Microbial Bioremediation of Chromium in Tannery Effluent: A …idosi.org/ijmr/ijmr4(3)13/12.pdf · 2019-08-02 · metal removal processes because of their low cost and soils surrounding

International Journal of Microbiological Research 4 (3): 305-320, 2013ISSN 2079-2093© IDOSI Publications, 2013DOI: 10.5829/idosi.ijmr.2013.4.3.81228

Corresponding Author: P. Saranraj, Department of Microbiology, Annamalai University, Annamalai Nagar,Chidambaram - 608 002, Tamil Nadu, India.

305

Microbial Bioremediation of Chromium in Tannery Effluent: A Review

P. Saranraj and D. Sujitha

Department of Microbiology, Annamalai University, Annamalai Nagar,Chidambaram- 608 002, Tamil Nadu, India

Abstract: Chromium, a priority pollutant is well known for its mutagenicity, carcinogenicity and teratogenicityin humans, experimental animals and plants. Extensive use of chromium in industries such as leather tanning,stainless-steel production, electroplating and wood preservatives have resulted in chromium contaminated soiland ground water at production sites which pose a serious threat to human health. Bioadsorption is the simpleuptake of the constituents of the effluent by the organisms without any usage in its metabolism. Biodegradationmeans the breaking down of the constituents of the effluent into different fragments which will be either takenas a substrate by the organisms or simply remain in the system i.e., metabolism of the constituents by theorganisms or simple cleavage by them into simpler fragments by the release of enzymes. Biodegradation is oneof the biological processes facilitating the chemical changes of pollutants by microorganisms present in thepolluted environment. Microorganisms are involved in the removal of toxic wastes, either in the environmentor in controlled treatment systems.

Key words: Tannery Effluent Chromium Bioremediation Bacteria and Fungi

INTRODUCTION Tanning industries worldwide generate approximately

Elimination of heavy metals from industrial With inadequate regulatory guidelines, wastes werewastewater is important for preserving the quality largely disposed on land and water odies throughout theof aquatic systems, streams and ground waters. world. Studies showed that tannery waste disposals haveContaminated waters are generally cleaned by led to severe contamination of productive agriculturalprecipitation of a metallic oxyhydroxide sludge or by ion land in Bangladesh, [3] in India [4] and in Australia [5].exchange with synthetic resins. Various types of Chromium is frequently one of the most toxicnonliving biomass, bacteria, filamentous fungi, algae elements present in tannery waste. High chromiumand higher plants can be profitably used in alternative concentrations ranging from 1 to 50g/kg were reported inmetal removal processes because of their low cost and soils surrounding tannery waste disposal sites in India,the high ion exchange capacity of cell walls. The with hexavalent chromium was present in groundwater athexavalent chromium compounds are comparatively these sites [6].more toxic than trivalent chromium compounds due to Chromium level was found to increase with increasetheir higher solubility in water, rapid permeability in the concentration of the tannery effluent. Chromiumthrough biological membranes and subsequent interaction associated pollution is of increasing concern nowadays.with intracellular proteins and nucleic acids [1]. Conventional methods for treatment of toxic chromateAccordingly, chromium and its compounds are placed include chemical reduction followed by precipitation, ionon the priority list of toxic chemicals by US EPA [2]. A exchange and adsorption on activated coal, alum, kaolinitemaximum acceptable concentration of 0.05 mg/l for and ash which require large amounts of chemicals andhexavalent chromium in drinking water has been energy and therefore are unsuitable [7]. Several reportsestablished on basis of health considerations. However, have indicated biological reduction of hexavalentits high toxicity, mutagenicity and carcinogenicity chromium by microorganisms, both aerobes andrenders it hazardous even at very low concentration. anaerobes. Biological reduction of hexavalent chromium

40 million waste containing chromium (Cr) every year.

Intl. J. Microbiol. Res., 4 (3): 305-320, 2013

306

usually occurs at a neutral pH range and generates an Biosorptive capacity of different biosorbentsinsignificant quantity of chemical sludge as well as offers including dried mycelium of some species of fungi,potential cost – effective remediation strategy. A number baggase, rice rusk and fermented baggase by selectedof chromium resistant microorganisms have been reported fungal species or natural micro flora was examined toto detoxify hexavalent chromium, which include remove cyanide from industrial effluent. The biomass ofPseudomonas sp., Microbacterium sp., Desulfovibrio sp., Rhizopus sexualis and the fermented baggase byEnterobacter sp., Escherichia coli, Shewanella alga and Rhizopus sexualis or Aspergillus terreus showed higherBacillus sp., where the method of detoxification is sorption capacity than activated charcoal. The biomass ofperiplasmic biosorption, intracellular bioaccumulation and Rhizopus sexualis and Mortierella ramanniana exhibitedbiotransformation through direct enzymatic reaction or higher CN sorptive capacity than ascomycetes e.g.indirectly with metabolites [8]. Some of the fungi that Aspergillus terreus and Penicillium capsulatum. Maximalremove chromium from tannery wastes are Aspergillus, removal of Ni from electroplating industries occurred byNostoc and Cyanobacteria etc. 2.5 gm of biomass of Saccharomyces cerevisiae with in

Biosorption by bacteria and fungi as an alternative 5 hrs. Ni uptake capacity from aqueous solution was alsotreatment option for wastewater containing heavy studied in filamentous fungi such as Rhizopus sp.,metal has been reviewed by Kapoor and Viraghavan [9]. Penicillium sp. and Aspergillus sp. The metal uptake wasAny fungi can tolerate high concentration of potentially highest by Rhizopus sp. [12].toxic metals and with other microbes; this maybe correlated with decreased intracellular uptake or Chromium: Chromium (Cr) is a transition metal present inimpermeability. A close relation between toxicity and group VI-B of the periodic table. Although it can exist inintracellular uptake has been shown for Cu , Cd , nine valence states, from -2 to +6 [13] only trivalent2+ 2+

Co and Zn in yeast Saccharomyces cerevisiae. chromium Cr (III) and hexavalent chromium Cr (VI) are2+ 2+

Waste mycelia from industrial fermentation plants ecologically important because these are the most stable(Aspergillus niger and Penicillium chrysogenum) were oxidation states in the natural environment. Chromium isused to as a biosorbent for removal of Zn ions from a chemical element which has the symbol Cr and atomicaqueous environments, both batch wise as well as in number 24. It is a steely gray, lustrous, hard metalcolumn mode. Under optimized conditions Aspergillus that takes a high polish and has a high melting point.niger and C. paspali were found superior to Penicillium It is odorless, tasteless and malleable metal. The name ofchrysogenum. Removal of lead ions from aqueous the element is derived from the Greek word ‘chroma’solution by non-living biomass of Penicillium meaning color, because many of its compounds arechrysogenum was studied and observed that Pb was intensely colored. Chromium is an important metal due to2+

strongly affected by the pH in the range of 4-5. its high corrosion, resistance and hardness. It is usedUptake of Pb was 116 mg/g dry biomass, which was extensively in manufacturing of stainless steel. Chromium2+

higher than that of activated carbon and some other contamination of the environment is of concern becausemicroorganisms [10]. of the mobility and toxicity of Cr (VI).

Chromium biosorption by non-living biomass of Trivalent and hexavalent chromium differ widely inChlorella vulgaris, Clodophora crispate, Zoogloea physicochemical properties and biological reactivity.ramigera, Rhizopus arrhizus and Saccharomyces While Cr (VI) species and dichromate’s are extremelycerevisiae was studied and observed that optimum water-soluble and mobile in the environment, Cr (III)initial pH (1.0-2.0) of the metal ion solution affects the species are much less soluble and comparativelymetal uptake capacity of the biomass for all the immobile. Moreover, Cr (VI) is recognized to be highlymicroorganisms. Maximum adsorption rates of metal ions toxic, carcinogenic, mutagenic and teratogenic forto microbial biomass were obtained at temperature in the mammals including humans, whereas Cr (III) is anrange of 25-35°C. The adsorption rates increased with essential trace element necessary for glucose, lipid andincreasing the metal concentration of Chlorella vulgaris, amino-acid metabolism as well as a popular dietaryClodophora crispate, Zoogloea ramigera, Rhizopus supplement [14].arrhizus and Saccharomyces cerevisiae up to 200, 200, 75, Studies have revealed that Cr (VI) is approximately125 and 100 mg/l respectively [11]. Dead cells of 100 times more toxic and 1000 times more mutagenic thanSaccharomyces cerevisiae removed 40% more uranium or Cr (III). Although, trivalent chromium (Cr (III) or Cr ) iszinc than the corresponding live cultures. required in trace amounts for sugar and lipid metabolism

3+


307

in humans, however its deficiency causes disease. engaged in the chrome tanning process. The tanneryHexavalent chromium (Cr (VI) or Cr ) is a toxin and a waste primarily consists of chromium and protein.6+

carcinogen metal pollutant that tremendously affects the Long term disposal of tannery wastes has resulted inenvironment at abandoned chromium production sites. extensive contamination of agricultural land and waterHence its environmental cleanup is highly essential. sources in many parts of the India. There are more thanCr (VI) is highly toxic, carcinogenic and mutagenic. 2500 tanneries in the country and nearly 80% of theIt causes severe diarrhea, ulcers, eye and skin tanneries are engaged in the chrome tanning process.irritations, kidney dysfunction and probably lung In the process of tanning, chromium salts are used tocarcinoma. It is also associated with decrease in plant convert hide to leather and the waste water generated isgrowth and changes in plant morphology. Chromium is discharged into the environment which containspresent in the environment as either Chromium (III) or chromium salts in the excess of the maximum permissibleChromium (VI). Chromate [Cr (VI)] is highly soluble in limits. Tannery industry is one of the major industries inbacteria, it is transported rapidly across the cell India. In tannery effluent, Cr (VI) is present as eithermembranes via the sulfate pathway and reduced in the dichromate (Cr O ) in acidic environment or as chromatecytoplasm to trivalent (III).Trivalent chromium, which (CrO ) in alkaline environments [18].interacts with proteins and nucleic acids, however, is far Heavy metals exhibit toxic effects on soil biota andless soluble than hexavalent chromium and does not pass they can affect key microbial process and decreasethrough biological membranes [15]. the number and activity of soil microorganisms [19].

Bacterial reduction has been found in metallic Metal contaminants are commonly found in soils,minerals such as manganese, metal iron, mercury, selenite sediments and water. Metals pollutants can be producedand tellurite. Some microbial transformations enable the through industrial processes such as mining, refining andbacteria to increase their tolerance toward toxic heavy electroplating. At low concentrations, metals can servemetals. Chromium, a transition metal, is one of the major as important components in life processes, oftensources of environmental pollution. It is discharged into serving important functions in enzyme productivity.the environment through the disposal of wastes from Metals can become toxic to many species. Fortunately,industries like leather tanning, metallurgical and metal microorganisms can affect the reactivity and mobility offinishing, textiles and ceramics, pigment and wood metals. Microorganisms that affect the reactivity andpreservatives, photographic sensitizer manufacturing mobility of metals can be used to detoxify some metalsetc. [16]. and prevent further metals contamination. Thus far,

In the environment chromium occurs mainly in tolerance mechanisms for metals such as copper, zinc,trivalent and hexavalent forms. The hexavalent chromium arsenic, chromium, cadmium and nickel have been(Cr ) compounds are comparatively much more toxic than identified and described in detail.6+

those of trivalent chromium (Cr ) [17]. There is only When looking at the microbial communities of3+

limited investigation for mining effluent treatment metal-contaminated environments, it has been foundparticularly Cr (VI) contaminants using microbial strains. that among the bacteria present, there is more potential forTill date there is no literature cited on any molecularly unique forms of respiration. Also, since the oxidationidentified and sequenced microbial species for chromium state of a metal ion may determine its solubility, manyresistant and removal from Sukinda region. Thus our scientists have been trying to use microbes that are ablepresent study used potential indigenous microbial strains to oxidize or reduce heavy metals in order to remediatefor treatment of industrial and mining effluent that may be metal-contaminated sites. Another implication of heavysuitable for biological treatment of Cr-contaminated metal tolerance in the environment is that it maywaste of Sukinda mines. This study a remediation route contribute to the maintenance of antibiotic resistancefor detoxification of Cr (VI) using an indigenous genes by increasing the selective pressure of themicroorganism. environment. Calomiris et al. [20] studied bacteria isolated

from drinking water and found that a high percent ofBioremediation of Tannery Effluent by Using bacteria that are tolerant to metals are also antibioticMicroorganisms: Tannery effluents are a major source of resistant.aquatic pollution in India with chemical oxygen demand Effluents from tannery, electroplating and electronic(COD), biological oxygen demand (BOD) and hexavalent industries contain chromium which is highly toxic.chromium. Nearly 80% of the tanneries in India are This paper reported isolation of chromium tolerant

2 72-

4-


308

microorganisms from solid waste as well as liquid effluent concentration of 0.05 mg/l for hexavalent chromium inof an electroplating industry. Nine isolates were obtained drinking water has been established on basis of healththat can tolerate chromium concentration up to 700 mg/L. considerations.They reached their stationary phase within 8-12 hours An Arthrobacter sp. and a Bacillus sp., isolated fromand can biosorbed 95% of initial 200 mg/L concentration a long-term tannery waste contaminated soil, wereof chromium within 4-10 hours. Fourier Transform Infra examined for their tolerance to hexavalent chromiumRed analysis of the biomass exposed to chromium [Cr(VI)] and their ability to reduce Cr (VI) to Cr (III), aindicated that amino and carboxylate groups in the detoxification process in cell suspensions and cellbiomass are involved in biosorption process. 16S RNA extracts. Both bacteria tolerated Cr (VI) at 100 mg/ml on aresults of two most active organisms indicate that they are minimal salts agar medium supplemented with 0.5%Bacillus marisflavi and Arthrobacter sp. and they show glucose, but only Arthrobacter could grow in liquid98% and 96% homology similarity in the phylogenetic medium at this concentration. Arthrobacter sp. couldtree, respectively [21]. reduce Cr (VI) upto 50 µg/ml, while Bacillus sp. was not

Bento et al. [22] observed that maximum chromium able to reduce Cr (VI) beyond 20 µg/ml. Arthrobacterreduction occur at the optimum pH (7-9) and temperature sp. was distinctly superior to the Bacillus sp. in terms of(30°C) of growth by Bacillus sp. Ravibabu [23] studied their Cr (VI)-reducing ability and resistance to Cr (VI).the remediation of effluents using physical methods like Assays with permeabilized (treated with toluene oractivated charcoal, pH ranges and time periods and Triton X 100) cells and crude extracts demonstrated thatbiological methods using the aquatic weed hyacinth as a the Cr (VI) reduction was mainly associated with thebiological pollutant removal. soluble protein fraction of the cell. Arthrobacter sp. has

The pollution of the environment with toxic heavy a great potential for bioremediation of Cr (VI) containingmetals is spreading throughout the world along with waste [27].industrial progress. Microorganisms and microbial Cr (VI) (chromate) is a widespread environmentalproducts can be highly efficient bioaccumulations of contaminant. Bacterial chromate reductases can convertsoluble and particulate forms of metals especially dilute soluble and toxic chromate to the insoluble and less toxicexternal solutions. Microbes related technologies may Cr (III). Bioremediation can therefore be effective inprovide an alternative or addition to conventional removing chromate from the environment, especially if themethod of metal removal or metal recovery. The present bacterial propensity for such removal is enhanced bystudy deals with isolation, identification and genetic and biochemical engineering. Gram positive,characterization of heavy metal resistant bacteria was chromium (Cr)-resistant bacterial strain (ATCC 700729)isolated from tannery effluent collected in and around was isolated from effluent of tanneries. It was grown inChennai, South India. Initially, a total of 50 isolates were media containing potassium dichromate concentration upscreened from tannery effluent [24]. to 80 mg ml of the medium. The dichromate reducing

Chromium, a transition metal, is one of the major capability of the bacterium was checked by estimating thesources of environmental pollution. It is discharged into amount of Cr (VI) in the medium before and afterthe environment through the disposal of wastes from introduction of bacterial culture. The influence of factorsindustries like leather tanning, metallurgical and metal like pH of the medium, concentration of Cr and the amountfinishing, textiles and ceramics, pigment and wood of the inoculum was studied to determine the ability ofpreservatives, photographic sensitizer manufacturing etc. the bacterium to reduce Cr (VI) in the medium underIn the environment chromium occurs mainly in trivalent various conditions. In a medium containing dichromateand hexavalent forms. The hexavalent chromium (Cr ) 20 mg ml more than 87% reduction of dichromate ions6+

compounds are comparatively much more toxic than those was achieved within 72 hrs. The feasibility of the use ofof trivalent chromium (Cr ). The hexavalent chromium this bacterial strain for detoxification of dichromate in the3+

compounds are comparatively more toxic than trivalent industrial wastewater has been assessed. The isolatedchromium compounds due to their higher solubility in strain can be exploited for specific environmental clean-upwater, rapid permeability through biological membranes operations [28].and subsequent interaction with intracellular proteins Hexavalent chromium [Cr (VI)], is a toxic,and nucleic acids [25]. Accordingly, chromium and its water-soluble contaminant present in many soils andcompounds are placed on the priority list of toxic industrial effluents. Bacteria from various soils werechemicals by US EPA [26]. A maximum acceptable examined for Cr (VI) resistance and reducing potential.

1

1


309

Microbes selected from both Cr (VI)-contaminated and environment was discussed [35]. Turick et al. [36]non-contaminated soils and sediments were capable of investigated several bacteria from various soils forcatalyzing the reduction of Cr (VI) to Cr(III) a less hexavalent chromium resistance and reducing potential.toxic, less water-soluble form of Cr, demonstrating the Microbes selected from both hexavalent chromium-utility of using a selection strategy for indigenous contaminated and non-contaminated soils and sedimentsCr(VI)-reducing bacteria in a bioprocess. As a result, were capable of catalyzing the reduction of hexavalentindigenous Cr (VI)-reducing microbes from contaminated chromium to trivalent chromium a less toxic, lesssites should provide the means for developing a water-soluble form of chromium, demonstrating the utilitybioprocess to reduce Cr (VI) to Cr (III) in non-sterile of using a selection strategy for indigenous hexavalenteffluents such as those from soil washes. This approach chromium reducing bacteria in a bioprocess. As a result,also avoids the contamination problems associated indigenous hexavalent chromium reducing microbes fromwith pure cultures of allochthonous microorganisms. contaminated sites should provide the means forIn addition the apparent ubiquity of Cr (VI)-reducing developing a bioprocess to reduce hexavalent chromiumbacteria in soil and sediments indicated the potential for to trivalent chromium in non-sterile effluents such asin situ bioremediation of Cr (VI)-contaminated soils and those from soil washes.ground water [29]. The occurrence of metal tolerant and antibiotic

Viamajala et al. [30] studied the pollution effects of resistant organisms was investigated in tannery effluent.tannery water and reported that the salts of the Seventy-seven isolates comprising heterotrophs andtannery effluent percolates through the soil causing coliforms which were tolerant to chromate level of >50µg/lsevere salinity to the land. Srinath et al. [31] found were selected for detailed study. The majority of theincreased water soluble potassium, sulphur, iron, coliforms were resistant to higher levels of chromateammonium acetate, extractable iron and soil sulphur as (200 µg/ml) whereas around 3% of the heterotrophs werewell as traces of chromium in soils irrigated with tannery resistant to Cr at a level of >150 µg/l. All chromateeffluent. Sultan and Hasnain [32] observed a reduction in tolerant heterotrophs were also tolerant to Cu (100%)the micronutrient status with increasing concentrations whereas only 58.53% coliforms were tolerant to Cu .of tannery effluent in soil (incubated for six months). Except in the case of Cd a higher number of heterotrophsThe chromium level was also found to increase with were found tolerant to other heavy metals tested. Bothincrease in the concentration of the tannery effluent. groups of isolates were found sensitive to mercury.Rajamani et al. [33] showed that chromates are absorbed Resistance to cephaloridine was more abundantin soils and low pH favoured their reduction in soils. (P<0.001) in coliforms as compared to heterotrophs.

Megharaj et al. [34] isolated chromium resistant On the other hand a significantly higher number (P<0.01)bacterial strain Bacillus cereus S-6 from effluents of of heterotrophs showed resistance to streptomycin andtannery which was used for the reduction of toxic carbencillin. All coliforms were sensitive tohexavalent chromium into less toxic trivalent chromium. chloramphenicol. Around 80% and 31.70% of coliformsAt an initial hexavalent chromium concentration of and heterotrophs exhibited a relationship to the100 µg/ml, the cytosol and membrane preparation of the combination of metals and antibiotics. Both heterotrophsstrain were able to reduce almost 67 and 43% of and coliforms tolerant to Hg were also resistant tohexavalent chromium within 24 hrs incubation period polymixin-B [37].while the heat killed cytosol and membrane preparation Reduction of hexavalent chromium (chromate) toreduced 24 and 18% within the same time period. less-toxic trivalent chromium was studied by using cellThey reported that tannery effluent may change the suspensions and cell-free supernatant fluids fromcharacteristics of soil and interfere with the intake of water Pseudomonas putida PRS2000. Chromate reductaseby plants. The presence of sulphide and chromium in activity was associated with soluble protein and not withtannery effluent affects plant life and soil productivity. the membrane fraction. The crude enzyme activity was

Many genera of microbes like Bacillus, Enterobacter, heat labile and showed a Km of 40, µM CrO NeitherEscherichia, Pseudomonas and also some yeasts sulfate nor nitrate affected chromate reduction eitherand fungi help in bioremediation of metals and in vitro or with intact cells [38].chromium-contaminated soil and water by bioabsorption Bacterial strains (CrT-11, CrT-12, Brevibacterium sp.and bioaccumulation of chromium. The potential of CrT-13, CrT-14) were isolated from the effluents ofbioremediation of metal toxicity and its impact on the tanneries. All strains could resist very high concentration

6+

2+

2+

2+

2+

42-.


310

of K CrO that is upto 40 mg ml on nutrient agar become barren lands. Guha et al. [52] pointed out the2 41

and 25 mg ml in nutrient broth. They have wide pH characteristics of tannery effluent led into the land and1

(5 to 9) and temperature (24 to 42°C) growth range. said that the discharged effluents create severe landThey exhibited multiple metals (Ni, Zn, Mn, Cu, Co and pollution. Jonnalagadda et al. [53] studied the pollutionPb) and antibiotics (streptomycin, ampicillin, tetracycline, effects of tannery water and reported that the salts of thekanamycin and chloramphenicol) resistances. All the tannery effluent percolates through the soil causingstrains were able to reduce Cr (VI) in to Cr (III) aerobically. severe salinity to the land. Komori et al. [54] assessedBrevibacterium sp. CrT-13 accumulated and reduced more that effluents containing toxic chemicals have seeped intoCr (VI) at all the concentrations applied in comparison to the arable land and agriculture has declined because ofthe other strains. These bacterial strains also took up and the effects of tannery effluent. With the declined with inreduced Cr (VI) present in industrial effluents and their productivity, the land value has also decreased. Lofrothreduction potential was not significantly affected in the and Ames [55] found increased water soluble potassium,presence of different metallic salts [39]. sulphur, iron, ammonium acetate, extractable iron and soil

Several reports have indicated biological reduction of sulphur as well as traces of chromium in soils irrigatedhexavalent chromium by microorganisms, both aerobes with tannery effluent. Lovley and Phillips [56] showedand anaerobes. Biological reduction of hexavalent that the experimental and epidemiological evidence existschromium usually occurs at a neutral pH range and for the carcinogenicity of some chromium compounds.generates an insignificant quantity of chemical sludge as Therefore chromium has been designated as a prioritywell as offers potential cost – effective remediation pollutant by US EPA.strategy [40]. Subsequent studies have shown that the Faisal and Hasnain [57] checked the multiple heavycapacity for hexavalent chromium reduction is widespread metals (Ni, Zn, Mn, Cu, Co, Pb) and antibiotic resistancesand is reported in organisms such as Bacillus cereus, of Brevibacterium isolated from tannery effluents.Bacillus subtilis, Pseudomonas aeruginosa, Thacker and Parikh [58] identified that the Brucella sp.Achromobacter, Eurydice, Micrococcus roseus and exhibit multiple heavy metals (Ni, Zn, Hg, Co, Pb)Escherichia coli [41] as well as Pseudomonas ambigua tolerance and resistance to various antibiotics.[42], Pseudomonas fluorescens [43], Enterobacter Middleton et al. [59] identified that Ochrobactrum triticicloacae [44], Streptomyces sp. [45], Pseudomonas putida is resistant to chromium, nickel, cobalt, cadmium and zinc[46], D. desulfuricans and D. vulgaris [47] and and able to grow in the presence of NaCl within the pHPseudomonas liquefaciens [48]. range of 4 -10.

Effect of Heavy Metals on the Growth of Bacteria: status with increasing concentrations of tannery effluentAs chromium metal ion is present abundantly in the in soil (incubated for six months). The chromium level wastannery effluents, the review in the present investigation also found to increase with increase in the concentrationfocuses primarily on effect of chromium on the growth of of the tannery effluent. Park et al. [61] showed thatbacteria. Germain and Patterson [49] inferred that chromates are absorbed in soils and low pH favoured theirwastewaters containing hexavalent chromium (chromate) reduction in soils. Pedersen [62] reported that tanneryare generated by many industries including the metal effluent may change the characteristics of soil andfinishing industry, leather tanning, petroleum refining, interfere with the intake of water by plants. The presencetextile manufacturing and pulp production. The chromium of sulphide and chromium in tannery effluent affects plantpresent in industrial wastes is primarily in the hexavalent life and soil productivity.form as chromate and dichromate. Petrilli and DeFlora [50]found that the hexavalent chromium is highly soluble in Chromium Adsorption by Bacteria: Srinath et al. [63]water while the reduced form of chromium, trivalent studied that the Bacillus circulans and Bacilluschromium, forms less soluble chromium hydroxides under megaterium are able to bioaccumulate 34.5 and 32.0 mgnon-acidic conditions. Hexavalent chromium is more toxic chromium/g dry weight, respectively and brought thethan trivalent chromium and has been shown to be residual concentration of hexavalent chromium to themutagenic in a number of bacterial systems. permissible limit in 24 hrs when the initial concentration

Flores and Perez [51] reported that about 800 acres of was 50 mg hexavalent chromium/L. He stated thatagricultural land in Dindigul have been seriously biosorption of hexavalent chromium was shown bypolluted by tannery effluents. All the fertile lands have Bacillus megaterium and another strain, Bacillus

Obbard [60] observed a reduction in the micronutrient


311

coagulans. Living and dead cells of Bacillus coagulans Rao et al. [69] investigated that the adsorption ofbiosorbed 23.8 and 39.9 mg chromium/g dry weight,respectively, whereas, 15.7 and 30.7 mg chromium/g dryweight was biosorbed by living and dead cells ofBacillus megaterium, respectively.

Arvindhan and Madhan [64] assessed that thereduction of hexavalent chromium by intact cells and acell-free extract of an actinomycete, Arthrobactercrystallopoietes isolated from soil contaminated withdichromate. Asatiani et al. [65] found that theArthrobacter sp. could reduce hexavalent chromium upto50 mg/ml, while Bacillus sp. was not able to reducehexavalent chromium beyond 20 mg/ml. Arthrobactersp. was distinctly superior to the Bacillus sp. in terms oftheir-hexavalent chromium reducing ability and resistanceto hexavalent chromium. Assays with permeabilized(treated with toluene or Triton X 100) cells and crudeextracts demonstrated that the reduction of hexavalentchromium is mainly associated with the soluble proteinfraction of the cell.

Muhammed Faisal and Shahida Hasnain [66]demonstrated that the ability of Brevibacterium cells toaccumulate toxic hexavalent chromium at differentchromate concentrations (100, 500 and 1000 µg/ml) indifferent time intervals (15 min, 2 hours and 4 hours).They showed that the Arthrobacter oxydans does acomplete uptake of hexavalent chromium concentration(35 mg/ml) in about 10 days.

Gonul Donmez and Nur Kocberber [67] isolatedthe microorganisms and their hexavalent chromiumbioaccumulation capacities increased by enrichmentprocedure. At the end of the experiments, the highestspecific chromium uptake was obtained at pH 8 as109.45mgg for 164.4mgl initial hexavalent chromium1 1

concentration in the absence of NaCl. In the highestNaCl concentration the maximum specific chromiumuptake was found at pH 9 (26.2mgg ) in samples with1

lower initial hexavalent chromium concentrations at pH 7(as 87.5mgg ) for high initial hexavalent chromium1

concentrations.Baldi et al. [68] studied the biosorption process for

treatment of electroplating wastewater containinghexavalent chromium. They also explained that to treatchromium wastewaters is through the use of biomaterialsas a low-cost adsorbent for chromium. Variousbiomaterials, such as dead biomass (of microalgae,seaweed, fungi and bacteria), agricultural waste biomass,industrial waste biomass and biomaterial-basedcontaining activated carbons for the removal ofchromium from aqueous solutions or wastewaters in abatch or column reactor system.

hexavalent chromium ions from aqueous solutions oncrude tamarind fruit shell, HCl treated and Oxalic acidtreated shells at room temperatures The influence ofdifferent experimental parameters such as pH, effect ofinitial metal ion concentration and effect of dosage ofadsorbent on biosorption were evaluated.

Chromium Adsorption by Fungi: Chromium and nickelare released into the environment by a large number ofprocesses such as electroplating, leather tanning, woodpreservation, pulp processing, steel manufacturing, etc.and the concentration levels of chromium and nickel in theenvironment widely varies. These two metals are of majorconcern because of their larger usages in developingcountries and their non degradability nature. Hexavalentchromium is highly soluble in water and carcinogenic tohuman. Ni(II) is more toxic and carcinogenic metal whencompared with Ni(IV). Due to their toxic effects on livingsystems stringent limits have been stipulated for thedischarge of chromium and nickel into the environment.According to ISI: Bureau of Indian Standard (BIS) theindustrial effluent permissible discharge level ofCr(VI) and Ni(II) into inland water is 0.1 and 3.0 mgL , respectively. Gupta et al. [70] tested the tolerance1

and accumulation of hexavalent chromium by marineseaweed associated strains of Aspergillus flavus andAspergillus niger. They revealed that both the isolatesaccumulated more than 25% of the chromium supplied.Aspergillus flavus invariably exhibited higheraccumulation potential.

Igwe and Abia [71] found that the chromium wasbioremoved from tannery industries effluent byAspergillus oryzae. Aspergillus oryzae can grow indifferent concentration of chromium 120-1080 mg/L.They observed that maximum biomass growth andchromium removal rate at pH, 3.3, trivalent chromiumconcentration equal to 240 mg/L and inoculum size equalto 0.12% (dry weight) were 0.25 (dry weight ) and 94.2%,respectively. They stated that bacterial strains wereisolated and enriched from the contaminated site ofTamil Nadu Chromates and Chemicals Limited (TCCL)premises, Ranipet, Tamil Nadu, India. It was found thata bacterial concentration of 15+/-1.0 mg/g of soil(wet weight) 50 mg of molasses/g of soil as carbon sourcewere required for the maximum hexavalent chromiumreduction. The bioreactor operated at these conditionscould reduce entire hexavalent chromium (5.6 mg /g ofsoil) in 20 days.


312

Srivastava and Thakur [72] explained the potency of environments. It provides the means for developing aAspergillus niger evaluated in shake flask culture bioprocess to reduce hexavalent chromium to trivalentby absorption of chromium at pH 6, temperature 30°C. chromium in non sterile effluents. This approach alsoHe inoculated Aspergillus niger in soil microcosm avoids the contamination problems associated with pure(40% moisture content) with different concentrations of cultures of allochthonous microorganisms. Kankal [80]chromate (250, 500, 1000, 1500 and 2000ppm), it removed added easily degradable organic substances of a verymore than 70% chromium in soil contaminated by 250 and narrow C:N ratio and found marked hexavalent chromium500ppm of chromate. However, chromium-contaminated reduction. Kapoor and Viraraghavan [81] investigatedsoil (2000ppm of potassium chromate) mixed with compost several bacteria from various soils for hexavalent(5% and 10%) significantly removed chromium in chromium resistance and reducing potential. Microbespresence of fungus, Aspergillus niger. selected from both hexavalent chromium-contaminated

Igwe and Abia [73] explained about the sorption and non contaminated soils and sediments were capablebehavior of some biosorbents with various heavy metals, of catalyzing the reduction of hexavalent chromium totheir relative performance evaluated and a bioseperation trivalent chromium a less toxic, less water-soluble form ofprocess flow diagram for heavy metal removal from chromium, demonstrating the utility of using a selectionwastewater using biosorbents was proposed. Some strategy for indigenous hexavalent chromium reducingbiosorbents such as algae, fungi, bacteria have been bacteria in a bioprocess. As a result, indigenousinvestigated for their capacity towards heavy metals. hexavalent chromium reducing microbes from

Chromium Reduction by Bacteria: Many industrial developing a bioprocess to reduce hexavalent chromiumsites are contaminated with toxic trace metals which are to trivalent chromium in non-sterile effluents such asthen diverted into the environment, leading to pollution of those from soil washes.surface and groundwater supplies. Heavy metals have Kapoor and Viraraghavan [82] reported that thea wide range of industrial applications such as reduction of hexavalent chromium to trivalent chromiumelectroplating, metal finishing or tanning and in mining decreases the toxicity and mobility of chromiumindustries. As a result, they are present in many industrial contaminants in soils and water. In addition, the formationdischarges. These heavy metals pose serious of a highly insoluble trivalent chromium product wouldenvironmental implications as they remain mobilized in the decrease the likelihood o f future trivalent chromiumfood chain and are toxic to the biota [74]. Komori et al. re-oxidation. Kapoor et al. [83] reported that chromium[75] inferred that conventional methods for removing toxic reduction by Pseudomonas putida. He explained thechromium include chemical reduction followed by characterization of chromate reductase activities by aprecipitation, ion exchange and adsorption on activated soluble protein fraction from Pseudomonas putida.coal, alum, kaolinite and ash. However, most of these Chromate reduction required either NADH or NADPH formethods require high energy or large quantities of maximum activity. Romanenko and Koren Ken [84]chemical reagents. indicated that the early investigations demonstrate the

Jeyasingh and Philip [76] indicated that vast facultative anaerobic bacteria such as Pseudomonasliterature is available on chromate reduction by bacteria dechromaticans, Pseudomonas chromatophila andincluding physiological, biochemical and genetic Aeromonas dechromatica remove hexavalent chromiumaspects of chromate toxicity/resistance and reduction. from solution by the formation of a trivalent chromiumJuliette Lamberta and Mohammed Rakib [77] explained precipitate.that reduction of hexavalent chromium by the earthworm Romanenko and Korenken [85] first reported that theEisenia foetida. He also suggested that Eisenia foetida Aeromonas sp. Capable of hexavalent chromium reductionplay an important role during occasional hexavalent >70% anaerobically. He also found that several facultativechromium pollution of soils. Kader et al. [78] explained anaerobes tolerant to high levels of chromate (>400µg/ml)that the technical process for removing trivalent chromium were isolated from tannery effluents. Laxman and Morefrom tannery wastewater via precipitation. (2001) [86] found that chromate is a oxidizing agent that

Kamaludeen et al. [79] demonstrated that isolation is reduced intracellularly to pentavalent chromiumof hexavalent chromium reducing anaerobes from and reacts with nucleic acids and other cell componentshexavalent chromium contaminated and non contaminated to produce mutagenic and carcinogenic effects on

contaminated sites should provide the means for


313

biological systems. LilianaMorales-Barrera and for bioremediation. Shaili Srivastava and Indu ShekharEliseoCristiani-Urbina [87] assessed that hexavalent Thakur [96] studied the relationship between thechromium reduction to pentavalent chromium is hexavalent chromium resistance of the culturable microbialresponsible for chromate toxicity, further reduction to community and the hexavalent chromium resistance andtrivalent chromium leads to the formation of stable, less reducing ability strains of each population. Shailisoluble and less toxic trivalent chromium. Reduction of Srivastava and Indu Shekhar Thakur [97] isolatedhexavalent chromium to trivalent chromium is therefore a chromium resistant bacterial strain Bacillus cereus S-6potentially useful process for remediation of hexavalent from effluents of tannery was used for the reduction ofchromium affected environments. toxic hexavalent chromium into less toxic trivalent

Luef et al. [88] observed the microbial reduction of chromium. At an initial hexavalent chromiumtoxic hexavalent chromium has practical importance, concentration of 100 µg/mL, the cytosol and membranebecause biological strategies provide green technology preparation of the strain were able to reduce almost 67 andthat is cost-effective. Mahvi et al. [89] inferred that the 43% of hexavalent chromium within 24 hrs incubationrecovery of chromium III from tannery wastewater by period while the heat killed cytosol and membraneusing three aqueous oxidants, Hydrogen peroxide, preparation reduced 24 and 18% within the same timeSodium Hypochlorite and Calcium Hypochlorite were period.independently oxidizing to soluble chromate under Shikha Rastogi and Saxene [98] concluded thatalkaline conditions. Megharaj and Naidu [90] highlighted Pseudomonas fluorescens LB 300, reduces hexavalentthat amino acid mixtures are the best electron donars for chromium while growing aerobically glucose medium, alsohexavalent chromium reduction. Infact, in one study, grows in an anaerobic chamber containing oxygen-freethe number of viable cells decreased in the initial stages nitrogen on agar plates containing acetate as a potentialafter hexavalent chromium was added and 50% of the electron donor and hexavalent chromium as the potentialadded hexavalent chromium was reduced before viable electron acceptor. However, no hexavalent chromiumcell numbers increased over what was present prior to reduction occurs in anaerobic liquid cultures. Siegel et al.hexavalent chromium addition. Modak et al. [91] stated [99] demonstrated that Enterobacter cloacae strain HO1that organic matter content and bioactivity were reduces hexavalent chromium while growing underimportant factors in reducing almost 96% of the added anaerobic conditions in a medium that contains acetatehexavalent chromium under aerobic, field moist and amino acids as a potential electron donars.conditions. It suggests that organic amended soils can Enterobacter cloacae can grow anaerobically in thereadily reduce hexavalent chromium and could promote absence of added hexavalent chromium and no evidenceexcellent removal efficiency. for hexavalent chromium depended growth has been

Rathinam Aravindhan et al. [92] demonstrated that presented.the biological removal of carcinogenic hexavalent Srinath et al. [100] found that some organism reducechromium using mixed Pseudomonas strains. Under hexavalent chromium during anaerobic growth in media inoptimal conditions, 100mg/L of hexavalent chromium was which hexavalent chromium is provided as the solecompletely reduced within 180 min. Puranik and electron acceptor, in no instance has hexavalent chromiumPaknikar [93] found that the hexavalent chromium was reduction definitely been shown to yield energy toreduced by gram negative bacteria Providencia sp. support anaerobic growth. For example, PseudomonasIt reduced chromate to 100% at a concentration ranging chromatophila uses hexavalent chromium as an electronfrom 100-300 mg/L. It also exhibited multiple heavy metal acceptor to support growth under anaerobic conditionstolerance. Quintelas and Fernandes [94] assessed that with a variety of electron donars, including thethe low temperature reduction of hexavalent chromium non-fermentable substrate, acetate.by a Arthrobacter aurescens. Saranraj et al. [101] isolated a bacterial strain from

Urvashi Thacker and Rasesh Parikh [95] assessed tannery effluent and identified it as Enterococcusthat the reduction of chromate by cell-free extract of casseliflavus. It showed a high level resistance ofBrucella sp. Isolated from hexavalent chromium 800 µg/ml chromium. The minimal inhibitory concentrationcontaminated sites. High hexavalent chromium of chromium was found to be 512 µg/ml of potassiumconcentration resistance and high hexavalent chromium dichromate in Nutrient broth medium. The chromiumreducing ability of the strain make it a suitable candidate adsorption was more significant by the live cells than


314

killed cells at different time intervals. It was observed Properties of the Tannery Effluents: Bioremediation hasthat, the inoculation of Enterococcus casseliflavus developed from the laboratory to a fully commercializedreduced the BOD and COD values of tannery effluent. technology over the last 30 years in many industrializedThe maximum adsorption of chromium was at a countries. A successful bioremediation scheme relies ontemperature of 35 to 45°C and at a pH of 7.0 to 7.5. the management of soil microbial populations capable of

Subsequent studies have shown that the capacity for catabolizing the contaminants. Heavy metals exhibit toxichexavalent chromium reduction is widespread and is effects on soil biota and they can affect key microbialreported in organisms such as Bacillus cereus, Bacillus processes and decrease the number and activity of soilsubtilis, Pseudomonas aeruginosa, Achromobacter microorganisms [114]. Microbial population has oftenEurydice, Micrococcus roseus and Escherichia coli been proposed to be an easy and sensitive indicator of[102] as well as Pseudomonas ambigua [103], anthropogenic effects on soil ecology. Cr (VI) has beenPseudomonas fluorescens [104], Enterobacter cloacae reported to cause shifts in the composition of soil[105], Streptomyces sp. [106], Pseudomonas putida [107], microbial populations and known to cause detrimentalDesulfovibrio desulfuricans and Desulfovibrio vulgaris effects on microbial cell metabolism at high[108] and Pseudomonas liquefaciens [109]. concentrations. Quite a few studies on soil contamination

Chromium Reduction by Fungi: Filamentous fungi can Since, the discovery of the first microbe capablebe profitably used in processes for heavy metals removal of reducing Cr in the 1970s [116], the search forfrom wastewater due to their low cost and to the high ion Cr -reducing microorganisms (both aerobic andexchange capacity of their cell walls. This property arises anaerobic) has been enthusiastically pursued, withfrom the large density of functional groups present in the numerous strains being isolated. Based on recentcell wall (carboxyl, hydroxyl, amine, phosphoryl, isolation and purification of Cr reductases from aerobicsulfhydryl), creating a negatively charged surface [110]. bacteria and the fact that the process involved inThe sorption properties of cell have been widely Cr reduction occurring under anaerobic conditions isstudied by solution chemistry [111], but the chemical starting to be understood, biological processes fornature of complexing groups is not known. The nature of treating chromium contaminated sites are becoming veryPb binding sites on the cell walls of the filamentous promising. Some of the emerging technologies for thefungus Penicillium chrysogenum was investigated at the mitigation and remediation of Cr (VI) include microbialmacroscopic level by sorption isotherm and at the strategies for in situ and on-site bioremediation strategiesmolecular level by extended X-ray absorption free and use in permeable reactive barriers.structure (EXAFS) spectroscopy by varying the Discovery of microorganisms capable of reducingmetal concentration by two orders of magnitude, down Cr (VI) to Cr (III) have significant potential in developmentto 4.8 10.3 m mol Ph/g. of in situ or on-site bioremediation strategies. In 1977, the

ShailiSrivastava and InduShekharThakur [112] first reported bacterial strains, Pseudomonas, wereisolated the Aspergillus niger from soil and effluent of isolated from chromate (CrO contaminated sewageleather tanning mills had higher activity to remove sludge by Russian scientists N.A. Romanenko andchromium. He also indicated that removal of more than V. Korenkov. Since 1977, several other CrO42- reducing75% chromium by Aspergillus niger determined by strains have been reported, including other strains suchdiphenylcarbazide colorimetric assay and atomic as B. cereus, B. subtilis, P. aeruginosa, P. ambigua,absorption spectrophotometry after 7 days. P. fluorescens, E. coli, Achromobacter eurydice,

LilianaMorales-Barrera and EliseoCristiani-Urbina Micrococcus roseus, Enterobacter cloacae,[113] identified that hexavalent chromium was removed Desulfovibrio desulfuricans and D. vulgaris [117].by a Trichoderma inhamatum fungal strain isolated from A number of bacteria in other genera, viz., Bacillus spp.,Tannery effluent. And the fungus exhibited a remarkable E. coli ATCC 33456, Shewanella alga BrY-MT and acapacity to tolerate and completely reduced hexavalent few unidentified strains have also been shown to reducechromium concentrations up to 2.43mM. He indicated that Cr [118]. Terry Beveridge [119] worked on isolation andthe Trichoderma inhamatum fungal strain may have characterization of a chromium reducing bacterium from apotential applications in bioremediation of hexavalent chromated copper arsenate contaminated site. Reportschromium contaminated wastewaters. conclude a Gram-negative bacterium (CRB5) isolated from

of heavy metal from industrial sites were reported [115].

6+

6+

6+

6+

42-

6+


315

a chromium-contaminated site that was capable of Jonnalagadda Raghava Rao [127] reported biologicalreducing hexavalent chromium to an insoluble precipitate, removal of carcinogenic chromium (VI) using mixedthereby removing this toxic chromium species from Pseudomonas strains. In this study an aerobic reductionsolution. of Cr (VI) to Cr (III) by employing mixed Pseudomonas

Laxman and More [120] found that the effect of cultures isolated from a marshy land has been reported.pH and temperature on maximum chromium reduction The role of chromium concentration, temperature, pH andoccurred in pH range of 6-7 and 37°C -50°C by additives on the microbial reduction of Cr (VI) has beenStreptomyces griseus. Zainul Akmar Zakaria et al. [121] investigated. NADH was found to enhance the rate ofobserved that maximum chromium reduction occur at the reduction of Cr (VI). Complete reduction of Cr (VI) hasoptimum pH (7 – 9) and temperature (30°C) of growth by been possible even at Cr (VI) concentrations of 300 ppm.Bacillus sp. Ravibabu [122] studied the remediation of Sadeeshkumar et al. [128] studied that the removal ofeffluents using physical methods like activated charcoal, COD from tannery wastewater is attractive for thepH ranges and time periods and biological methods using betterment of environment. Tanning wastewaterthe aquatic weed hyacinth as a biological pollutant containing high COD (3413 mg/ml) was oxidized withremoval. aqueous oxidants i.e. Hydrogen peroxide, Sodium

Yoshinobu Ishibashi and Simon Silver [123] explained Hypochlorite and Calcium Hypochlorite at differentabout the various industrial discharges of toxic chemical temperatures and reaction durations.pollutants requires biological treatment. He showed apermissible reduction of BOD (80%-90%) for both paper REFERENCESmill and dying industry effluents. Duangporn Kantachoteet al. [124] identified the reduction of biological oxygen 1. Sultan, S. and S. Hasnain, 2005. Chromate reductiondemand in tannery effluents from 4967 mg/L to 1010 mg/ml capability of a gram positive bacterium isolated fromafter inoculation of Rhodopseudomonas blastica. He also effluent of dying industry. Environmentfound the reduction of chemical oxygen demand from Contamination and Toxicology, 75: 699-706.7328 mg/L to 3371 mg/L in tannery effluents. 2. Cheung, K.H. and J.D. Gu, 2005. Reduction of

Young Hak Kwak and Han Bok Kim [125] chromate by an enrichment consortium and an isolatedemonstrated that the maximum amount of biomass of marine sulphate-reducing bacteria. Chemosphere,growth and chromium removal rate occurred at pH 5 and 52: 1523-1529.were 0.35% (Dry weight) and 96.6%, respectively. And the 3. Thacker, U. and M. Datta, 2006. Reduction of toxicenzymatic activities of Aspergillus oryzae at pH 5 was chromium and partial localization of chromiumvery suitable in which the living cell of fungi were able to reductase activity in bacterial isolate DM1,grow significantly. He also observed that the maximum World Journal of Microbiology and Biotechnology,biomass growth and chromium removal rate was 21: 891-899.achieved at 30°C and were 0.29% (Dry weight) and 4. Park, D., Y.S. Yun, J.H. Jo and J.M. Park, 2000.96.9%, respectively. While decreasing temperature below Biosorption process for treatment of electroplating24°C decreased fungal growth and enzymatic activity. wastewater containing Cr (VI): Laboratory-scaleFurthermore, increasing the temperature up to about 40°C, feasibility test. Industrial Engineering and Chemicaldecreased the fungal growth and consequently the Research, 45(14): 5059-5065.chromium removal extent. 5. Megharaj, M., S. Avudainayagam and R. Naidu, 2003.

Abubacker and Ramanathan [126] found that another Toxicity of hexavalent chromium and its reduction byapproach was molecular techniques used to genetically bacteria isolated from soil contaminated with tanneryengineer plants that could hyperaccumulate chromium waste. Current Microbiology, 47: 51-54.and other heavy metals. In a recent study, it was found 6. Sultan, S. and S. Hasnain, 2005. Chromate reductionthat there was a high correlation in chromium content in capability of a gram positive bacterium isolated fromshoots of many plant species with the content of other effluent of dying industry. Environmentheavy metals such as cadmium, copper, nickel and zinc. Contamination and Toxicology, 75: 699-706.He stated that accumulations of these heavy metals in 7. Camargo, F.A.O., F.M. Bento, B.C. Okeke andplant shoots were found to be associated. Using recent W. T. Frankenberger, 2003. Chromate reduction bymolecular approaches, it will be possible to evolve plants chromium resistant bacteria isolated from soilssuitable for phytoremediation of soils and waters contaminated with dichromate. Journal ofcontaminated with chromium and other heavy metals. Environmental Quality, 32: 1228-1233.


316

8. Camargo, F.A.O., F.M. Bento, B.C. Okeke and 21. Park, D., Y.S. Yun, J.H. Jo and J.M. Park, 2000.W. T. Frankenberger, 2003. Chromate reduction by Biosorption process for treatment of electroplatingchromium resistant bacteria isolated from soils wastewater containing Cr (VI): Laboratory-scalecontaminated with dichromate. Journal of feasibility test. Industrial Engineering and ChemicalEnvironmental Quality, 32: 1228-1233. Research, 45(14): 5059-5065.

9. Kapoor, A. and T. Viraraghavan, 1997. Heavy Metal 22. Bento, G. and K. Okeke, 2003. Chromate reductionBiosorption sites in Aspergillus niger. Bioresource by chromium resistant bacteria isolated from soilsTechnology, 61: 221-227. contaminated with dichromate. Journal of

10. Niu H., X. Xu and J.H. Wang, 1993. Removal of lead Environment Quality, 32: 1228-1233.from aqueous solutions by penicillin biomass. 23. Ravibabu, C.H., K. Nagaveni and N. Jamil, 2007.Biotechnology and Bioengineering, 42: 785-787. The toxic effects industrial influence on rats:

11. Nourbakhsh, M., Y.S ag, D. Ozer, Z. Aksu, T. Katsal Analysis and remediation methods. Internationaland A. Calgar, 1994. A comparative study of various Journal of Toxicology, 3(2): 45-47.Biosorbents for Removal of Chromium (VI) ions 24. Flores, A. and J.M. Perez, 1999. Cytotoxicity,from Industrial wastewaters. Process Biochemistry, apoptosis and in vitro DNA damage induced by29: 1-5. potassium chromate. Toxicology and Applied

12. Gill, R.K., V. Jindal, S.S. Gill and S.S. Marwaha, 1996. Pharmacology, 161: 75-81.Studies on the biosorption of nickel from industrial 25. Sultan, S. and S. Hasnain, 2005. Chromateeffluent. Pollution Research, 15(3): 303-306. reduction capability of a Gram positive bacterium

13. Smith, W.A., W.A. Apel, J.N. Petersen and isolated from effluent of dying industry.B.M. Peyton, 2002. Effect of carbon and energy Environment Contamination and Toxicology,source on bacterial chromate reduction. 75: 699-706.Bioremediation Journal, 6: 205-215. 26. Cheung, K.H. and J.D. Gu, 2005. Reduction of

14. Viamajala, S., B.M. Peyton, R.K. Sani, W.A. Apel chromate by an enrichment consortium and an isolateand J.N. Petersen, 2004. Toxic effects of chromium of marine sulphate-reducing bacteria. Chemosphere,(VI) on anaerobic and aerobic growth of Shewanella 52: 1523-1529.oneidensis MR-1. Biotechnology, 20: 87-95. 27. Megharaj, M., S. Avudainayagam and R. Naidu, 2003.

15. Costa, M., 2003. Potential hazards of hexavalent Toxicity of hexavalent chromium and its reduction bychromate in our drinking water. Toxicology and bacteria isolated from soil contaminated with tanneryApplied Pharmacology, 188: 1-5. waste. Current Microbiology, 47: 51-54.

16. Desh Deepak and Ajay Kumar Gupta, 1991. 28. Thacker, U. and M. Datta, 2006. Reduction of toxicCr VI removal from wastewater. Indian Journal of chromium and partial localization of chromiumEnvironmental Health, 33(3): 297-305. reductase activity in bacterial isolate DM1,

17. Schulin, R., 2007. Heavy metal contamination along a World Journal of Microbiology and Biotechnology,soil transect in the vicinity of the iron smelter of 21: 891-899.Kremikovtzi (Bulgaria). Geoderma, 140: 52-61. 29. Park, D., Y.S. Yun, J.H. Jo and J.M. Park, 2000.

18. Srinath, T., P.W. Verma, P. Ramteke and S.K. Garg, Biosorption process for treatment of electroplating2002. Chromium (VI) biosorption and bioaccumulation wastewater containing Cr(VI): Laboratory-scaleby chromate resistant bacteria. Tannery Technology, feasibility test. Industrial Engineering and Chemical48 (4): 427-435. Research, 45(14): 5059-5065.

19. Obbard, P., 2001. Ecotoxicological assessment of 30. Viamajala, S., B.M. Peyton, R.K. Sani, W.A. Apelheavy metals in sewage sludge amended soils. and J.N. Petersen, 2004. Toxic effects of chromiumJournal of Applied Geochemistry, 16: 1405-1411. (VI) on anaerobic and aerobic growth of Shewanella

20. Calormiris, J., J.L. Armstrong and R.J. Seidler, 1984. oneidensis MR-1, Biotechnology, 20: 87-95.Association of metal tolerance with multiple 31. Srinath, T., P.W. Verma, P. Ramteke and S.K. Garg,antibiotic resistance of bacteria isolated from 2002. Chromium (VI) biosorption and bioaccumulationdrinking water. Applied Environmental Microbiology, by chromate resistant bacteria. Tannery Technology,47(6): 1238-1242. 48(4): 427-435.


317

32. Sultan, S. and S. Hasnain, 2005. Chromate reduction 43. Jonnalagadda, R.R., A. Rathinam, J.S. Kalaricalcapability of a gram positive bacterium isolated from and U.N. Balachandran, 2007. Biological removal ofeffluent of dying industry. Environmental carcinogenic chromium (VI) using mixedContamination and Toxicology, 75: 699-706. Pseudomonas strains. Journal of General and

33. Rajamani, S., T. Ramasami, J.S.A. Langerwerf and Applied Microbiology, 53(2): 71-91.J.E. Schappman, 1995. Environment management in 44. Komori, K.A., A. Rivas, K. Toda and H. Ohtake, 1990.tanneries feasible chromium recovery and reuse A method for removal of toxic chromium usingsystem. In proceedings of 3 international conference dialysis-sac cultures of a chromate-reducing strain ofrd

on appropriate waste management technologies for Enterobacter cloacae. Applied Microbiology anddeveloping countries. Nagpur, 965-973. Biotechnology, 33: 117-119.

34. Megharaj, M., S. Avudainayagam and R. Naidu, 45. Romanenko, V.I. and V.N. Korenkov, 1977. A pure2003. Toxicity of hexavalent chromium and its culture of bacterial cells assimilating chromatesreduction by bacteria isolated from soil and bichromates as hydrogen acceptors whencontaminated with tannery waste. Current grown under anaerobic conditions. Mikrobiologiya,Microbiology, 47: 51-54. 46: 414-417.

35. Bento, H. and O. Okeke, 2003. Chromate reduction by 46. Schulin, R., 2007. Heavy metal contaminationchromium resistant bacteria isolated from soils along a soil transect in the vicinity of the ironcontaminated with dichromate. Journal of smelter of Kremikovtzi (Bulgaria). Geoderma,Environmental Quality, 32: 1228-1233. 140: 52-61.

36. Turick, M., F. Edwards and W. Carmiol, 1996. 47. Lovley, D.R. and E.J.P. Phillips, 1994. ReductionIsolation of Cr VI reducing anaerobes from of chromate by Desulfovibrio vulgaris and itsCr contaminated and non-contaminated areas. C3 cytochrome. Applied EnvironmentalApplied Biotechnology and Microbiology, Microbiology, 60: 726-728.44(5): 683-688. 48. Sultan, S. and S. Hasnain, 2005. Chromate reduction

37. Camargo, F.A.O., F.M. Bento, B.C. Okeke and capability of a Gram positive bacterium isolated fromW.T. Frankenberger, 2003. Chromate reduction by effluent of dying industry. Environmentalchromium resistant bacteria isolated from soils Contamination and Toxicology, 75: 699-706.contaminated with dichromate, Journal of 49. Turick, J. and R. Carmiol, 1996. Isolation of Cr VIEnvironmental Quality, 32: 1228-1233. reducing anaerobes from Cr contaminated and non

38. Cheung, K.H. and J.D. Gu, 2010. Reduction of contaminated areas. Applied Biotechnology andchromate by an enrichment consortium and an isolate Microbiology, 44(5): 683-688.of marine sulphate-reducing bacteria. Chemosphere, 50. Beszedits, S., 1988. Chromium removal from industrial52: 1523-1529. wastewaters, In: J.O. Nriagu and E. Nieboer (Eds.),

39. Costa, M., 2003. Potential hazards of hexavalent Chromium in the Natural and Human Environments,chromate in our drinking water. Toxicology and John Wiley, New York, pp: 232-263.Applied Pharmacology, 188: 1-5. 51. Flores, A. and J.M. Perez, 1999. Cytotoxicity,

40. Donati, E., C. Oliver and G. Curutchet, 2003. apoptosis and in vitro DNA damage induced byReduction of chromium (VI) by the indirect action of potassium chromate. Toxicology and AppliedThiobacillus thioparus. Brazil Journal of Chemical Pharmacology, 161: 75-81.Engineering, 20(1): 1999-2005. 52. Guha, H., K. Jayachandran and F. Maurrasse, 2001.

41. Flores, A and J.M. Perez, 1999. Cytotoxicity, Kinetics of chromium (VI) reduction by a type strainapoptosis and in vitro DNA damage induced by Shewanella alga under different growth conditions.potassium chromate. Toxicology and Applied Environmental Pollution, 115: 209-218.Pharmacology, 161: 75-81. 53. Jonnalagadda, R.R., A. Rathinam, J.S. Kalarical and

42. Guha, H., K. Jayachandran and F. Maurrasse, 2001. U.N. Balachandran, 2007. Biological removal ofKinetics of chromium (VI) reduction by a type strain carcinogenic chromium (VI) using mixedShewanella alga under different growth conditions. Pseudomonas strains. Journal of General and AppliedEnvironmental Pollution, 115: 209-218. Microbiology, 53(2): 71-91.


318

54. Komori, K.A., A. Rivas, K. Toda and H. Ohtake, 1990. 66. Muhammed Faisal and Shahida Hasnain, 2004.A method for removal of toxic chromium usingdialysis-sac cultures of a chromate-reducing strain ofEnterobacter cloacae. Applied Microbiology andBiotechnology, 33: 117-119.

55. Lofroth, G. and B.N. Ames, 1997. Mutagenicity ofinorganic compounds in Salmonella typhimurium:arsenic, chromium and selenium. Mutation Research,53: 65-66.

56. Lovley, D.R and E.J.P. Phillips, 1994. Reductionof chromate by Desulfovibrio vulgaris and itsC3 cytochrome. Applied EnvironmentalMicrobiology, 60: 726-728.

57. Muhammed Faisal and Shahida Hasnain. 2004.Microbial conversion of Cr VI to Cr III in industrialeffluent. African Journal of Biotechnology, 3: 610-617.

58. Urvashi Thacker and Rasesh Parikh, 2006.Reduction of chromate by cell-free extract ofBrucella sp. isolated from Cr VI contaminated sites.Bioresource Technology, 98: 1541-1547.

59. Middleton, S.S., R.B. Latmani, M.R. Mackey,M.H. Ellisman, B.M. Tebo and C.S. Criddle, 2003.Co-metabolism of Cr (VI) by Shewanella oneidensisMR-1 produces cell-associated reduced chromiumand inhibits growth. Biotechnology andBioengineering, 83: 627-637.

60. Obbard, P., 2001. Ecotoxicological assessment ofheavy metals in sewage sludge amended soils.Journal of Applied Geochemistry, 16: 1405-1411.

61. Park, D., Y.S. Yun, J.H. Jo and J.M. Park, 2000.Biosorption process for treatment of electroplatingwastewater containing Cr(VI): Laboratory-scalefeasibility test. Industrial Engineering and ChemicalResearch, 45(14): 5059-5065.

62. Pedersen, N.B., 1982. The effects of chromium onthe skin. In: S. Langards, editor. Biological andenvironmental aspects of chromium. Amsterdam:Elsevier Biomedical Press, pp: 249-75.

63. Srinath, T. Verma, P.W. Ramteke and S.K. Garg, 2002.Chromium (VI) biosorption and bioaccumulation bychromate resistant bacteria. Tannery Technology,48(4): 427-435.

64. Arvindhan, S. and M. Madhan, 2004.Bioaccumulation of Cr from tannery wastewater.Journal of American Leather Chemist Association,1: 197-203.

65. Asatiani, Z., N. Abuladze and H. Lejava, 2004.Effect of chromium VI action on Arthrobacteroxydans. Journal of Current Microbiology,49(5): 321-326.

Microbial conversion of Cr VI to Cr III in industrialeffluent. African Journal of Biotechnology, 3: 610-617.

67. Gonul Donmez and Nur Koçberber, 2005.Bioaccumulation of hexavalent chromium by enrichedmicrobial cultures obtained from molasses and NaClcontaining media. Journal of Process Biochemistry,40(7): 2493-2498.

68. Franco Baldi, Ann M. Vaughan and Gregory J. Olson,1990. Chromium(VI)-resistant yeast isolated from asewage treatment plant receiving tannery wastes.Journal of Applied and Environmental Microbiology,56(4): 913-918.

69. Srinivasa Rao, Popuri Ajithapriya and JammalaKrishnaiah Abburi, 2007. Biosorption of hexavalentchromium using tamarind (Tamarindus indica) fruitshell-a-comparative study. Electronic Journal ofBiotechnology, 10(3): 69-75.

70. Gupta, R., P. Ahuja, S. Khan, R.K. Saxena andH. Mohapata, 2000. Microbial biosorbents: Meetingchallenges of heavy metal pollution in aqueoussolutions. Current Science, 78(8): 967-973.

71. Igwe, J.C. and A.A. Abia, 2006. A bioseparationprocess for removing heavy metals from waste waterusing biosorbents. African Journal of Biotechnology,5(12): 1167-1179.

72. Shaili Srivastava and Indu Shekhar Thakur, 2006.Evaluation of bioremediation and detoxificationpotentiality of Aspergillus niger for removal ofhexavalent chromium in soil microcosm. Journal ofSoil Biology and Biochemistry, 38(7): 1904-1911.

73. Igwe, J.C. and A.A. Abia, 2006. A bioseparationprocess for removing heavy metals from waste waterusing biosorbents. African Journal of Biotechnology,5(12): 1167-1179.

74. Butter. T.J., L.M. Evison, I.C. Hancock, F.S. Hollandand K.A. Matis, 1996. Removal and recovery of heavymetals from dilute aqueous streams by biosorptionand electrolysis. Medical Genetics, 61(4b): 1863-1870.

75. Komori, K.A., A. Rivas, K. Toda and H. Ohtake,1990. A method for removal of toxic chromium usingdialysis-sac cultures of a chromate-reducing strainof Enterobacter cloacae. Applied Microbiology andBiotechnology, 33: 117-119.

76. Jeyasingh, J. and L. Philip, 2005. Bioremediation ofchromium contaminated soil: optimization ofoperating parameters under laboratory conditions.Journal of Hazardous Materials, 118: 113-120.


319

77. Juliette Lamberta and Mohammed Rakib, 2006. 90. Megharaj, L. and M. Naidu, 2003. Toxicity ofTreatment of solutions containing trivalent chromium Cr VI and its reduction by bacteria isolated from soilby electrodialysis. Journal of Ecobiotechnology, contaminated with tannery waste. Current34 (7): 100-106. Microbiology, 47(1): 51-54.

78. Kader, P., O. Sannasi, B.S. Othman, B. Ismail and 91. Modak, J.M., K.A. Natarajan and B. Saha, 1996.B. Salmijah, 2007. Removal of Cr(VI) from Aqueous Biosorption of copper and zinc using wasteSolutions by Growing and Non-growing Populations Aspergillus niger biomass. Minerals and Metallurgyof Environmental Bacterial Consortia. Global Journal Process, 13(2): 52 -57.of Environmental Research, 1(1): 12-17. 92. Rathinam Aravindhan and Balachandran Unni Nair,

79. Kamaludeen, S.P., M. Megharaj, A.L. Juhasz, 2006. Biological removal of carcinogenic Cr VI usingS. Sethunathan and N. Naidu, 2003. Chromium- mixed Pseudomonas strains. Bioresourcemicroorganism interactions in soils: remediation Technology, 11(3): 11-17.implications. Journal of Environmental Toxicology, 93. Puranik, P.R. and K.M. Paknikar, 1999. Biosorption178: 93-164. of lead, cadmium and zinc by Citrobacte strain

80. Kankal, G., 1987. Dissolved oxygen and detention MCM B-181: characterization studies. Biotechnologytime as process parameters in sewage treatment by Progress, 15: 228-237.created lagoon. Recent Advances in Science and 94. Quintelas, J. and M. Fernandes, 2012. Biosorption ofTechnology, 14: 61-64. Cr (VI) by an Escherichia coli Biofilm Supported on

81. Kapoor, A. and T. Viraraghavan, 1997. Heavy Metal GAC. Journal of Applied Sciences, 34(6): 223-231.Biosorption sites in Aspergillus niger. Bioresource 95. Urvashi Thacker and Rasesh Parikh, 2007.Technology, 61: 221-227. Reduction of chromate by cell-free extract of

82. Kapoor, A. and T. Viraraghavan, 1998. Biosorption of Brucella sp. isolated from Cr VI contaminated sites.heavy metals on Aspergillus niger: effect of Bioresource Technology, 98: 1541-1547.pretreatment. Bioresource Technology, 63: 109-113. 96. Shaili Srivastava and Indu Shekhar Thakur, 2006.

Biosorption potency of Aspergillus niger for1999. Removal of heavy metals using Aspergillus removal of chromium (VI). Journal of Biomedical andniger. Bioresource Technology, 70: 95-104. Life Sciences, 53(3): 232-237.

84. Krantz-Rulcker, C., B.A. Uard and J.H. Ephraim, 97. Shaili Srivastava and Indu Shekhar Thakur, 2007.1994. Environmental Science and Technology, Evaluation of biosorption potency of Acinetobacter28: 1502-1505. sp. for removal of hexavalent chromium from tannery

85. Romanenko, V.I. and V. N. Korenken, 1999. A pure effluent. Journal of Earth and Environmentalculture of bacterial cells assimilating chromates Science, 18(5): 637-646.and bichromates as hydrogen acceptors when 98. Shikha Rastogi and Saxene, 2003. BOD analysis ofgrown under anaerobic conditions. Mikrobiologiya, industrial effluents: 5 days to 5 min. Journal of46: 414-417. Current Applied Physics, 2(3): 191-194.

86. Laxman, S. and K. More, 2002. Reduction of hexvalent 99. Siegel, S.M., M. Balun and B.Z. Siegel, 1996.chromium by Streptomyces griseus. Journal of Water, Air and Soil Pollution, 53: 335-344.Environmental Toxicology, 27(4): 135-141. 100. Srinath Verma, P.W. Ramteke and S. K. Garg, 2002.

87. Liliana Morales-Barrera and Eliseo Cristiani-Urbina, Chromium (VI) biosorption and bioaccumulation by2008. Hexavalent Chromium Removal by a chromate resistant bacteria. Tannery Technology,Trichoderma inhamatum Fungal Strain Isolated 48(4): 427-435.from Tannery Effluent. Journal of Earth and 101. Saranraj, P., D. Stella, D. Reetha and K. Mythili, 2010.Environmental Science, 187(4): 233-239. Bioadsorption of chromium resistant Enterococcus

88. Luef, E., T. Prey and C.P. Kubicek, 1991. Biosorption casseliflavus isolated from tannery effluent. Journalof Zinc by Fungal mycelial waste. Applied of Ecobiotechnology, 2(7): 17-22.Microbiology and Biotechnology, 34: 688-692. 102. Sudha Nayar and P. Ramasami, 1985. Bacterial

89. Mahvi, R. Nabizadeh, F. Gholami and A. Khairi, accumulation of chromium. Journal of Leather2007. Adsorption of chromium from wastewater by Science, 32: 88-90.Platanus orientalis leaves. Iranian Journal of 103. Sumit Yadav, O.P. Shukla and U.N. Rai, 2005.Environmental Health, Science and Engineering, Chromium Pollution and Bioremediation. Journal of4(3): 191-196. Environmental Pollution, 11(1): 534-538.

83. Kapoor, A., T. Viraraghvan and D. Roy Cullimore,


320

104. Thiruneelakantan Srinath and Shilpi Khare, 2001. 118. Camargo, F.A.O., B F.M. Ento, B.C. Okeke andIsolation of hexavalent chromim-reducing Cr-tolerant W.T. Frankenberger, 2003. Chromate reduction byfacultative anaerobes from tannery effluent. Journal chromium resistant bacteria isolated from soilsof General Applied Microbiology, 47: 307-312. contaminated with dichromate, Journal of

105. Turick, M. and C. Carmiol, 1996. Isolation of Environmental Quality, 32: 1228-1233.Cr VI reducing anaerobes from Cr contaminated 119. Terry, J., Beveridge, S.M. Jeff and P. David,and non contaminated areas. Applied Biotechnology 2008. Isolation and characterization of aand Microbiology, 44(5): 683-688. chromium-reducing bacterium from a chromated

106. Urvashi Thacker and Rasesh Parikh, 2007. copper arsenate contaminated site. EnvironmentalReduction of chromate by cell-free extract of Microbiology, 2(6): 611-619.Brucella sp. isolated from Cr VI contaminated sites. 120. Laxman, S. and K. More, 2002. Reduction ofBioresource Technology, 98: 1541-1547. hexvalent chromium by Streptomyces griseus.

107. Vidal Nieto, K. Cooman, M. Gajardo and Journal of Environmental Toxicology, 27(4): 135-141.C. Bornhardt, 2004. Unhairing effluents treated by 121. Zainul Akmar Zakaria, Zainoha Zakaria,an activated sludge system. Journal of Hazardous Salmijah Surif and Wan Azlina Ahmad, 2007.Materials, 112: 143-149. Hexavalent chromium reduction by Acinetobacter

108. Lovley, D.R. and E.J.P. Phillips, 1994. Reduction of haemolyticus isolated from heavy-metalchromate by Desulfovibrio vulgaris and its C3 contaminated wastewater. Journal of Hazardouscytochrome. Applied Environmental Microbiology, Materials, 146: 30-38.60: 726-728. 122. Ravibabu, C., H. Nagaveni and K. Jamil, 2004.

109. Krantz-Rulcker, C., B.A. Uard and J.H. Ephraim, 1994. The toxic effects industrial influence on rats:Environmental Science and Technol., 28: 1502-1505. Analysis and Remediation methods. Internet Journal

110. Schulin, R., 2007. Heavy metal contamination along of Toxicology, 3(2): 45-47.a soil transect in the vicinity of the iron smelter of 123. Yoshinobu Ishibashi and Simon Silver, 1990.Kremikovtzi (Bulgaria). Geoderma, 140: 52-61. Chromium reduction in Pseudomonas putida.

111. Wase, J. and C. Forster, 1997. Biosorbents for Applied and Environmental Microbiology,metal ions. London: Taylor & Francis. pp: 2268-2270.

112. Shaili Srivastava and Indu Shekhar Thakur, 2006. 124. Duangporn Kantachote, Salwa Torpee andBiosorption potency of Aspergillus niger for Kamontam Umsakul, 2005. The potential use anremoval of chromium (VI). Journal of Biomedical and oxygenic phototrophic bacteria for treating latexLife Sciences, 53(3): 232-237. rubber sheet wastewater. Electronic Journal of

113. Liliana Morales-Barrera and Eliseo Cristiani-Urbina, Biotechnology, 8(3): 138-143.2008. Hexavalent Chromium Removal by a 125. Young Hak Kwak and Han Bok Kim, 2003.Trichoderma inhamatum Fungal Strain Isolated Vibrio harveyi is also a chromate reductase. Appliedfrom Tannery Effluent. Journal of Earth and Environmental and Microbiology, 69: 4390-4395.Environmental Science, 187(4): 233-239. 126. Abubacker, G. and H. Ramanathan, 2003.

114. Obbard, P., 2001. Ecotoxicological assessment of Bioremediation of tannery effluent pollutants.heavy metals in sewage sludge amended soils. Bioresource Technology, 19 (3): 237-242.Journal of Applied Geochemistry, 16: 1405-1411. 127. Jonnalagadda, R.R., A. Rathinam, J.S. Kalarical

115. Schulin, R., 2007. Heavy metal contamination along and U.N. Balachandran, 2007. Biological removala soil transect in the vicinity of the iron smelter of of carcinogenic chromium (VI) using mixedKremikovtzi (Bulgaria). Geoderma, 140: 52-61. Pseudomonas strains, Journal of General and

116. Romanenko, V. I. and V.N. Korenkov, 1977. Applied Microbiology, 53(2): 71-91.A pure culture of bacterial cells assimilating 128. Sadeeshkumar, R., P. Saranraj and D. Annadurai,chromates and bichromates as hydrogen acceptors 2012. Bioadsorption of the toxic heavy metalwhen grown under anaerobic conditions. Chromium by using Pseudomonas putida.Mikrobiologiya, 46: 414-417. International Journal of Research in Pure and

117. Wase, J. and C. Forster, 1997. Biosorbents for Applied Microbiology, 2(4): 32-36.metal ions. London: Taylor & Francis.

Documents

Microbial Bioremediation of Chromium in Tannery Effluent: A …idosi.org/ijmr/ijmr4(3)13/12.pdf · 2019-08-02 · metal removal processes because of their low cost and soils surrounding