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Review

Survey of recent trends in biochemically assisted degradation of dyes


Muhammad A. Rauf, S. Salman Ashraf

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.

Corresponding author. Tel.: +971 503126075.


E-mail address: salman.ashraf@uaeu.ac.ae (S. Salman Ashraf).
Chemical Engineering Journal 209 (2012) 520530
Contents lists available at SciVerse ScienceDirect
Chemical Engineering Journal
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4. Factors affecting microbial and enzymatic decolorization. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 525
4.1. Effect of oxygen. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 525
4.2. Changing pH . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 526
4.3. Effects of enzyme and dye concentration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 526
4.4. Dye structure. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 526
4.5. Temperature change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 527
4.6. Presence of redox mediators . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 527
5. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 527
Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 528
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 528
1. Introduction
Due to the enhanced industrial activity, newer chemicals are re-
quired which are generally synthetic in nature. Many of these
chemicals are organic macromolecules and are classied as dyes.
Due to the extensive use of these dyes in industries, they have be-
come an integral part of industrial efuent. In fact, of the one mil-
lion ton of organic dyes annually produced worldwide, more than
11% is lost in efuents during manufacture and application pro-
cesses [1]. Most of these dyes are harmful and potentially carcino-
genic in nature and their exclusion from wastewaters is a major
environmental problem [26]. The presence of dyes in water im-
parts color to it which can block sunlight penetration and oxygen
dissolution, both of which are essential ingredients for aquatic life.
Thus, there is a considerable need to treat these colored efuents
before discharging them to various water bodies. To achieve a via-
ble development with low environmental impact, it is necessary to
remove a wide range of environmental contaminants. Water reser-
voirs comprising both polluted wastewaters and groundwater
from seas, rivers and lakes are of special concern to people working
in water purication and the environment in general. Therefore,
water quality standards and regulations with regards to hazardous
pollutants have become increasingly stringent [7].
1.1. Cataloguing of dyes
Dyes are an important class of organic macromolecules which
are an integral part of our lives and are used in numerous indus-
tries. For example, textile, paint and plastic industry, dye sensitized
solar cells, optics, metal extraction, sensors, etc. are industries that
depend heavily on dyes. Molecular structure, source, color and
method of application in color index (CI) are some of the properties
used for the classication of dyes. Dyes can be more systematically
classied based on the chromophores present in these chemicals.
These include the acridine dyes, azo dyes, arylmethane dyes,
anthraquinone dyes, nitro dyes, xanthenes dyes, quinineamine
dyes, etc. Fig. 1 summarizes the structures of various classes of
dyes along with an example of each class.
Many industries such as textiles, papers, leathers, and gasoline
are extensive users of azo dyes which comprise the largest group
of synthetic organic chemicals. The resulting by-products and the
waste generated by these industries contain both dyes and metal
ions. These contaminants when present in the environment be-
come hazardous. The insoluble dyes have low biodegradability
and only 4547% dyestuffs are known to be biodegradable [8].
The major characteristic of azo dyes are the nitrogen to nitrogen
double bonds (AN@NA) that are usually attached to two moieties
of which at least one but usually both are aromatic groups (ben-
zene or naphthalene rings). Some typical examples of azo dyes
are Methyl Orange, Acid Orange 7, Acid Orange 20, Orange II,
Methyl Red, Reactive Red 2, Reactive Orange 16, Reactive Black 5,
Congo Red, Solvent Red 1, Direct Blue 160, Basic Yellow 15, Basic
Blue 41, Disperse Orange 1, Disperse Red 1, Amido Black, Remazol
Brilliant Orange 3R, Amaranth, etc. Depending upon the number of
AN@NA groups in the molecule, azo dyes can be further classied
as monoazo (Acid Orange 7, Orange G, Methyl Red, etc.), diazo
(Congo Red, Trypan Blue, etc.), and triazo (Direct Blue 71, Chloran-
tine Fast Green BLL, etc.), as shown in Fig. 2. Due to the toxic nature
of azo dyes and their impact on the environment, various research-
ers have focused their attention on removing these chemicals from
wastewaters by using various physical and chemical means.
2. Decoloration and degradation of dyes by various methods
2.1. Physical processes
Decontamination of dye efuents have been a concern to the
scientic community for quite some time. The classical technique
includes the adsorption method, which has been extensively docu-
mented in the literature [911]. The selection of an adsorbent is
based on its characteristic properties such as high afnity, pore
size, retention and adsorbent regeneration. Although activated car-
bon has been classically and effectively used for this purpose, it is
not very practical due to its high cost. Lowcost adsorbent materials
like peat, bentonite clay, y ash, sand, polymeric resins, ion
exchangers and many biological materials such as, corn/maize
cobs, maize stalks, and wheat straw for the color removal of dye
wastewater have been suggested to make the process more eco-
nomical and feasible [1216]. However, the major limitation in
using these adsorbents is associated with their regeneration or dis-
posal as well as high sludge production.
Physical methods based on coagulation, occulation and sedi-
mentation of dyes are another set of effective means for the re-
moval of sulfur and disperse dyes [1719]. The low color
removal efciency and large amount of sludge produced limits
the application of these techniques, especially towards the acid, di-
rect, reactive and vat dyes.
Filtration methods (ultraltration, nanoltration) and reverse
osmosis have also been explored for water reuse and chemical
recovery [2022]. The membranes have also been used for the sep-
aration of hydrolyzed dyestuffs in the textile industry. They simul-
taneously reduce color, BOD and COD of wastewater. The selection
of the type of membrane and porosity of the lter depends upon
the chemical composition of the wastewater and the specic tem-
perature required for the process. However, high investment costs,
potential membrane fouling and the production of secondary
waste streams which need further treatment are the major draw-
backs in using membranes in this work [23].
2.2. Advanced oxidation processes (AOPs)
The advanced oxidation processes appear to be an emerging ap-
proach, which have been successfully used for the removal of sol-
uble organic contaminants from water and soil. The method
utilizes the strong oxidizing species such as

OH radicals produced
M.A. Rauf, S. Salman Ashraf / Chemical Engineering Journal 209 (2012) 520530 521
Diazonium Acridine
Anthroquinone Triarylmethane
Azo Quinone-immine
Xanthene(fluorene) Phthalocyanine
O NH
2
N
S NH
C
N N
N
N
N
N
N
N
N
N
Cu
X
X
X
X
N
N N Cl
O
O
Fig. 1. Structures of some of the diverse classes of textile dyes.
Fig. 2. Sub-classes of azo dyes, based on the number of azo groups.
522 M.A. Rauf, S. Salman Ashraf / Chemical Engineering Journal 209 (2012) 520530
in situ, which causes a sequence of reactions thereafter to break
down the macromolecules into smaller and less harmful sub-
stances. The macromolecule in most of the cases is completely
mineralized into water and carbon dioxide. As compared to the
classical approaches, the biggest merit of AOP technique is its eas-
iness to handle and production of signicantly less residuals. Read-
ers are directed to a recent review by the authors on the
application of AOPs for dye degradation [24]. The various AOPs
include photolysis [2528], Fenton process [2934], ozonation
[3538], photocatalysis [3944], radiation induced degradation
[4547] and sonolysisis [4850].
3. Bioremediation/biodegradation
Bioremediation/biodegradation is the process of removing pol-
lutants from the environment by biological methods and uses met-
abolic potential of microorganisms to degrade a wide variety of
compounds. This treatment causes the contaminant to be trans-
formed into smaller molecules which are considerably less harmful
to the environment. Removal of pollutants from the environment
by biological methods has signicant advantages over other meth-
ods because of the adaptability of various microorganisms in
degrading various compounds. Environmental microbiology has
provided new dimensions towards the understanding of degrada-
tion pathways and to their working mechanisms [51,52]. Further-
more, it is an environmentally friendlier technique which leaves
the ecosystem intact. The bioremediation process can also deal
with lower concentration of contaminants, whereby the cleanup
by physical or chemical methods would not be feasible. Its major
drawback is the fact that the process may take longer and is less
predictable than conventional methods.
The main advantage of bioremediation is that it is cost effective
as compared to conventional techniques. Besides being economical
in nature, it may lead to complete mineralization of the pollutant.
A great deal of attention in recent years has been focused on micro-
bial biodegradation of pollutants to protect our environment from
the manmade contaminants. The bioremediation and biotransfor-
mation methods are based on the microbes activity to degrade a
certain compound. They can be easily used to treat compounds
such as polyaromatic hydrocarbons, polychlorinated biphenyls
(PCBs), radioisotopes and heavy metals [5356]. The usefulness
and compliance of microbial degradation to hazardous waste has
also demonstrated its prospects to clean soil and water. Literature
review on this subject reveals the importance of biodegradation of
various wastewater efuents containing dye solutions using
microorganisms due to its low cost, ability to produce less sludge
and environmental compatibility. In this regard, many studies have
indicated that microorganisms like Bacillus subtilis, Phanerochaete
chrysosporium, Aeromonas hydrophila, Penicillium sp., Klebsiella
pneumoniae, Proteus mirabilis and Pseudomonas cepacia have shown
very promising results for dye degradation [5759].
The degree of saturation and aeration of an area are the main
factors in choosing a certain type of a technique. The following
strategies namely in situ and ex situ can be used in biodegradation.
In situ techniques are dened as those that are applied to soil and
groundwater at the site with minimal disturbance [60], whereas, ex
situ techniques are those that are applied to soil and groundwater
at the site which has been removed from the site by digging of soil
or injecting water [61]. The addition of microorganism to degrade
pollutants would normally be termed as Bioaugmentation [62].
Azo compounds can undergo biological degradation under both
aerobic and anaerobic conditions. The degradation generally occurs
by reductively cleaving the azo bonds (AN@NA) by microbes un-
der anaerobic conditions. This involves the transfer of electrons
or reducing equivalents. The process is known to occur in two
stages at the azo linkage, and in each stage two electrons are trans-
ferred to the azo dyes, which act as nal electron acceptors. This
results in dye degradation and the formation of colorless com-
pounds [63]. The resulting intermediate metabolites are also prone
to further microbial degradation [64]. Azo dyes are normally decol-
orized under anaerobic conditions and this is a relatively simple
and non-specic process and has been reported by many groups.
Azo dyes might act as an electron acceptor provided by the elec-
tron transport chain carriers [65]. It was also reported that in
anaerobic conditions the permeation of these dyes through biolog-
ical membrane into the microbial cells acts as the principal rate-
limiting factor for decolorization [66].
3.1. Using algae/fungi
Efuents containing dye molecules can be treated effectively by
fungi [6771]. The fungalmycelia have an advantage over single cell
organisms because they can dissolve the insoluble substrates by
producing extracellular enzymes. The large cell-to-surface ratio
in fungi makes them more suitable for physical and enzymatic
interactions with the environment. Fungal enzymes are also capa-
ble of tolerating high concentrations of the toxic species. Literature
survey reveals that studies on the azo dye biodegradation have fo-
cused on cultures from white rot fungi which have been used to
develop bioprocesses for the mineralization of such dyes [72].
Amongst the class of white-rot fungi, P. chrysosporium is the most
widely studied, although considerable attention has also been fo-
cused on others, such as Trametes (Coriolus) versicolor, Bjerkandera
adusta, Aspergillus ochraceus, species of Pleurotus, and Phlebia,
Fomes sclerodermeus, and a variety of other isolates [7376]. Long
growth cycle and the need for nitrogen are some of the limiting
conditions for the removal of dyes from textile wastewater while
using the white-rot fungi. White-rot fungi are not naturally found
in wastewater, thus its preservation and long termculturing in bio-
reactors is also a matter of concern [77].
3.2. Phytoremediation
Plants can be used for treating environmental problems. The
method commonly called as phytoremediation, reduces the envi-
ronmental problem without digging out the contaminant material
and disposing it off elsewhere. The technique is based on removing
the contaminants from soil, water, or air, with plants. These plants
are able to degrade or remove various types of organic and inor-
ganic species from the up-taken media. The method is a promising
approach in the decolorization of dyes because it is cost-effective,
has aesthetic advantages and long-term applicability, and can be
directly applied at the hazardous waste sites [78]. The main advan-
tages of phytoremediation are the low cost, the recovery of impor-
tant metals, and the potential of being the least harmful method.
The environment is preserved by using these naturally occurring
organisms [79]. Phytoremediation is most useful when the plants
used for this purpose have deep, brous roots and fast growth,
such as grasses. Some limitations in using this technique include
the surface area and depth occupied by the roots. Slow growth
and smaller biomass requires long-term assurances. Plant survival
depends on the general condition of soil and its toxicity. Plants can
uptake trace amounts of contaminants, like metals which can enter
into the food chain. This requires that the contaminated plant
material be discarded off properly. Therefore, not surprisingly very
few reports on phytoremediation of textile dyes are available. For
example the plant Phragmites australis have been studied for the
degradation of Acid Orange 7 (AO7) dye [80]. Likewise, Typha
angustifolia L. has been used in wastewater treatment containing
reactive dyes [81]. Additionally, a 75% reduction in color in wet-
lands vegetated with coco yam plants has been reported in the
M.A. Rauf, S. Salman Ashraf / Chemical Engineering Journal 209 (2012) 520530 523
literature [82]. Whole plants and tissue cultures of Blumea mal-
colmii H and Typhonium agelliforme have been found to degrade
dyes such as Malachite Green, Red HE8B, Methyl Orange, Reactive
Red 2, Brilliant Blue and Direct Red 5B [83,84]. Common sorrel (Ru-
mex acetosa) has shown promising results for the removal of sulfo-
nated aromatic compounds from dye and textile industrial
efuents [85]. Other examples include the use of Tagetes petula
(Marigold) to degrade Reactive Red 198 [86] and Aster amellus for
decolorization of textile dye Remazol Red [87].
3.3. Using yeasts
Yeasts have been used by many researchers to degrade dyes. For
example, Debaryomyces polymorphus has been used to degrade
Reactive Black 5 dye [88], whereas, some yeast species isolates
such as Trichosporon, Cyberlindera, Barnettozyma and Candida col-
lected from rain forests have also been reported for the degrada-
tion of dyes [89]. Recently, Bakers yeast has also been employed
for the degradation of Astrazone basic dye [90]. Galactomyces geot-
richum MTCC 1360 was shown to have a promising removal ef-
ciency (88%) in mixtures of structurally different dyes (Remazol
Red, Golden Yellow HER, Rubine GFL, Scarlet RR, Methyl Red,
Brown 3 REL and Brilliant Blue) [91]. Crystal Violet, Phenol Red,
Malachite Green, Methyl Green and Fuchsin were degraded into
non-toxic compound by using Staphylococcus epidermidis [92].
More recently, a detailed study has been reported on the isolation
of yeasts and their ability to degrade various dyes [93].
3.4. Enzymatic decolorization and degradation of dyes
A number of micro-organisms including bacteria, fungi, and
yeasts have been found to decolorize textile dyes. It has been
known that decoloration rate of dyes generally becomes less by
using microorganisms and decreases with increasing dye concen-
trations above certain levels. This factor may strongly limit the ef-
ciency of bio-elimination of many dyes. Enzymatic degradation is
preferred in cases where the target molecule or additives inhibit
the growth process. A large number of reports show that enzymes
have been used for the removal of dyes from aqueous solution un-
der certain environmental conditions. The dye molecules are de-
graded by only a few enzymes because of the structural variation
in these macromolecules. The main mechanistic feature of a bio-
catalyst is that it acts as a redox-active molecule and thus exhibits
relatively wide substrate specicities. Reactive free radicals are
generated by enzymes and these radicals are responsible for caus-
ing a complex series of spontaneous cleavage reactions. Some com-
mon examples of enzymes used for dye degradation are lignin
peroxidases, laccases, horseradish peroxidases, soybean peroxi-
dases, tyrosinases, polyphenol oxidases, azo-reductases, etc.
[9497]. Azo reductases and laccases appear to be very promising
enzymes for bioremediation of azo dyes [98,99].
3.5. Mechanisms of enzymatic degradation of dyes
Recently, there has been an increased interest in determining
the exact mechanism of how these organic pollutants are broken
down. Depending on the enzyme used, different mechanistic path-
ways have been reported in the literature and reviewed below:
3.5.1. Degradation of azo dyes by azo reductases
Degradation of azo compounds by azo reductases has been
shown to be almost exclusively anaerobic in nature. There are
numerous reports of recalcitrant azo dyes being efciently de-
graded by anaerobic microbes (due to their azo reductases) or puri-
ed azo reductase enzymes, but only under anaerobic conditions
[100]. These reactions require reducing cofactors like nicotinamide
adenine dinucleotide (NAD
+
), nicotinamide adenine dinucleotide
phosphate (NADP
+
), etc. for catalyzing the enzymatic reduction of
azo dyes by azo reductases. Since these azoreductases are cytosolic
in nature, it is assumed that azo dyes have to be transported into
cell before they are degraded by dye-degrading anaerobic
microbes. However, some studies have suggested an alternative
mechanism for high molecular weight and highly charged dyes,
which are unlikely to pass through the cell membranes. It has been
hypothesized that some of the azo dye reducing activity of the dye
may not be dependent on the intracellular uptake of the macro-
molecule [101]. This alternate proposed mechanism suggests the
involvement of the electron reduction of these dyes in the extra-
cellular environment of the microbes. For this to happen, the
bacteria should rstly link itself with the intracellular electron
transport system and the dye molecules. This linkage requires that
the electron transport component must be present in the outer
membrane of the bacterial cells, so that at the cell surface, the
dye and the redox mediator comes in a direct contact. Moreover,
it has been shown that redox mediators acting as electron carriers
can dramatically increase the degradation of dye molecules by azo
reductases [101]. The mediator compounds can be generated by
the microbial metabolism or they may need to be added externally.
As mentioned earlier these reactions work only in the absence of
oxygen, as oxygen can inhibit the reduction mechanism and pref-
erentially oxidize the redox mediators as compared to the dye
molecule [102].
3.5.2. Azo dye degradation by laccases
Laccases are copper-containing multimeric glycoproteins that
have generic phenol oxidase activity [103]. The presence of copper
gives a blue color to these enzymes and is responsible for the ac-
tual oxidation of the substrate. Laccases use molecular oxygen to
oxidize various aromatic and non-aromatic compounds by
abstracting protons and creating radicals in the mechanistic pro-
cess. These radicals can then further participate in other reactions
such as polymerization, hydration or proton abstraction. Degrada-
tion of phenols, pesticides, and aromatics in efuents either in the
free or immobilized form have been explored by using various en-
zymes. Laccases isolated from various sources have also shown to
degrade dyes as well [104106].
3.5.3. Dye degradation by peroxidases
Both azo and non-azo dyes can be efciently degraded by vari-
ous peroxidases as well. Although there are various peroxidases
that are commonly employed for remediation of dye-contaminated
wastewater, they all share a common mechanism in which the
heme groups are the main constituents and are responsible for
catalyzing the reactions in the presence of hydrogen peroxide.
Although peroxidases and polyphenol oxidases participate in the
catalysis of a broad range of substrates and can also work at very
low concentrations, they have generally not been used for the deg-
radation of dyes on a larger scale due to their low catalytic activity
and high purication cost [107]. However, recent studies
employing redox mediators have shown very promising results
[108110].
Peroxidases from Momordica charantia have been shown to be
very effective in decolorizing disperse dyes [111]. A wide variety
of industrially important dyes such as Naphthalene Black 12B, Coo-
massie Brilliant Blue R 250, Evans Blue, Eriochrome Black T, Car-
mine, Methyl Orange, Coomassie Brilliant Blue G 250, Rhodamine
6G, Methylene Blue and Methyl Violet 6B and Celestine Blue were
also treated with M. charantia and the decolorization rate was
found to increase signicantly in the presence of free radical medi-
ator 1-hydroxybenzotriazole (HOBT) [112]. Turnip peroxidase (TP)
has also been shown to have an appreciable effect on the degrada-
tion of three dyes namely Direct Red 23, Direct Red 80 and Direct
524 M.A. Rauf, S. Salman Ashraf / Chemical Engineering Journal 209 (2012) 520530
Red 239. Moreover, the immobilized TP treated dye solutions
exhibited great loss of total organic carbon (TOC) from the
wastewater which suggested that the major organic compounds
could have been removed out of the treated samples [113].
Peroxidase from cauliower bud (Brassica oleracea) has also
been shown to be effective for the degradation of various dyes such
as Reactive Red 2, Reactive Black 5, Reactive Blue 4, Disperse
Orange 25 and Disperse Black 9 [114]. The ndings showed that
in the presence of the HOBT, various dyes can be cheaply and ef-
ciently degraded by the soluble cauliower bud peroxidases.
Peroxidase from cauliower bud was found to be a better choice
than other vegetable peroxidases due to their thermal stability, be-
sides being operational in a wide range of pH, and their effective-
ness at low concentrations of redox mediators in degrading the
dyes. Decolorization of Acid Orange 7 using peroxidase enzyme
produced by the fungus C. cinereus has also been reported in the lit-
erature. Under optimized conditions of pH, dye concentration and
temperature, an overall removal of the dye was reported in a very
short time [115]. Although these enzymes are more genetically re-
lated to other fungal peroxidases including lignin peroxidase (LiP)
and manganese peroxidase (MnP), they are very similar to classical
plant peroxidases such as horseradish peroxidase (HRP) rather
than the ligninolytic peroxidases in substrate specicity, pH opti-
mum (nearly neutral) and specic activity.
The partial decoloration of industrial dyes solutions and textile
efuents by means of HRP, soybean peroxidase (SBP), and radish
peroxidase has been reported in the literature [116118]. It has
been shown that SBP can oxidize various substrates and is also
highly stable in terms of thermal and chemical denaturation which
thus makes it suitable for industrial applications [119,120]. SBP
was used to catalyze the degradation of Remazol Turquoise Blue
G 133 (RTB) and the reaction products were analyzed by LCmass
spectrometry (MS), ion chromatography and EPR techniques. The
analysis showed that SBP breaks the phthalocyanine ring produc-
ing sulfophthalimide and releases ammonium and Cu(II) ions
[121].
In an another study, the oxidation of the two dyes namely Meth-
ylene Blue (MB) and Azure B (AB) were degraded by horseradish
peroxidase (HRP) and compared to lignin peroxidase (LiP). Results
show that HRP is able to N-demethylate both dyes, but exhibits
much slower reaction kinetics than LiP and requires higher H
2
O
2
concentrations. Product yields were also found to be different for
HRP, and contrary to LiP, HRP was unable to achieve aromatic ring
cleavage. Azure C (AC), which is formed by sequential oxidation of
either MB or AB, was a major reaction product in HRP-mediated
reactions [122]. Horseradish peroxidase enzyme (HRP) has also
been reported in the literature for the possible removal of Erio-
chrome Blue Black R and Fluorescein by a process involving chem-
ical transformation and polymerization [123]. For azo dyes,
degradation by peroxidase/H
2
O
2
system has been reported to pro-
ceed via symmetric or asymmetric azo bond cleavage. Our initial re-
sults with LC/MS analysis of Trypan Blue degradation using soybean
peroxidase/H
2
O
2
indicates that the symmetric and asymmetric azo
breakage may both be at work at the same time (Fig. 3). Similar
results have also been reported by Lopez et al. [124].
4. Factors affecting microbial and enzymatic decolorization
The degradation rate and efciency of the enzymatic decolor-
ization of the dye are highly dependent on a number of operational
parameters that govern the degradation of the organic molecule.
This section will briey discuss the signicance of each operational
parameter.
4.1. Effect of oxygen
Dye degradation can occur under anaerobic and aerobic condi-
tions by different microbial organisms. Carbon sources such as glu-
cose, starch, acetate, and ethanol affects the decoloration process
of dyes under anaerobic conditions [125]. Under anaerobic condi-
tions, reductive enzyme activities are generally higher; however,
Symmetric azo-bond breakage Asymmetric azo
-
bond breakage
OH NH
2
SO
3
Na
NH
2
OH
NH
2
HO
3
S
SO
3
Na
HO
CH
3
NH
2
CH
3
H
2
N
Further degradation
Fig. 3. Symmetric and asymmetric breakage of the azo bond in Trypan Blue when degraded using SBP and H
2
O
2
. LC/MS was used to identify the various metabolites produced
upon enzymatic degradation of Trypan Blue (unpublished data). (For interpretation of the references to colour in this gure legend, the reader is referred to the web version of
this article.)
M.A. Rauf, S. Salman Ashraf / Chemical Engineering Journal 209 (2012) 520530 525
a small amount of oxygen is also required for the regeneration of
reducing cofactors (e.g. NADH and NADPH) as well as oxidative en-
zymes which may also be involved in the degradation of azo dyes.
The intermediates formed during azo dye reduction reaction, like
the simple aromatic compounds, are broken down via hydroxyl-
ation and ring-opening in the presence of oxygen [64]. Hence, for
the complete mineralization of the azo molecules, aerobic condi-
tion is better. Thus, for the most effective efuent treatment an
anaerobic process with subsequent aerobic treatment can be used
to decolorize wastewaters containing dyes and improve their bio-
degradability [126]. The main reasons limiting the degradation
rates of dyes in wastewater streams are the lack of oxygen and
the use of high energy cost electron acceptors needed for the min-
eralization processes [127].
4.2. Changing pH
The enzymatic activity depends upon pH and on the acidicba-
sic behavior of the substrate and the amino acid side-chains in the
enzyme active site. For example, the enzyme horseradish peroxi-
dase (HRP) showed a better performance at pH 4.0, wherein 59%
decoloration of Lanaset Blue 2R dye was achieved [96]. The enzy-
matic decolorization of the other two dyes namely Remazol Blue
and Red Cibacron, carried out at different pH values showed that
above pH 6.0, the HRP activity was signicantly inhibited [116].
Similarly, degradation of Turquoise Blue G 133 has been carried
out with the soybean peroxidase (SBP)/H
2
O
2
system and found to
be strongly inuenced by the pH of the solution. The SBP activity
was found to change with pH and was highest at pH 3. At higher
pH values the percentage degradation of the dye decreased and be-
came almost zero at pH 8 [122]. We have also observed a similar
effect of pH on SBP-mediated breakdown of other dyes. Fig. 4
shows the effect of pH on Trypan Blue degradation by SBP/H
2
O
2
system. The results have been explained on the basis that the cat-
alytic cycle of peroxidases involves the formation of two interme-
diates, namely Compound I and Compound II, according to the
following reactions [128]:
Peroxidase H
2
O
2
! Compound I H
2
O 1
Compound I SH ! Compound II S

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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