Bioresource Technology 91 (2004) 6975

Decolorization of reactive azo dyes by Cunninghamella elegans

UCP 542 under co-metabolic conditions
S.T. Ambr

osio a, G.M. Campos-Takaki
a

a,b,*

Doutorado em Ci^
encias Biol

ogicas, Universidade Federal de Pernambuco, 50670-420 Recife-Pernambuco, Brazil
b
Departamento de Qu
mica e N

ucleo de Pesquisas em Ci^
encias Ambientais,
Universidade Cat

olica 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 eective in the decolorization of textile euents. The decolorization of dyes with dierent 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 prole 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 signicantly 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 respiration 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 presence of a nitrogennitrogen double bond (N@N),
namely the azo group, which is bound to aromatic
groups. Usually during the textile processing, around
3070% 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 exposure 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 euents (Robinson et al., 2001). Due to their genetic diversity and metabolic versatility, microorganisms
*
Corresponding author. Tel.: +55-81-32164017; fax: +55-8132714043.
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 pollution problem caused by reactive azo dyes (Alexander,
1994). Currently, bioremediation is becoming important
because it is cost eective, environmentally friendly, and produces 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); however, in many cases the metabolic products, usually aromatic amines (Hu, 2001), are toxic or even more toxic
than the starting azo dyes. Phanerochaete chrysosporium
has been reported to eciently degrade azo reactive dyes
such as Orange II, Congo red e Tropaeolim (Cripps
et al., 1990). In addition, it has recently been demonstrated that peroxidases (LiP and MnP), phenoloxidases
(laccases), and dioxygenases can act on specic recalcitrant pollutants by precipitation or transforming them
into other products, thus allowing for a possible better
nal treatment (Dur
an and Esposito, 2000).
It has been shown that some species of Basidiomycetes such as Phlebia tremellosa (Kirby et al., 2000),
Irpex lacteus, Pleurotus ostreaus (Novotn
y et al., 2001)
and Trametes modesta (Nyanhongo et al., 2002), can

70

S.T. Ambr
osio, G.M. Campos-Takaki / Bioresource Technology 91 (2004) 6975

nambuco State, Brazil by Gomes et al. (2000). The isolation and identication of strain are according to
ODonnell (1979). The culture was maintained on Sabouraud 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^extil 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
nal concentrations of 0.025 mM for the pure dyes and
0.034 mM for the mixture of dyes.

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 understood (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 substances such as aniline, as the sole source of carbon and
nitrogen (Emtiazi et al., 2001). Consequently, the eciency 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), signicantly 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.

2.2. Culture conditions

The fungal cultures were grown in 250 ml Erlenmeyer
asks using spore suspensions (3.8 108 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
modied 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 described earlier without the fungi. All experiments were

2. Methods
2.1. Microorganism and dyes
C. elegans UCP 542 was isolated from mangrove
sediment collected in the City of Rio Formoso, Per-

Table 1
Structure of azo dyes and their respective wavelength maximum absorption (kmax )
Dyes

kmax (nm)

Orange II

485

Chemical structure
OH
NaO3S

Reactive black 5

597

OH NH2
NaO3 SOCH2 CH 2 O2 S

N N

NaO 3 S

Reactive red 198

SO3Na

517

H 3C
NH
N

SO3Na
N

OH
N

NH

N
N
Cl

NaO 3S

SO 3 Na

SO2 CH 2 CH2 OSO3 Na

S.T. Ambr
osio, G.M. Campos-Takaki / Bioresource Technology 91 (2004) 6975

Table 2
Composition of media used in the dye decolorization experiments
Componentsa

Medium
I

II

III

IV

Peptone (10 g/l)

Sucrose (20 g/l)
KH2 PO4 (0.5 g/l)
Dye

X
X
X
X

X
X

X
X
X

X
X

71

structure, culture media, incubation period, and the interaction among them. The means of the signicantly
dierent main eects were compared by the Duncans
test at the 5% level using the Statistica program (Statsoft
Inc., 1997).

3. Results and discussion

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
UVVIS spectrophotometer (Spectronic Genesis, model
2-Spectronic Instruments Inc., USA). The wavelengths
for the measurements were set at the values presented in
Table 1 as kmax for the pure dyes, and at 511 nm for the
mixture. Dye concentration was calculated from an
absorbance x concentration calibration curve. All calibration curves yielded a linear range 0.0050.025 mM/l
and a linear regression coecient 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~ao
Paulo, Brazil). The indicator organism, E. coli ATCC
25922, was provided by Culture Collections of Tropical
Fundation Andr
e Tosello (University of Campinas, S~ao
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 involves the incubation of E. coli cultures at 37 C with
known amounts of the pollutant (solution-dyes). When
the CO2 concentration produced by microbial respiration reached 0.5 mmol/l, 45 ml of the cultures of the E.
coli was transferred into several asks 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 asks and the CO2 production monitored
every 20 min using ow injection analysis (FIA). The
test is described in detail in Moraes et al. (2000).
2.5. Statistical analysis
To evaluate the inuence 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

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 dierent 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 signicant (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 dierent
letters.
These results showed that for this particular fungus
the decolorization of the dyes solutions could be selectively supported by the media composition. For instance, 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 decolorization 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 signicant (P <
0:05) increase of the biomass (50% and 70%, respectively). Consequently the metabolism and the biosorption 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 decolorization of the other dyes not as signicant (Fig.
1A). Conversely, in the presence of peptone as the sole
source of organic nitrogen (medium II) the decolorization was not satisfactory, since the most signicant decolorization (48% after 72 h) was achieved for the

72

S.T. Ambr
osio, G.M. Campos-Takaki / Bioresource Technology 91 (2004) 6975

Medium II

0.65
a

1.0

Medium I

0.9

0.55

0.8

0.50

0.6

0.5
b
a

0.3

ab
a

b
ab
bb

bcc

0.35
ab

0.30

bc

0.25

c
ab
b

0.05

a
b

ab

0.20
ab

b
c

0.10

0.0

0.40

0.15

ab
b

0.1

ab

ab

0.4

b b

Decolorization (%)

Decolorization (%)

0.45

0.7

0.2

0.60

0.00
12

24

72

48

(A)

96

12

168

120

24

72

48

(B)

Time (hours)

96

Time (hours)

Medium III
1.4

Medium IV

168

120

1.0

1.2

Decolorization (%)

Decolorization (%)

0.8
a

1.0
0.8
a

ab

0.6

b
0.4

ab

b
b

bb
b

a
0.4

bb

b
ab
bc

bb

0.0

c
b

0.0
12

(C)

0.2
aa

a
c

0.6

bc

a
0.2

24

48

72

96

120

168

Time (hours)

12

(D)

24

48

72

96

120

168

Time (hours)

Fig. 1. Eect of medium composition I decolorization of the dyes orange II (j), reactive black (), reactive red ( ) and mixture ( ) by C. elegans
542. The letters indicate average values which are statistically dierent at P 0:05, using the Duncan test.

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 Viraraghavan, 2001) concerning the color removal reduction due
to the presence of inorganic nitrogen, such as ammonium 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 signicant just after 48 h of incubation.
These dierences can be interpreted as a negative in-

terference of peptone (medium I), as observed in medium 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 signicant decolorization 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 decolorization of dyes by this fungus treatment and that selective decolorization can be obtained by combining
dierent conditions.

S.T. Ambr
osio, G.M. Campos-Takaki / Bioresource Technology 91 (2004) 6975

70

60

Toxicity (%)

50

40

30

20

10

0
Orange II

Reactive black

Reactive red

Mixture

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 dierent as should be their metabolites.
The UVVIS 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 signicant, the UVVIS spectra
exhibit a shift of the maximum of absorption towards
shorter wavelengths upon fungal treatment. This indicates 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
Medium III

1.0

Medium IV

0.8
Control
Absorbance

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 2448 h of incubation; this strong color became
faint after 96 h and then returned to the original appearance 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 solution (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 important in decolorization (Novotn

y 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 9599% was
obtained (Sumathi and Manju, 2000). The dye everzol
turquoise blue was 98% decolorized by Coriolus versicolor 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 respiration of E. Coli when compared to the untreated solutions. 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, particularly 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 biodegradation 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

73

0.6

0.4

0.2

0.0
300

350

400

450

500

550

600

650

700

750

Wavelength (nm)

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

74

S.T. Ambr
osio, G.M. Campos-Takaki / Bioresource Technology 91 (2004) 6975

the UVVIS region were not signicant 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 wavelengths 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 conjugation eects 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 2530 nm in polyeniccarbonyl conjugated systems (Streitwieser et al., 1992).
In Fig. 4 we presented the UVVIS 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 dierences between the control and the solution 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 signicant spectral shifts
in the 500 and 400 nm regions.
Thus, the results of the UVVIS 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 UVVIS
spectroscopy to determine the kinetics of the biosorption and the degradation processes during the decolorization. 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 eect
upon the decolorization. This decolorization process
was also dependent upon the molecular structure of the
Mixture
0.6

Absorbance

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. UVVIS spectra of the mixture of dyes, before ( ) and after 24

(- - -) and 96 ( ) h of treatment with C. elegans UCP 542 on condition
medium III.

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 UVVIS spectral analysis
that the decolorization process involved biodegradation,
in addition to the visually observed biosorption.

Acknowledgements
The authors gratefully acknowledge Prof. Dr. Ricardo L. Longo (DQF/UFPE) for assistance on analytical 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

rido) for helping with the statistical analyses. We
Semi-A
would like to acknowledge the Brazilian agencies CNPq,
CAPES, the programs FINEP/CTPETRO/AVINA
GROUP and PRONEX for nancial support.
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