Professional Documents
Culture Documents
Chemistry Department, UAE University, P.O. Box 17551, Al-Ain, United Arab Emirates
h i g h l i g h t s
" Recent studies on the use of microbes and enzymes for bioremediation is surveyed.
" Various approaches using microbial/enzymatic degradation is summarized.
" Data is presented showing how various factors affect enzymatic dye degradation.
a r t i c l e i n f o
Article history:
Received 16 May 2012
Received in revised form 24 July 2012
Accepted 2 August 2012
Available online 17 August 2012
Keywords:
Biodegradation
Dyes
Degradation
Decolorization
Microbes
Enzymes
a b s t r a c t
Synthetic organic dyes are an extremely important class of compounds that are intimately linked to mod-
ern life, and are used in numerous industries such as food, textile, paper, plastics, and pharmaceuticals.
Upon release to the environment, the majority of these dyes not only impart color to water bodies (even
when present in small quantities), but directly impact aquatic and non-aquatic life due to their carcino-
genic nature. Removal of dyes from wastewaters has drawn a great deal of attention in the last few years
and various approaches have been developed to address it. Literature survey on this topic has revealed
the importance of biochemical approaches for handling the transformation of dyes to smaller, and more
environmentally friendlier molecules. The various enzymes, microorganisms and other species studied
for this purpose have been isolated from different matrices, such as soil and plants. This review focuses
the biochemically assisted transformation methods which are presently being explored to tackle the
problem of removing these organic pollutants from aqueous solutions.
2012 Elsevier B.V. All rights reserved.
Contents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 521
1.1. Cataloguing of dyes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 521
2. Decoloration and degradation of dyes by various methods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 521
2.1. Physical processes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 521
2.2. Advanced oxidation processes (AOPs). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 521
3. Bioremediation/biodegradation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 523
3.1. Using algae/fungi. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 523
3.2. Phytoremediation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 523
3.3. Using yeasts. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 524
3.4. Enzymatic decolorization and degradation of dyes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 524
3.5. Mechanisms of enzymatic degradation of dyes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 524
3.5.1. Degradation of azo dyes by azo reductases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 524
3.5.2. Azo dye degradation by laccases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 524
3.5.3. Dye degradation by peroxidases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 524
1385-8947/$ - see front matter 2012 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.cej.2012.08.015
Abbreviations: AB, Azure B; AC, Azure C; AOP, advanced oxidation process; BOD, biological oxygen demand; COD, chemical oxygen demand; EPR, electron paramagnetic
resonance; HOBT, 1-hydroxybenzotriazole; HRP, horseradish peroxidase; LC/MS, liquid chromatographymass spectrometry; LiP, lignin peroxidase; MB, Methylene Blue; MG,
Malachite Green; MnP, manganese peroxidase; MS, mass spectrometry; NAD
+
/NADH, nicotinamide adenine dinucleotide; NADP
+
/NADPH, nicotinamide adenine dinucleotide
phosphate; PCBs, polychlorinated biphenyls; RTB, Remazol Turquoise Blue G 133; SBP, soybean peroxidase; TOC, total organic carbon; TP, turnip peroxidase.
2
Compound II SH ! Peroxidase S
H
2
O 3
where SH indicates a generic substrate.
Both the above reaction steps are highly pH dependent. Com-
pound I is favorably formed in the presence of a network of hydro-
gen bonds (between the Fe-heme/H
2
O
2
adduct) and the distal
histidine and arginine side chains, whereas, the substrate oxidation
may depends on its protonation state [129].
Lacasse mediated degradation of vat dyes namely Cibanon Red
2B-MD, Cibanon Golden-Yellow PK-MD and Cibanon Blue GFJ-MD
(CI 69825) has also been reported in the literature and found to be
pH-dependent as well. It was shown in this study that dye removal
increased with an initial increase in pH (maximumactivity at pH 5)
and showed a parabolic decline, thereafter [130]. Our own study
with SBP/H
2
O
2
system also show that lowpH values of 35 are best
for SBP and that efciency of dye degradation falls at pH 2 and at
pH values above 5. In fact, the dye degradation is almost negligible
at pH value of 9 (Fig. 4).
4.3. Effects of enzyme and dye concentration
The degradation of dyes is very much affected by the enzyme
activity and the initial dye concentration. In some cases, e.g. Acid
Red 27 (AR27), the absolute enzyme activity can be crucial and be-
low a certain level, decolorization did not occur and an increased
amount of puried laccase catalyzed the complete decolorization
of recalcitrant AR 27 within 24 h [131]. Similarly in other studies,
varying concentrations of different dyes were tested and lower
concentrations (50500 mg/l) were reported to be best decolorized
[132134]. In another study, Lentinus crinitus cultured in Liquid
Minimal Medium was successfully used to degrade 0.1 g/l concen-
tration of Reactive Blue 220 (RB-220). However, the authors re-
ported that increasing concentrations of RB-220 signicantly
delayed fungal growth, suggesting that higher dye concentration
of dyes may result in decreased dye degradation because of their
toxicity to the microbial organisms [135]. Likewise, the effect of
initial Methyl Red dye concentration (750, 800, 850, 900, 950 and
1000 ppm) on the % decolorization by using an isolated Sphingo-
monas paucimobilis has also been published, which showed that
the percentage of dye decolorization decreased with increase in
the initial dye concentrations [136]. In summary, not only do high-
er dye concentrations adversely affect pure enzyme-based decolor-
ation processes, they can negatively affect microbial growth and
decrease the efciency of microbe-based dye degradation pro-
cesses as well.
4.4. Dye structure
Since microbial and enzyme-based dye degradation involve
binding of dyes to enzymes, it is not surprising that chemical struc-
tures of dyes strongly affect their decolorization efciencies. How-
ever, it is difcult to suggest the actual molecular mechanism,
because dye structure and efciency of redox mediators contrib-
utes largely to peroxidase mediated catalysis. Azo dyes are elec-
tron-decient molecules which can undergo degradation via azo
reduction. Studies of model azo dyes have shown that dyes which
have hydroxyl group either in the ortho- or para-position relative
to azo-bond were the most reactive ones and are also more prone
to oxidation when treated with peroxidase in the presence of redox
mediators. Moreover, the efciency of color removal of dyes is
strongly dependent on the steric effect of chemical substituents
on dyes. Upon substitution, most of the substrates become less
susceptible towards oxidation. Electron donating groups show en-
hanced susceptibility of the dye towards oxidative attack, whereas,
electron-withdrawing substituents were generally found to dimin-
ish the reaction rates. The electron-withdrawing substituent may
contribute towards recalcitrance of dyes which undergo redox
mediated enzymatic decolorization [137]. The main function of
the peroxidase/redox mediator thus consists of oxidatively render-
ing the azo-dye more susceptible to further nucleophilic attack and
nitrogen is eliminated in molecular form. Strong electron with-
drawing group such as sulfo groups at specic positions in an
azo dye are more easily biodegradable as compared to the ones
with a carboxyl group [138]. Dyes with sulfonate group (such as
pH 2 pH 3 pH 5 pH 7 pH 9
30
40
50
60
70
80
90
100
%
D
y
e
r
e
m
a
i
n
i
n
g
Fig. 4. Temperature dependence of peroxidase-mediated dye degradation. Trypan
Blue (40 ppm) was incubated with soybean peroxidase (40 U/ml) and 64 lM H
2
O
2
in different pH buffers for 5 min after which the amount of dye remaining was
measured using spectrophotometer.
526 M.A. Rauf, S. Salman Ashraf / Chemical Engineering Journal 209 (2012) 520530
Reactive Blue 15) were found to exhibit a strong electron-with-
drawing effect and thus exhibited low overall reactivity [110]. Lit-
erature ndings have also indicated a higher afnity of laccase for
anthraquinone dyes, for example, Jarosz-Wilkoazka et al. have
shown that various fungi could degrade Basic Blue 22 much more
efciently than the azo dye, Acid Red 183 [139].
4.5. Temperature change
Temperature is another parameter that appears to have an ef-
fect on the enzymatic degradation of dyes. For example, the decol-
orization ability of C. versicolor improved with an increase in
incubation temperature to 30 C as the optimum temperature
showing 92% decolorization of Cibanon Blue GFJ-MD in 10 days
[130]. Similarly, the temperatures for optimum growth, ligninase
activities and dye decolorization for most white rot fungi were
found to be around 2537 C [140]. We have also observed very
similar results for in vitro experiments using SBP/H
2
O
2
system,
where increasing the temperature from 25 C to 45 C led to in-
creased dye degradation (Fig. 5). In fact, this was also found to hold
for the bio-catalytic oxidation of environmental pollutant bisphe-
nol A by HRP [141]. As expected for enzyme-based biological sys-
tems, increasing the incubation temperature too high would lead
to microbial growth inhibition as well as to denaturation of en-
zymes, and hence to eventual decline in dye degradation efciency.
A simultaneous reduction in the efciency of the decolorization of
the dyes Bromophenol and Methyl Orange by about 50% was
shown in a recent study in the HRP/H
2
O
2
system wherein the tem-
perature was increased from 30 to 80 C [142]. This behavior is
most likely due to the thermal denaturation and subsequent failure
of enzymatic activity at higher temperatures.
4.6. Presence of redox mediators
Although enzyme-mediated degradation of dyes (either in vivo
(microbes) or in vitro (pure enzymes)) is very versatile and ef-
cient, there are some dyes that are not degraded (or degraded very
poorly) by enzymes/H
2
O
2
alone. For these dyes, the addition of cer-
tain chemicals known as redox mediator dramatically enhances
the degradation efciency. Frequently used redox mediators are
1-hydroxybenzotriazole (HOBT), veratryl alcohol, violuric acid, 2-
methoxyphenothiazone, etc. [143]. In the last few years, natural
compounds, such as syringaldehyde and acetosyringone, have also
been explored as eco-friendly laccase mediators for various envi-
ronmental applications [144]. The mechanism by which redox
mediators play a role in laccase-mediated oxidation reactions is
not well known. The oxidation of a substrate by a laccase/peroxi-
dase enzyme occurs because the redox mediator forms cation rad-
icals, which can be formed by two mechanisms. Firstly, the
substrate can undergo a one-electron oxidation in the presence
of a redox mediator and transform to a radical cation and secondly
the mediator can abstract a H-atom from the substrate and convert
it into a radical, which can then cause the substrate to co-oxidize
[145]. There are numerous published examples on the use of medi-
ators to efciently degrade various classes of dyes. For example,
Fig. 6 shows SBP/H
2
O
2
alone failed to degrade Rhodamine B, how-
ever as soon as the mediator HOBT was added to the reaction mix-
ture, the dye degraded almost completely. Similarly, Immobilized
turnip peroxidases in the presence of HOBT have been efciently
used to degrade Direct Red 23, Direct Red 239, Direct Blue 80
and Direct Yellow 4 dyes [113]. Furthermore, researchers have re-
ported examining the efciency of six different mediators together
with fenugreek seed peroxidase (with HOBT being the best), to
decolorize textile efuents [146]. In an another study it was dem-
onstrated that Malachite Green (MG) decolorization was enhanced
in the presence of all mediators tested, however vanillin was found
to be more effective in laccase-mediated degradation of MG than
HOBT[147]. Additionally, this study also demonstrated that lac-
case/mediators system could produce metabolites that were less
toxic than the parent compound [147]. Interestingly, a different
laccase-mediated study showed that HOBT was the best mediator
in decolorizing textile wastewater efuent, but it was found that
only laccaseacetosyringone treated efuent was not toxic,
whereas crude and laccaseHOBT treated efuent remained toxic
[148]. Clearly, it appears that different mediators degrade different
dyes via different mechanism, some of which may produce still
toxic metabolites.
Lastly, it is worth highlighting the amazing potential these mi-
crobes/enzymes offer for wastewater remediation. For example, re-
cently, a bacterial strain exhibiting laccase activity was isolated
and identied as B. licheniformis LS04. The spore laccase of this
strain was found to be resistant to inactivation by high tempera-
ture and alkaline conditions. This bacterial enzyme in the presence
of acetosyringone, as a mediator, effectively decolorized a range of
synthetic dyes such as Reactive Blue 19, Reactive Black 5 and Indi-
go Carmine under neutral to alkaline conditions. These unusual
and potentially very useful properties should be further explored
for a wide range of industrial applications [149].
5. Conclusion
Biochemically assisted processes are important techniques for
the transformation/degradation of synthetic dyes. In this article,
we have reviewed the various biochemical methods which are
used for dye degradation. These include the microbial degradation,
methods using algae/fungi, yeasts and pure enzymes. The various
reports that shed light on the importance of these tools for
25 30 35 40 45 50
30
35
40
45
50
55
Reaction temperature (
o
C)
%
D
y
e
d
e
g
r
a
d
a
t
i
o
n
Fig. 5. Temperature dependence of peroxidase-mediated dye degradation. Trypan
Blue (40 ppm) was incubated with soybean peroxidase (40 U/ml) and 64 lM H
2
O
2
in pH 7 buffer at various temperatures for 2 min after which the amount of dye
degraded was measured using spectrophotometer.
200 300 400 500 600 700
0.0
0.5
1.0
1.5
2.0
2.5
Wavelength (nm)
A
b
s
Dye
Dye + H
2
O
2
+ SBP
Dye + H
2
O
2
+ SBP + HOBT
Fig. 6. Requirement of the mediator HOBT for peroxidase-mediated degradation of
Rhodamine B. The solid and long-dashed lines show the dye alone or in the
presence of SBP and H
2
O
2
. The short-dashed line shows the dye in the presence of
SBP, H
2
O
2
and HOBT (unpublished data).
M.A. Rauf, S. Salman Ashraf / Chemical Engineering Journal 209 (2012) 520530 527
handling the transformation of dyes to smaller, environmentally
friendlier molecules have been reviewed and cited. The ndings
indicate that degradation/decoloration rates can be inuenced by
operational parameters such as the amount of a biochemical, pH,
temperature, dye structure and concentration of organic dyestuff
besides the presence of mediators and other additives. Addition-
ally, many of the cited studies focus on the optimization of the
above mentioned conditions which vary from case to case. It is
therefore clear that systematic and careful optimization studies
as well as metabolite toxicity testing must be carried out for each
system (dye and microbe (or enzyme) or mediator), as to-date it is
not very clear how and why certain dyes are degraded while others
are not. In fact, our preliminary survey of degradation of 13 diverse
classes of dyes using the SBP/H
2
O
2
system shows that some of the
dyes are readily degraded with SBP/H
2
O
2
alone, while others re-
quire mediators, and yet there is a third group of dyes that are to-
tally recalcitrant to enzymatic degradation (at least with HOBT as a
mediator) (Table 1). Although this review is non-exhaustive in the
scope of biochemically assisted degradation of dye degradation, it,
however, addresses the fundamental principles and applications in
this area. Continued research in this area could give us further in-
sight as to how new biological techniques can help with the issue
of wastewater pollution.
Acknowledgement
The authors graciously acknowledge the kind nancial support
by UAEU/NRF Research Grant Program 27/11/2 to S.S.A. and M.A.R.
The authors also thank Ms. Umme Kalsoom for sharing some of her
data shown here.
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Table 1
Examples of some dyes that can be degraded by peroxidases alone (with H
2
O
2
), some
that require mediators (with H
2
O
2
), and some that are totally recalcitrant.
Peroxidase only
degradable
Peroxidase and HOBT
requiring
Recalcitrant
Remazol Turquoise Blue G Tartrazine Naphthol
Yellow
Trypan Blue Orange G Chlorophenol
Red
Naphthol Blue Black Methylene Blue
Brilliant Yellow Toluidine Blue
Methyl Blue Rhodamine B
Congo Red
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