ROLE OF MICROORGANISMS IN AZO DYE DEGRADATION 8.5. 7 FUNGI

In general, fungi is a saprophytic organism, which can rapidly use different nature of nutritional sources, because it can produce a significant number of intra and extracellular enzymes that are needed to degrade several complex organic pollutants such as dyestuffs, polyaromatic compounds, organic waste and steroids (Gadd, 2001; Humnabadkar et al., 2008). Last few decades, the fungal system have been utilized in the treatment of colored and metallic textile effluents (Ezeronye and Okerentugba, 1999) because they can produce nonspecific enzymes such as lignin peroxidase (LiP), manganese peroxidase (MnP) and laccase (Christian et al., 2005) that can mineralize dyes. Mostly, the fungi such as Phanerochaete chrysosporium, Trametes versicolor, Coriolus versicolor, Bjerkan deraadusta, Aspergillus niger, Geotrichum candidum, Pleurotus ostreatus and Cunninghamella elegans have shown effective dye decolorization (Ventura-Camargo and Marin-Moralas, 2013). In the last few years, azo dye decolorization by fungi has been reported by many researchers (Table 8.1).

TABLE 8.1 Decolorization of Azo Dyes by Fimgi

Fungi Name

Dye

Mechanism

References

Aspergillus niger

Acid blue 29

Adsorption

Fu and Yiraraghavan, 1999

Phanerochaete

chrysosporium

Congo red

Lignin

degradation

Tatarko and Bumpus, 1998

Phanerochaete

chrysosporium

Acid yellow 9, orange II

Peroxidase

Pasti Grigsby et al., 1992

Trametes versicolor

Acid green 27

Laccase

Wong and Yu, 1999

Ganoderma sp.

Orange II

Adsorption

Mou et al., 1991

Geotrichum fuci

Reactive black 5

Adsorption

Polman and Breckenridge, 1996

Cyathus bulleri

Malachite green

Laccase

Vasdev et al., 1995

Trametes versicolor

Rhodamine В

Laccase

Kliammuang and Samthima, 2009

Thelephora sp.

Congo red, Orange G, Amido black 10B

Adsorption

Selvam et al., 2003

Annillaria sp. F022

Reactive Black 5

Laccase

Hadibarata et al., 2012

Cerrena uni color

Acid Red 27

Laccase

Michniewicz et al., 2008

Coprinopsis cineria

Methyl Orange

Laccase

Tian et al., 2014

Ganoderma sp.

Methyl Orange

Laccase

Zhao et al., 2011

Geobacillus catenu- latus MS 5

Congo Red

Laccase

Л erma and Sliirkot, 2014

Lentinus polychrous

Congo Red

Laccase

Suwannawong et al., 2010

Pleurotus os treat us

Remazol Brilliant Blue R

Laccase

Pahnieri et al., 2005

Pleurotus os treat us

Synazol Red HF6BN

Laccase

Ilyas et al., 2012

Py’cnoporus

sanguineus

Trypan Blue

Laccase

Annual' et al., 2009

Thelephora sp.

Orange G

Laccase

Selvam et al., 2003

Trametes versicolor, Ganoderma lucidum, Iipex lacteus

Black Dycem

Laccase

Baccar et al., 2011

Trametes versicolor

Reactive Black 5

Laccase

Bibi and Bhatti, 2012

Providencia rettgeri HSL1

Reactive Blue 172

Laccase,

Azoreductase,

NADH-DCIP

reductase

Harshad Lade et al., 2015

TABLE 8.1 (Continued)

Fungi Name

Dye

Mechanism

References

Aspergillus flavus

R Navy, Blue M3R,

R Red M8B, R Green HE4B. R Orange M2R.

R RedM5B, Dt Orange, RS. Dt Black ВТ, Dt Blue GLL, and Dt Sky Blue FF

Lignin

peroxidase>

laccase>

manganese

peroxidase>

tyrosinase

Laxmi and Nikam. 2015

In addition to enzymatic biodecolorization, fungi remove dyes from the effluent by adsorption mechanism. Both living and dead fungal biomass adsorb dye from wastewater by physicochemical interactions such as adsorption, deposition, and ion-exchange. However, adsorption of dye by wet fungal biomass is veiy fast (Mou et al., 1991), and adsorbed dye are gradually degraded within a week by fungal cells depending on the type of molecule. It is stated that compared with living cells, dead cells decolorize dye solution by adsorption process effectively because of an increased surface area that is due to cell rupture upon death (Mou et al., 1991). It is advantageous that dead cells may be used or stored for a longer period over living cells that need nutrient supply as well as cultural maintenance. The demerits of bioabsorption are the dye remains unaltered form after- adsorptions and will create secondary pollution.

8.5.2 ALGAE

Algae can decolorize azo dyes with the aid of an induced form of an azo reductase enzyme. It removes the color by three different mechanisms: (i) Assimilation of chronrophores for the synthesis of algal biomass, carbon dioxide, and water, (ii) Transformation of colored to non-colored molecules, and (iii) Adsorption mechanism. Some species of algae such as CliJoreUa and OscilJotoria have the capability to reduce azo dye into corresponding aromatic amines that subsequently metabolize to simpler compounds or carbon dioxide (Acuner and Dilek, 2004). It has been found that ChJorella pyrenoidosa, Chlorella vulgaris, and OscilJateria tenuis decomposed more than 30 azo dyes into simpler aromatic amines (Yan and Pan, 2004). In the last few years, azo dye decolorization by algae has been well documented (Table 8.2).

TABLE 8.2 Algae in Azo Dyes Decolorization

Algae

Dye

References

Phormidium valderianum

Acid red 119, Direct black 115

Vislial et al., 2001

Spirogyra rhizopus

Acid red 247

Ozer et al., 2006

Cosmarium sp.

Triphenylmethane dye, Malachite green

Daneshvar et al., 2007

Chlorella vulgaris

G-Red

El-Sheekli et al.. 2009

Nostoc lincki

Methyl red

El-Sheekli et al.. 2009

OsciUatoria formosa

Amido black dye

Mubarak Ali et al., 2011

Enteromorpha sp.

Basic Red 46

Khataee et al., 2013

Nostoc muscorum

RGB-Red

Surbhi et al., 2015

Haematococcus sp.

Congo red

Mahalakshmi et al., 2015

Spirogyra sp., Cladophora sp.

Reactive Blue

Waqas et al., 2015

8.5.3 ACTINOMYCETES

Actinomycetes, especially Streptomyces, can degrade lignin and azo dyes by producing extracellular enzymes laccases and peroxidases. Halotol- erant laccase enzyme produced from S. ipomoea in the presence of a redox mediator could detoxify 90% of the azo dye Orange II (Molina-Guijarro et al., 2009). A peroxidase enzyme has been identified from S. chromo- fuscu, which has the ability to degrade sulfonated dyes (Goszczynski et al., 1994). Combined actions of different enzymes such as lignin peroxidase, NADH-dichloroindophenol oxidoreductase (DCIP), and Methylenetetra- hydrofolate reductases (MR) from S. krainskii degraded reactive blue 59 completely within 24 horns (Mane et al., 2008). Laccase from S. psatn- moticus showed extensive decolorization of remazol brilliant blue R and to a less significant range of methyl orange, Bismarck brown, and acid orange (Niladevi and Prema, 2008) degradation. Table 8.3 shows a few important azo dyes degrading actinomycetes and their substrates.

8.5.4 BACTERIA

Many researchers have found the role of various groups of bacteria in decolorization and degradation of azo dyes. Since bacteriological decolorization is, (i) inexpensive, (ii) higher degree of biodegradation and mineralization, (iii) applicable to a wide variety of azo dyes, (iv)

Strains

Type of Enzyme

Dyes Degraded

References

Streptomyces chromofuscus

Peroxidase

3,5-dimethyl-4-hydroxy-aobenzene- 4'-sulfonic acid (I), 3-methoxy-4- hydroxyazobenzene-4 ’-sulfonamide (II)

Goszczvnski et al., 1994

Streptomyces psammoticus

Laccase

Remazol brilliant blueR

Niladevi and Prema, 2008

Streptomyces sbmnskii

Ligninperoxidase, NADH-DCIP reductase, MR- reductases

Reactive blue 59

Mane et al., 2008

Sti eptomyces ipomoea

Laccase oxidoreductase

Orange II

Molina-Guijarro et al., 2009

Nocardia sp. KN5

-

Congo red

Bhoodevi et al., 2015

Saccharothrix aerocolonigenes

-

Reactive Red 1, Reactive Orange (RY107) and Reactive black 5

Rizwana and Uma, 2015

Streptomyces spp.

-

Azo blue and azo orange

Jai et al., 2015

Micromonospora sp., Stieptomyces sp., Micropolyspora sp.

-

Ami do black

Mohamed et al., 2016

faster mineralization than fungi, (v) eco-ffiendliness and (vi) less sludge production (Venna and Madamwar, 2003; Rai et al., 2005; Khehra et al., 2006; Saratale et al., 2009c). Several members of the genus including Micrococcus, Aeromonas, Escherichia, Acinetobacter, Pseudomonas, Enterococcus, Klebsiella, Desulfovibrio, Rhodopseudomonas, Rhizo- bium, Acinetobacter, Alcaligenes, Bacillus, Brevibacterium, Proteus, Microbacterium, Sphingomonas sp., Staphylococcus, and Gracilibacillus are degrading various azo dyes by their unique metabolic process.

Bacteria have the ability to decolorize a broad spectrum of dyes. The bacterial decolorization of azo dyes can be mainly by either aerobic or anaerobic metabolism. However, a wide variety of azo dyes degradation takes place under both anaerobic and aerobic conditions, the preliminary step of bacterial decolorization is the reductive cleavage of -N=N linkage with the help of azoreductase enzyme under anaerobic conditions, which forms colorless potentially toxic aromatic amines (Chang and Kuo, 2000; Vander Zee and Villaverde, 2005). Further, aromatic amines are broken down aerobically or anaerobically (Joshi et al., 2008). It has been reported that mixed bacterial culture can degrade dyes more successfully than pure bacterial strains (Nigam et al., 1996) due to synergistic metabolic activities of the microbial consortia. The pure culture of bacteria such as Proteus mirabilis, Pseudomonas luteola, and Pseudomonas sp. degrade azo dyes under axenic conditions (Chen et al., 1999; Yu et al., 2001; Kalyani et al., 2008). Moreover, decolorization by pure culture method helps to understand the mechanisms of biodegradation in-depth in the course of biochemical and molecular studies; this information may useful to produce modified strains with higher enzyme activities. However, a pure culture of bacteria cannot degrade azo dye completely and also produce a toxic intermediate which requires further decomposition to become non-toxic (Joshi et al., 2008). It has been suggested that a pure culture of bacteria requires a long-term adaptation process for efficient decolorization of azo dyes (Saratale et al., 2011). However, in a mixed bacterial culture system, aromatic amines that are formed by reductive cleavage of the azo bond are further degraded by co-existing organisms. Therefore, the mixed culture system is effective because dye molecules are attacked at a different positions by various bacteria or formed intermediate may be further decomposed by complementary organisms. The reported azo dye decolorizing bacteria are tabulated in Table 8.4.

TABLE 8.4 Decolonization of Azo Dyes by Bacteria

Organism

Dye Degraded

Type of Enzyme

References

Pseudomonas luteola

Red G

Azoreductase

Hu. 1994

Klebsiella pneumoniae

Methyl Red

Reductive

Wong and Yuen, 1996

Rhodopseudomonas palustiis

Reactive Brilliant Red

Reductive

Wong and Yuen, 1996

Sphingomonas sp. BN6

Amaranth

Azoreductase

Kudlich et al„ 1997

Desulfovibrio desulfuhcans

Reactive Orange 96, Reactive Red 120

Reductive

Yoo et al., 2000

Bacillus strain SF

Reactive Black 5, Mordant black 9

Reductive

Maier et al., 2004

Pseudomonas aeruginosa

Navitan fast blue S5R, Amaranth, Orange G

Azoreductase

Nachiyar and Rajkumar, 2005

Staphylococcus aureus

Orange II, Ponceau BS, Ponceau S

Azoreductase

Chen et al., 2005

Bacillus cereus

Indigo caramine, Ruby red, Flame orange

Azoreductase

Pricelius et al., 2007

Gracilibacillus sp.

Acid red В

Azoreductase

Uddin et al., 2007

Bacillus velezensis AB

Congo red

Azoreductase

Bafana et al., 2008

Rhizobium radiobacter

Reactive Red 141

Oxidative and reductive

Telke et al., 2008

Enterococcus faecalis

Methyl red

Azoreductase

Punj and John. 2009

Micrococcus glutamicus

Reactive Green 19A

Oxidative and reductive

Saratale et al., 2009c

Aeromonas hydrophila

Reactive Red 198, Reactive Black 5

Reductive

Hsueh et al., 2009

Escherichia coli

Direct Blue 71

Reductive

Jin et al., 2009

Acinetobacter calcoaceticus

Direct Brown MR

Oxidative and reductive

Ghodake et al., 2009a

Enterococcus gallinarum

Direct Black 38

Reductive

Bafana et al., 2009

Mutant Bacillus sp. ACT2

Congo Red

Reductive

Gopiuath et al.. 2009

Escherichia coli JM109 (pGEX-AZR)

Direct Blue 71

Reductive

Jin et al., 2009

Organism

Dye Degraded

Type of Enzyme

References

Enterococcus gallinaivm

Direct Black 38

Reductive

Bafana et al., 2009

Enterococcus gallinaivm

Direct Black 38

Reductive

Bafaua et al., 2009

Mutant Bacillus sp. ACT2

Congo Red

Reductive

Gopinath et al., 2009

Pseudomonas aeruginosa

Remazol Orange

Reductive

Sarayu and Sandhya, 2010

Pseudomonas aeruginosa

Remazol Orange

Reductive

Sarayu and Sandhya, 2010

Pseudomonas aeruginosa

Remazol Ch ange

Reductive

Sarayu and Sandhya, 2010

Acinetobacter radioresistens

Acid Red

Reductive

Rarnya et al., 2010

Bacillus megaterium

Red 2G

Reductive

Khan. 2011

Bacillus subtilis ORB7106

Methyl Red

Reductive

Leelakriaugsak and Borisut, 2012

Brevibacteiium sp. strain "N-15

RY107

Reductive

Franciscon et al., 2012

Proteus sp.

Congo Red

Reductive

Penmial et al., 2012

Alcaligenes sp. AA09

Reactive Red BL

Reductive

Paudey and Dubey. 2012

Brevibacteiium sp. str ain "N-15

Reactive Yellow 107

Tyrosinase activity

Elisangela Franciscon et al., 2012

Bacillus lentus BI377

Reactive Red 141

Reductive

Oturkar et al., 2013

Pseudomonas spp.

Reactive Violet 5

Laccase

Shall. 2014

Pseudomonas stutzeri

Disperse Yellow (D4). Disperse Blue (R16), Reactive Red, Synozol (R4)

-

Amr Fouda et al., 2016

Microbactehum sp. B12 Mutant

Reactive Blue 160

Reductive

Chetana et al., 2016

Pseudomonas entomopliila

Reactive Black 5

Azoreductase

Sana and Abdul, 2016

8.5.5 AEROBIC BACTERIAL DECOLORIZATION

Bacteria are capable of decolorizing azo dyes in the presence of oxygen by a reductive mechanism with the aid of aerobic azoreductase enzyme. In general, azo reductases require NADH/NADPH for their redox reaction. Perhaps azo dyes are resisting to bacterial decolorization under aerobic conditions, because aerobic respiration may take over to utilize NADH, thus inhibiting the electron transfer from NADH to azo bonds. Thus organisms with specific azo dye reducing enzymes can only degrade azo dye. Bacteria such as Bacillus, Rhodobacter spheroids, Enterococcus, ShigellaJlexneri, E. coli, Xenophilus azovorans, Pseudomonas aeruginosa, and Pigmentiphaga kullae (Bafana and Chakrabarti, 2008) decolorize azo dyes aerobically with the help of aerobic azoreductase enzyme which reduces the azo group to aromatic amines (Bafana et al., 2009). For example, azoreductase from Staphylococcus aureus cleaved methyl red into 2-aminobenoic acid (Carcinogenic) andN,N-dimethyl-p-phenylenediamine (Figure 8.7) (Chen et al., 2005).

Some bacteria utilize azo dyes for its carbon and energy requirements. They can slowly degr ade the complex dyestuffs and to minerals in aerobic conditions without production of carcinogenic aromatic amines. Example, Xenophilus azovorans KF 46 and Pigmentiphaga kullae K24 can grow on media with azo compounds carboxy orange 1 and carboxy orange II, as the sole carbon source (McMullan et al., 2001), but Sphingomonas sp. degrades azo dye by reductases enzymes for its carbon and energy requirements (Coughlin et al., 1999). Normally, these bacteria reduce -N=N- bonds and utilize amines as carbon and energy source for their growth through aerobic metabolism.

Direct enzymatic method of azo dye degradation

FIGURE 8.7 Direct enzymatic method of azo dye degradation.

8.5.6 ANAEROBIC BACTERIAL DECOLORIZA TION

One such approach used to degrade the dyes by the anaerobic method is electron acceleration, in which the transfer of an electron to the dye increases the degradation efficiency in an anaerobic environment. Different types of bacteria such as Eubacterium, Proteus, Bacteroids, Streptococcus, and Clostridium could reduce azo compounds anaerobically (Stolz, 2001). In anaerobic condition, the azo bond is cleaved by nonspecific reduction with the aid of reduced flavin (electron earner). Cytoplasmic flavin reductases assist the transfer of an electron to the azo dye through reduced electron earners hi an anaerobic environment. But, azo dye substituted with a sulfonate group cannot be reduced by cytoplasmic enzyme because the permeability of the plasma membrane is low for sulfonated dyes (Wuhrmann et al., 1980). They can be reduced extracellularly with the assistance of redox mediator that transports electrons between cell and the dye. For example, Sphingomouas xeuophaga produces redox mediator itself during reduction of azo dye (Keck et al., 2002). Some anaerobic bacteria use their metabolic end products such as Fe2+ and H,S as a redox mediator to reduce azo dyes (Kim et al., 2007). The redox mediators (RMs) such as riboflavin and quinones are increasing the efficiency of degradation. It exhibits intermediate reduction potentials and simplifies the electron transfer from the substrate (donor) to the dye (acceptor); thereby speed up the decolorization process. RMs are veiy effective in azo dye reduction process because of the unstable nature of the azo bond, which can readily receive electron from riboflavin and quinines. Redox mediator dependent anaerobic process is accomplished in two steps (Rau et al., 2002), such as (i) RM reduction by the reducing equivalents produced by substrate metabolism, and (ii) Azo dye reduction by the reduced form of RM (RMreduc). This type of anaerobic process has been widely used for dye removal and reduction of COD in textile effluents. It has more advantageous, because of less sludge production, minimum energy requirements, and used to produce energy (methane-biofuel) (Diego et al., 2014).

However, anaerobic bacteria efficiently decolorize azo dye by nonspecific azo reductase enzyme activity; the formation of aromatic amines would become a problem. For example, metabolism of a dye direct black 38 by human intestinal microflora was carried out in a semi-continuous culture system that mimics the lumen of human large intestine. After 7 days of incubation, compounds such as benzidine, 4-aminobiphenyl, mono acetylben- zidine, and acetylaminobiphenyl have produced as the end products which were identified by GC-MS analysis (Manning et al., 1985). The aromatic amines generated by the reduction of the azo bond are not degraded further under anaerobic conditions. But, they are mineralized under aerobic conditions by nonspecific enzymes via hydroxylation and ring-opening (Feigel et al., 1993). It is proposed that the combined action of anaerobic and aerobic bacteria remove recalcitrant azo dye from the environment. This has been proved by the decolorization of reactive azo dyes such as remazol brilliant violet 5R, remazol black B, and remazol brilliant orange 3R was occurred effectively by mixed culture of bacteria in an anaerobic-aerobic treatment process (Supaka et al., 2004; Popli and Patel, 2015).

 
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