Water Air Soil Pollut (2014) 225:2026

DOI 10.1007/s11270-014-2026-6

Comparative Analysis of Azo Dye Biodegradation

by Aspergillus oryzae and Phanerochaete chrysosporium
Graziely Cristina Santos & Carlos Renato Corso

Received: 13 January 2014 / Accepted: 4 June 2014

# Springer International Publishing Switzerland 2014

Abstract The textile industry often releases effluents

into the environment without proper treatment or complete dye removal. Azo dyes, which are characterized by
azo groups (NN), are frequently used in the textile
industry. Among the different wastewater treatment
methods available, biological treatment has been extensively studied. The aim of the present study was to
compare the biodegradation of the azo dye Direct Blue
71 by the fungi Phanerochaete chrysosporium and
Aspergillus oryzae in paramorphogenic form using a
100 g/ml dye solution. Biodegradation tests were performed within 240 h. The absorbance values obtained
with UV-VIS spectrophotometry were used to determine
the absorbance ratio and the percentage of dye discoloration following the biodegradation test. FTIR analysis
allowed the identification of molecular compounds in
the solution before and after biodegradation. Both
A. oryzae and P. chrysosporium demonstrated considerable potential regarding the biodegradation of dyes in
wastewater. These results may contribute toward improving effluent treatment systems in the textile industry.

G. C. Santos : C. R. Corso (*)

Departamento de Bioqumica e Microbiologia, UNESP
Univ Estadual Paulista, Campus Rio Claro, Instituto de
Biocincias,
Avenida 24 A, 1515 Bela Vista, 13506-900 Rio Claro, SP,
Brazil
e-mail: crcorso@rc.unesp.br
G. C. Santos
e-mail: grazielycs@gmail.com

Keywords Direct Blue 71 . Fungi . Amines .

Paramorphogenic form . UV-VIS . FTIR

1 Introduction
Textile effluents contain substances from different stages
of dyeing and finishing as well other processes. The
pollutants found in these effluents are primarily persistent organic substances, such as dyes and salts, giving
the effluent a low degree of biodegradability (Fu et al.
2011). Dyes are visible compounds that, when released
into the environment, can cause the appearance of color
in rivers, hindering the penetration of sunlight and thereby reducing the process of photosynthesis among different organisms in these ecosystems (Wang et al. 2005).
Azo dyes are the class of dyes with the largest number of representatives, accounting for 60 to 70 %, and
therefore constitute the majority of the components in
effluents from the textile industry (Hunger 2003; Van
der Zee et al. 2003). In addition to textile applications,
this class of dyes is still widely used in pharmaceutical,
food, and cosmetic industries. The main characteristic of
azo dyes is the binding of aromatic rings by azo groups
(NN) which, added to sulfonated substitutions,
contribute to the resistance of dyes to chemical and
microbiological degradation processes (Martins et al.
2001; Stolz 2001; Hu and Wu 2001).
There is a need to remove dye from waste effluents
before it mixes with watercourses. Biological methods
have typically been applied to remove organic compounds and color from textile effluents due to the low

2026, Page 2 of 11

cost and simple operation and maintenance of these

methods (Hunger 2003).
In an attempt to mitigate this contamination, studies
have been conducted to evaluate the biodegradation of
these compounds by microorganisms that have metabolic versatility and are capable of degrading structures
such as those found in azo dyes. A large number of
microorganisms belonging to different taxonomic
groups have been reported to demonstrate the ability to
decolorize azo dyes (Vitor and Corso 2008).
Biodegradation occurs by enzymes that attack and
break the most important chemical bonds in dyes (Mou
et al. 1991). Fungi are widely used in biodegradation of
azo dyes due to their main feature of producing extracellular enzymes able to degrade complex molecules. Species
such as Aspergillus sp., Phanerochaete chrysosporium,
Neurospora crassa, Rhizopus sp., and Pleurotus ostreatus
have demonstrated considerable potential regarding the
bioremediation of textile dyes (Corso and Almeida 2009;
Kaushik and Malik 2009; Enayatzamir et al. 2010; Jesus
et al. 2010; Teixeira et al. 2010; Corso et al. 2012).
P. chrysosporium is the most widely studied white rot
fungus in terms of the biodegradation of xenobiotic
(Robinson et al. 2001). This microorganism has been used
in the biodegradation of gaseous chlorobenzene (Wang
et al. 2008), the pesticide endosulfan (Kullman and
Matsumura 1996), the insecticide heptachlor (Arisoy and
Kolankaya 1998), and a number of different dyes (Cripps
et al. 1990; Paszczynski and Crawford 1995; Martins et al.
2001; Wesenberg et al. 2003; Santos et al. 2009). The
ligninolytic system of this fungus is represented mainly by
the enzymes laccase, lignin peroxidase, and manganese
peroxidase, which are produced in media containing limited sources of carbon and nitrogen. These enzymes have
the ability to depolymerize lignin and a variety of other
compounds (Stolz 2001; Teixeira et al. 2010).
The filamentous fungus Aspergillus oryzae is classified as an imperfect fungus (anamorphic) with no sexual
stage in its life cycle (Galagan et al. 2005). This
organism has been extensively used for the production
of fermented foods and beverages. However, there is
little information on its use for the biodegradation of
pollutants, such as dyes. Thus, A. oryzae has been used
with the aim of evaluating and comparing its
biodegradation ability with that of P. chrysosporium,
which is known for its efficiency in this process.
Corso and Almeida (2009) evaluated the ability of
A. oryzae regarding the bioremediation of dyes in textile
effluents and identified its potential in removing azo dyes

Water Air Soil Pollut (2014) 225:2026

from aqueous solutions. Shakeri et al. (2008) used a

recombinant peroxidase from A. oryzae for the decolorization of the anthraquinone Remazol Brilliant Blue R dye.
In the attempt to find alternatives for the treatment of
textile effluents, the aim of the present study was to
evaluate the biological treatment of the azo dye Direct
Blue 71 using two filamentous fungi in
paramorphogenic form, A. oryzae and
P. chrysosporium, and compare the effectiveness of
both. The paramorphogenic form was used to facilitate
the quantification of the biomass needed for treatment.

2 Materials and Methods

2.1 Dye
Direct Blue 71 (DB71), Color Index 34140 and CAS
4399-55-7, is a direct azo dye obtained from the SigmaAldrich Chemical Company, Inc.
2.2 Microorganisms and Culture Conditions
P. chrysosporium (CCB 478) was obtained from the
culture collection of the So Paulo Institute of Botany
(Brazil), and A. oryzae (CCT 5321) was obtained from
the culture collection of the Andr Tosello Tropical
Research and Technology Foundation (Brazil). The microorganisms were kept in test tubes with a 2 % malt
medium (Lodder 1970). The medium to
P. chrysosporium culture was modified with the addition
of 1 % peptone and 4 % glucose.
Modified Minimum Mineral Medium (Pontecorvo
et al. 1953), consisting of NaNO3, KH2PO4, KCl,
MgSO4, 7H2O, glucose, yeast extract, and distilled water, was used for the growth of the mycelial pellets.
P. chrysosporium and A. oryzae cultures were used for
the paramorphogenic process after 7 days of culturing,
following the method described by Marcanti-Contato
et al. (1997).
2.3 Dye Biodegradation Test
Samples were prepared in triplicate in test tubes with
1 ml of dye stock solution to 1,000 g ml1, 8 ml of
distilled water at pH 2.5, adjusted with H2SO4 0.01 M,
and 1.03 mg ml1 (dry weight) of P. chrysosporium in
paramorphogenic form. The tests with A. oryzae were
prepared with 1 ml of stock solution of dye, 1.1 mg ml1

Water Air Soil Pollut (2014) 225:2026

Page 3 of 11, 2026

(dry weight) of A. oryzae in paramorphogenic form, and

7.5 ml of distilled water at pH 2.5. The control was
prepared without biomass with 9 ml of distilled water
at pH 2.5 and 1 ml of dye stock solution. The samples
were incubated at 301 C, and scans were performed
every 24 h in a UV-VIS spectrophotometer (Shimadzu
UV-2401 PC), totaling 240 h at the end of the test. The
scan occurred at wavelengths of 800 to 190 nm in quartz
cuvettes with an optical path of 5 mm.
The biodegradation of DB71 dye was analyzed from
data obtained by UV-VIS spectrophotometry to
determine the absorbance ratio, following the method
described by Glenn and Gold (1983), as well as from
data obtained by Fourier transform infrared spectroscopy (FTIR) by the change of the dye molecular structure
before and after treatment.
The samples of every triplicate were analyzed using
the UV-VIS spectrophotometer and FTIR. Every spectrum was evaluated and the spectrum was chosen according the similarity between the results.

control solution were dried for 48 h at 1051 C and

remaining in a desiccator for 24 h for the manufacture of
the disks. After drying, the disks were prepared with
1 mg of dry dye and 149 mg of KBr by compression to
40 kN for 5 min. The disks were scanned in the 400 to
4,000 cm1 range, with 16 scans and 4 cm1 resolution.
Baselines were corrected to 4,000, 2,000, and 400 cm1.
The spectra were normalized and expressed in terms of
absorbance.
The Lorentzian deconvolution function was used for
the analysis of overlapping bands, following the method
described by Forato et al. (1998). Higher resolution
methods are based on the separation of the peaks that
make up the band of interest and the correlation of their
intensities or areas with secondary structures.
Deconvolution is a technique used to reduce the bandwidth of the spectra (Forato et al. 1998).

2.4 UV-VIS Spectrophotometry

3.1 Dye Biodegradation Test

The absorbance ratio determined from data of UV-VIS

spectrophotometry allows the identification of evidence
of biodegradation, which was confirmed after the FTIR
analysis of these solutions. The absorbance ratio values
were determined by the ratio between absorbance at two
different wavelengths (A583/A320), corresponding to the
chromophore group (583 nm) and azo group (320 nm)
(Silverstein et al. 1994). According to Glenn and Gold
(1983), a compound shows signs of degradation when
there is a great variation between the absorbance ratio
value of the treatment and the absorbance ratio of the
control. However, when the absorbance ratio remains
constant, the predominant process is biosorption, i.e.,
absorbance decreases proportionally, with no change in
the structure of the dye.

3.1.1 UV-VIS Spectrophotometry

2.5 Fourier Transform Infrared Analysis

The analysis of the dye solution in an FTIR Shimadzu
IRPrestige-21 spectrometer requires the preparation of
potassium bromide (KBr) disks with dye.
2.6 Preparation of KBr Disks
After each scan, samples from the degradation test were
reserved for the manufacture of disks. The samples and

3 Results and Discussion

Figure 2 shows the absorbance at the wavelengths of the

chromophore (583 nm) and azo (320 nm) groups and the
absorbance ratios for each 24 h over 240 h following
treatment with P. chrysosporium (Fig. 1a) and A. oryzae
(Fig. 1b).
Variation occurred in the absorbance ratio of the
treated samples in comparison to the control (0 h).
According to Glenn and Gold (1983), the biodegradation occurs if the absorbance ratio values of the samples
remain constant in this situation. Therefore, this variation suggests that the molecular structure of the dye has
changed, possibly indicating degradation.
For the P. chrysosporium, there was considerable
variation in the absorbance ratio in the first 24 h of
treatment, indicating the fungus was able to break bonds
of the dye molecule within a short contact time (Fig. 1a).
This fact was confirmed with analysis of the FTIR
spectrum. Further changes occurred between 96 and
120 h, after which the absorbance ratio gradually
decreased.
Changes occurred in the first 48 h for the A. oryzae
remaining relatively constant up to 144 h, when the
absorbance ratio changed (Fig. 1b). Changes in the
structure of the dye likely occurred at this time.

2026, Page 4 of 11

Water Air Soil Pollut (2014) 225:2026

Fig. 1 Absorbance values of chromophore and azo groups and absorbance ratio after treatment of DB71 dye with P. chrysosporium (a) and
A. oryzae (b)

Subpanels a and b of Fig. 2 display the absorption

spectra of samples treated with P. chrysosporium and
A. oryzae, respectively. The spectra correspond to the
control, 24 and 240 h (representing the beginning and
end of the treatment), and 144 h (representing an intermediate point of the treatment), when variations in the
absorbance ratio occurred with both fungi.
The absorbance at both 583 and 320 nm decreased
with each scan, demonstrating the removal of the dye
from the solution by the fungus. However, although the
absorbance ratios provide data indicating the occurrence
of biodegradation, this process can only be confirmed
after the identification of the characteristic bands of each
structure in the FTIR spectra.
The absorption in UV-VIS allowed visualizing differences between the treatments with each fungus. After

24 h of treatment with P. chrysosporium, the dye demonstrated a different spectrum from the control, with the
chromophore peak (583 nm) smaller and displaced. The
chromophore peak, from the treatment with A. oryzae,
was also smaller and slightly displaced; the same occurred with the other peaks. However, the absorbance
values were higher in comparison to those of
P. chrysosporium, indicating that no greater removal of
the dye occurred after 240 h of treatment with A. oryzae.
3.1.2 Fourier Transform Infrared Analysis
An analysis of the FTIR spectra is required to better
appreciate the absorption ratio changes and breaking of
molecule bonds by both fungi. The spectra measured
correspond to 24 h (Fig. 3), 144 h (Fig. 5), and 240 h

Fig. 2 Absorption spectra of dye solution after 240 h of interaction with P. chrysosporium (a) and A. oryzae (b) at 301 C, with scans
performed at 24, 144, and 240 h

Water Air Soil Pollut (2014) 225:2026

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Fig. 3 FTIR spectrum of control dye solution and samples after 24 h of treatment with P. chrysosporium and A. oryzae

(Fig. 6) following treatment with P. chrysosporium and

A. oryzae. The most significant changes in the structure
of the dye occurred in the 2,000 to 400 cm1 range.
Different bands from the control were found after the
first 24 h of treatment, indicating changes in the structure of the dye following contact with the fungi. The
most significant change regards the appearance of a new
band at 1,116 cm1 with A. oryzae. This region is
characteristic of amine groups (Jurez-Hernndez et al.
2008; Fanchiang and Tseng 2009). A. oryzae likely has
enzymes capable of breaking any azo connection
(NN) within the first hours, enhancing the amine signal. Therefore, this band appeared and remained in the
spectra at 144 and 240 h. The band in the 1,734 cm1
range, which was not in the control, was found after
treatment with both fungi. According to Wharfe et al.
(2010) and Forato et al. (1998), the 1,700 to 1,500 cm1
range corresponds to the protein, specifically the
stretching of the CO bond of the amide I peptide.
This band likely appeared due to the presence of enzymes produced by P. chrysosporium, which has an
important ligninolytic system, and those produced by
A. oryzae, which is widely known for the synthesis of
enzymes such as laccase. This band remained in all
treatments analyzed.

The band at 1,008 cm1 was found in the control

solution and the treatment with A. oryzae after 24
(Fig. 3), 144 (Fig. 5), and 240 h (Fig. 6). Stretching of
the SO bond of the sulfonic group occurs in this range
(Silverstein et al. 1994; Alvares et al. 2006; Dhanve
et al. 2009). As these bands were not evident in the
spectrum with P. chrysosporium, it is believed that the
enzymes of the A. oryzae were able to cause a change in
the sulfonic group that P. chrysosporium could not. The
band at 991 cm1, which indicates COH deformation (Robert et al. 2005), only occurred in the solutions
treated with A. oryzae after 24, 144, and 240 h. The
CO bond is present in naphthol (Pham et al. 1997)
and had a signal at 1,053 cm1 in the samples. However,
the signal intensified with P. chrysosporium, while the
band performed with less intensity with A. oryzae.
Therefore, the naphthol COH bond was altered
by both fungi, but to different extents.
The bands at 881 and 869 cm1 appeared less intense
in the treated solutions than in the control solution,
especially with A. oryzae. These bands are characteristic
of deformation of the CH bond of the aromatic ring
(Barbosa 2007; Polunin et al. 2008; El-Kabbany et al.
2010). Thus, the action of A. oryzae on the dye was
more effective in this structure after 24 h.

2026, Page 6 of 11

Water Air Soil Pollut (2014) 225:2026

Fig. 4 FTIR spectrum in 1,280 to 1,100 cm1 range of control dye solution (a) and 24 h after treatment with P. chrysosporium (b) and
A. oryzae (c) after Lorentzian deconvolution

The same deformation of the CH bond of aromatic

ring occurred in the 582 cm1 range of the control
solution (Polunin et al. 2008). Again, the biggest change
occurred in the spectrum with A. oryzae. The band at
594 cm1 decreased in intensity, demonstrating a band at
617 cm1 of the sulfonic acid group (Silverstein et al.
1994; Dhanve et al. 2009).
The band in the 1,226 cm1 range, corresponding
to the stretching of the sulfonic group (Khaled et al.
2009) and the C S of thiocarbonyl group
(Silverstein et al. 1994) was visible after both treatments, but apparently did not appear in the control.
This was due to the overlapping of the bands at
1,225, 1,201, and 1,176 cm1 in the control, visible
only after deconvolution using the Lorentzian function (Forato et al. 1998) in the 1,280 to 1,100 cm1

range. Figure 5 illustrates the deconvolution of the

spectra of the control solution (Fig. 4a) and dye
treated with P. chrysosporium (Fig. 4b) and
A. oryzae (Fig. 4c).
Lorentzian deconvolution allowed the identification
of overlapping bands, demonstrating the band in the
1,225 cm1 range in the control. The bands at 1,201
and 1,176 cm1 correspond to the stretching of the
CN bond (Romo et al. 2003; Yadav et al. 2007;
Barbosa 2007). However, only the band at 1,201 cm1
remained constant after treatment with both fungi. The
band at 1,176 cm1 displayed lower intensity in the
spectra of the dye after contact with P. chrysosporium
and A. oryzae. This decrease in intensity was visible
only with the deconvolution of the bands in the 1,280 to
1,150 cm1 range.

Water Air Soil Pollut (2014) 225:2026

Page 7 of 11, 2026

Fig. 5 FTIR spectrum of control dye solutions and samples after 144 h of treatment with P. chrysosporium and A. oryzae

The lesser intensity at 1,173 cm1 in the spectrum

with P. chrysosporium (Fig. 4b) and displacement to
1,185 cm1 in the spectrum with A. oryzae (Fig. 4c)
indicate that the enzymes synthesized by the microorganisms acted on one or more CN amine bonds,
causing a change and even a possible breakage of these
bonds.
After 144 h of treatment (Fig. 5), early new bands in
the 1,128, 1,109, and 1,037 cm1 range occurred in the
spectrum with P. chrysosporium. According to
Fanchiang and Tseng (2009), these bands are characteristic of the CNH2 bond. The appearance of primary
amines in the treated solutions suggests that there was
breakage of the azo bond. Another characteristic band of
the deformation of CN of the primary amine was
found in the 833 cm1 range, characteristic of the
CNH2 bond (Barbosa 2007; Telke et al. 2010). This
low-intensity band appeared in the spectra with both
fungi. As DB71 dye has three azo bonds, the appearance
of signs of primary amines is expected to intensify,
resulting from the breakage of these bonds during the
biodegradation process.
Another variation in the spectra occurred in the
1,400 cm1 range. This band remained unchanged in
relation to the control after 24 h (Fig. 3). After 144 h,
however, intensification of the band occurred in the

spectrum with A. oryzae (Fig. 5). This region is characterized by the CC stretch of naphthalene derivatives
(Barbosa 2007), the NN stretch (Cervantes et al. 2009;
Franciscon et al. 2009), and the presence of free amines
(Wharfe et al. 2010). Thus, the action of enzymes from
A. oryzae on the dye molecule interfered with the bonds
and may cause their rupture, releasing amines into the
solution.
The other bands in the spectra remained apparently with the same intensity, except the band in the
597 cm1 region, representing the deformation of the
CH bond of the aromatic ring (Polunin et al. 2008),
which decreased in the spectrum with A. oryzae.
Thus, the band at 619 cm1 related to sulfonic groups
(Dhanve et al. 2009; Silverstein et al. 1994) appeared
more intensely than at 597 cm1. The bands in the
1,008 and 991 cm1 range, corresponding to the
stretching of the SO bond, were again found only
in the spectrum with A. oryzae.
Among the changes in the spectra 240 h after treatment (Fig. 6), the most evident was in the 1,400 cm1
region with A. oryzae. A significant increase in the
intensity of this band occurred. It is likely that the azo
bonds were broken, as already mentioned, releasing
primary amines. The dye is triazo and as this dye has
an amine linked to a naphthol, the azo bonds of the

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Water Air Soil Pollut (2014) 225:2026

Fig. 6 FTIR spectrum of control dye solution and samples after 240 h of treatment with P. chrysosporium and A. oryzae

molecule broke and six new amines emerged; thus, the

band appeared intensified. The band at 1,112 cm1 was
also enhanced, supporting the hypothesis of the breakage of bonds and demonstrating the degradation of the
dye molecule.
Observing the spectra, an absence of new bands
was noted. However, the intensification of another
band from the sulfonic group was observed at
619 cm1 in the spectrum with A. oryzae. The
dye has four sulfonate groups. It is possible that,
after the breakage of some bonds, these groups
may have intensified their signal, thereby increasing the intensity of characteristic bands.
Evaluating the spectra of the treated solutions up to
240 h, A. oryzae caused the greatest changes in the
spectra, indicating greater efficiency in the biodegradation process. This finding is due to the fact that the first
24 h of treatment were sufficient for the appearance of
characteristic bands of amine, indicating the possible
breakage of azo bonds. P. chrysosporium was also able
to degrade the dye molecule, but required a longer time
to achieve breakage.

Telke et al. (2010) report that some species of

Aspergillus are able to decolorize a wide range of structurally different dyes and are more effective than the
widely studied basidiomycete P. chrysosporium. This is
consistent with the findings of the present study for both
biosorption and biodegradation.
The analysis of all information collected by FTIR
relating to the structure of the dye allows establishing
a biodegradation pathway for the DB71 dye molecule.
Figure 7 represents the molecule before biodegradation
and the possible molecules formed after the process in
an acid medium.
Considering the major studies conducted on azo
dyes, information on the biodegradation mechanism is
limited (Telke et al. 2010). The FTIR analysis demonstrated that the biodegradation of DB71 dye does not
occur equally with the two fungi tested. It is likely that
these fungi synthesize a range of enzymes in certain
quantities that interact differently. However, based on
the molecules identified, the metabolites formed at the
end of the biodegradation process suggest broken bonds
(Fig. 7).

Water Air Soil Pollut (2014) 225:2026

Page 9 of 11, 2026

Fig. 7 Pathway proposed for degradation of DB71 dye after treatment with P. chrysosporium and A. oryzae

It should be stressed that the proposed pathway does

not consider the complete mineralization of the dye. The
mineralization may occur if other conditions for the
biodegradation test are established, especially with regard to the time available for biodegradation to occur at
higher speeds, thereby creating conditions for the breakdown of aromatic rings. However, there is little information on the mineralization of these compounds. Thus,
the data generated in the present study are relevant to the
advancement of studies on the biodegradation of dyes,
especially azo dyes.

4 Conclusion
UV-VIS spectrophotometer and FTIR analysis allowed
the determination of the susceptibility of the DB71 dye
to degradation by both fungi tested. Biodegradation was
proven by the appearance of characteristic bands in the

FTIR spectra of the expected metabolites stemming

from the breakage of bonds in the dye. This process
occurred unevenly between the two fungi. However, at
the end of treatment (240 h), both A. oryzae and
P. chrysosporium had degraded the dye molecules in
solution generating similar metabolites.
The treatment with A. oryzae demonstrated more
significant signs of biodegradation in the first 24 h in
comparison to P. chrysosporium. Thus, it is likely that
enzymes from A. oryzae have greater affinity for the dye
molecules. P. chrysosporium also proved effective, but
not with the same potential as that of A. oryzae.
Therefore, P. chrysosporium and A. oryzae demonstrate
considerable potential for the treatment of textile effluents through biodegradation.
Acknowledgments We thank CAPES (Coordination for Enhancement of Higher Education Personnel), CNPq (National
Council for Scientific and Technological Development), and
FAPESP (So Paulo Research Foundation) for financial support.

2026, Page 10 of 11

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