtained by combining different conditions.

S.T. Ambr oosio, G.M. Campos-Takaki / Bioresource Technology 91 (2004) 69–75

73

An additional observation should also be reported regarding the physical appearance of the samples. Namely, the samples on medium containing sucrose exhibited biomass production with a strong orange color after 24–48 h of incubation; this strong color became faint after 96 h and then returned to the original ap- pearance of the mycelium prior to treatment. However, the color of the solution remained unchanged during this observation, what suggests that the dye molecules adsorbed on the biomass were not released to the solu- tion (desorption), being probably degraded during the fungal metabolism. Comparisons with results reported in the literature (Fu and Viraraghavan, 2001) corroborate most of the observations for the decolorization of the reactive azo-dye by fungal treatment. As mentioned previously, the chemical structures of the dye molecules are im- portant in decolorization (Novotn yy et al., 2001) and no clear relationships have been established between the molecular structure, the amount and the selectivity of the decolorization. For instance, Aspergillus foetidus was unable to utilize drimared red and drimared blue dyes as the sole source of energy, whereas in the presence of sucrose a color removal of 95–99% was obtained (Sumathi and Manju, 2000). The dye everzol turquoise blue was 98% decolorized by Coriolus ver- sicolor in presence of sucrose and urea (Kapdan et al.,

2000).

Despite the observations mentioned before, it has not been clearly established if the present fungal treatment involved the degradation of the dyes in addition to the visually observed biosorption. Thus, two techniques were used to provide some indications of the presence or absence of degradation, namely, toxicity tests and UV– VIS spectra. Toxicity tests showed that the solutions resulting from the fungal treatment of all tested azo dyes, except for the reactive black, inhibited the respi- ration of E. Coli when compared to the untreated so- lutions. This was an indication that the fungus was producing metabolites and thus the degradation was active (Fig. 2). It is known that several enzymes are present in the microsomal and cytosolic fractions of C. elegans (Wackett and Gibson, 1982; Zhang et al., 1996). Most of these enzymes are oxidative mechanism, par- ticularly the cytochrome P-450, which might use the dye molecules as substrate rendering them colorless after the reaction. It has already been reported that the biode- gradation of crystal violet by C. elegans did not produce metabolites as toxic as the starting dye (Cha et al., 2001), whereas the reductive azo linkage by bacteria resulted in the formation of aromatic amines, which can be highly toxic and carcinogenic (Hu, 2001). Our results have shown that the solution resulting from the fungal treatment of the medium containing the reactive black did not inhibit the respiration of E. coli. This analogy should not be taken any further since the molecular

70 60 50 40 30 20 10 0 Orange II Reactive black Reactive red Mixture
70
60
50
40
30
20
10
0
Orange II
Reactive black
Reactive red
Mixture
Toxicity (%)

Dyes

Fig. 2. Toxicity of dyes to E. coli before (j) and after ( ) treatment with C. elegans UCP 542.

structures of the crystal violet and reactive black are very different as should be their metabolites. The UV–VIS spectra results, are presented in Fig. 3. The normalized spectra of the orange II dye solutions before (control) and after the fungal treatment under all media conditions were studied. It is apparent that for medias I and II, in which the descolorization of the orange II solutions were significant, the UV–VIS spectra exhibit a shift of the maximum of absorption towards shorter wavelengths upon fungal treatment. This indi- cates that decolorization of this dye solution occurred by degradation in addition to the visual observation of the biosorption process (Wang and Yu, 1998). For the decolorization in medias II and IV, the spectral shifts in

Medium II Medium I 1.0 Medium IV Medium III 0.8 Control 0.6 0.4 0.2 0.0
Medium II
Medium I
1.0
Medium IV
Medium III
0.8
Control
0.6
0.4
0.2
0.0
300
350
400
450
500
550
600
650
700
750
Absorbance

Wavelength (nm)

Fig. 3. UV–VIS spectra of orange II azo dye before and after the treatment with C. elegans UCP 542 on different media: control ( ), medium I ( ), medium II (––), medium III ( ) and medium IV ( ).

74

S.T. Ambr oosio, G.M. Campos-Takaki / Bioresource Technology 91 (2004) 69–75

the UV–VIS region were not significant and thus the dominant mechanism for decolorization would be the biosorption of the dye molecules (Zheng et al., 1999). Regarding the spectral shifts towards shorter wave- lengths observed in the treatment with medias I and III, they were probably produced by the biodegradation of the dye molecule that led to a decrease of the conju- gation effects between the aromatic rings. It should be noted that for conjugated systems the wavelength of the maximum absorption was very sensitive to the size of the conjugation, where a decrease of one unit of double bond can lead to shifts in range of 25–30 nm in polyenic- carbonyl conjugated systems (Streitwieser et al., 1992). In Fig. 4 we presented the UV–VIS spectra of the solution containing a mixture of all dyes before and after the fungal treatment. It can be readily observed that the decolorization that had already occurred just after 24 h is mainly due to biosorption, since there were no spectral differences between the control and the so- lution after the treatment. However, the solution after 96 h became re-colorized, due to some products from desorption, but mainly due to the degradation of the adsorbed dyes, since there were significant spectral shifts in the 500 and 400 nm regions. Thus, the results of the UV–VIS spectra corroborated the toxicity tests regarding the degradation of the dyes by C. elegans in the presence of sucrose. In addition, these data showed that it was viable to use UV–VIS spectroscopy to determine the kinetics of the biosorp- tion and the degradation processes during the decolor- ization. In conclusion, the decolorization process produced by treatment with C. elegans was strongly dependent upon the co-metabolism conditions, where the sucrose enhanced and peptone had a negative effect upon the decolorization. This decolorization process was also dependent upon the molecular structure of the

Mixture 0.6 0.5 0.4 Control 0.3 Mixture after 24 h 0.2 Mixture after 96 h
Mixture
0.6
0.5
0.4
Control
0.3
Mixture after 24 h
0.2
Mixture after 96 h
0.1
0.0
300
350
400
450
500
550
600
650
700
750
Wavelength (nm)
Fig. 4. UV–VIS spectra of the mixture of dyes, before (
) and after 24
Absorbance

(- - -) and 96 ( medium III.

) h of treatment with C. elegans UCP 542 on condition

dye, despite the fact that the studied dyes had a common stilbene-azo structural motif. In addition, it has been shown by toxicity tests and UV–VIS spectral analysis that the decolorization process involved biodegradation, in addition to the visually observed biosorption.

Acknowledgements

The authors gratefully acknowledge Prof. Dr. Ri- cardo L. Longo (DQF/UFPE) for assistance on ana- lytical interpretation of the experimental data and review of the manuscript; Dra. Sandra G. Moraes (IQM/UNICAMP, SP) for the toxicity tests and Dra. Adriana M.Y. Melo (Pesquisadora CNPq/Embrapa Semi- AArido) for helping with the statistical analyses. We would like to acknowledge the Brazilian agencies CNPq, CAPES, the programs FINEP/CTPETRO/AVINA GROUP and PRONEX for financial support.

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