Biosorption of Copper Ions by Bacillus cereus M 16 from Aqueous Solution

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Biosorption of Copper Ions by Bacillus cereus M1 16

from Aqueous SolutionHimadri Bairagi a , Amit Ghati a & Lalitagauri Ray aa Department of Food Technology and Biochemical Engineering , Jadavpur University ,Kolkata, 700 032, IndiaPublished online: 16 Apr 2010.

To cite this article: Himadri Bairagi , Amit Ghati & Lalitagauri Ray (2010) Biosorption of Copper Ions by Bacillus cereus M1 16

from Aqueous Solution, Indian Chemical Engineer, 51:3, 203-214, DOI: 10.1080/00194500903361348

To link to this article: http://dx.doi.org/10.1080/00194500903361348

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Biosorption of Copper Ions byBacillus cereus M 16

1 fromAqueous Solution

Himadri Bairagi, Amit Ghati and Lalitagauri Ray*Department of Food Technology and Biochemical Engineering

Jadavpur University, Kolkata - 700 032, India

Abstract: The severity of heavy metal contamination and its potential adverse healthimpact on the public has led to tremendous efforts being made to purify water containingtoxic metal ions. Biosorption is presented as an alternative to traditional physicochemicalmeans for removing toxic metals from ground water and wastewater. Removal of copperfrom solution was studied using growing cells and washed cells of Bacillus cereus M1

16.Optimum process conditions for maximum biosorption (73.3%) of Cu (II) ions usinggrowing cells were – volume of medium: 50 ml in a 250 ml Erlenmeyer flask; temperature:30°C; pH: 6.0; fermentation time: 24 h; inoculum size (24 h cell growth): 3%; initial metalion concentration: 75 mg/L. Removal of copper using washed cells of the selected strainwas investigated in batch mode and equilibrium was attained within 180 min at 30°C,pH 3.5 when initial metal ion concentration was 100 mg/L using 8.18 g/L biomass (dryweight) in 50 ml saline in 250 ml Erlenmeyer flask. Both Langmuir and Freundlichisotherms were tested and it was found that the former had a better fit with the data.

Keywords: Bacillus cereus, Copper, Biosorption, Adsorption isotherm, Kinetics.

IntroductionToxic heavy metal concentration of industrial wastewater is an important environmentalproblem. Heavy metals are toxic to the aquatic ecosystem and human health [1]. Theprogress in technology has also caused detrimental effects of industrial pollution on thenatural environment. The natural process of transportation of metals between the soil andwater consolidates metal contamination, which affects areas of the natural ecosystem [2].

As far as copper is concerned, it is present in industrial wastes, primarily, in the formof bivalent Cu (II) ion as a hydrolysis product, CuCO3 (aqueous) and/or organic complexes.

INDIAN CHEMICAL ENGINEER Copyright © 2009 Indian Institute of Chemical EngineersVol. 51 No. 3 July-September 2009, pp. 203-214Print ISSN: 0019-4506, Online ISSN: 0975-007X, DOI: 10.1080/00194500903361348

*Author for Correspondence. E-mail: [email protected] received: 24/05/2009; Revised paper accepted: 11/09/2009

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Several industries such as dyeing, paper, petroleum, copper-/brass-plating etc., releasehigh amounts of Cu (II) ions. In copper cleaning, copper plating and metal processingwaste, Cu ion concentrations approach 100-120 mg/L, which is very high in relation towater quality standards and permissible Cu (II) concentration of wastewater. These shouldbe reduced to 1.0-1.5 mg/L [3]. The United States (US) Environment Protection Agency(EPA) requires copper concentration in drinking water to not exceed 1.3 mg/L [4]. Ingestinglarge amounts of copper compounds can cause death due to nervous system, liver andkidney failure. It may cause coronary heart disease and high blood pressure. High levelsof copper in drinking water can also cause vomiting, abdominal pain, nausea and diarrhea.

Conventional methods for removing dissolved heavy metal ions from wastewaterhave significant disadvantages including incomplete metal removal, the need for expensiveequipment and monitoring systems, high reagent or energy requirements [5, 6]. Due todevelopments in the field of environmental microbiology, recent studies have focussedon the use of inexpensive microbial biomass as potential biosorbents, which are capableof removing heavy metals from waste streams [7-14].

In the present work, adsorption ability of growing and washed cells of Bacilluscereus M1

16 to remove Cu (II) from aqueous solutions has been investigated. The mechanismand kinetics of copper binding have also been determined.

Materials and Methods

OrganismA mutated strain of Bacillus cereus M1

16 [15] was used for the biosorption of Cu (II) ionsfrom an aqueous solution. It was maintained by monthly subculturing using nutrient agarincubated at 30°C and stored at 4°C.

Removal of Copper using Growing Cells of the Selected StrainBacillus cereus M1

16 was grown in a 250 ml Erlenmeyer flask containing 50 ml medium(beef extract: 1.0; yeast extract: 2.0; peptone: 5.0; NaCl: 5.0 g/L; and pH: 6.0) containing50 mg/L Cu (II) ion incubating at 30°C ± 1 and 120 rpm for 24 h. Cell suspension (3%,v/v) was used as inoculum. After 24 h the culture fluid was centrifuged at 5,000 rpm for10 min at room temperature. Residual concentration of Cu (II) ion present in the clearsupernatant was estimated. The percent metal bound was taken to be the differencebetween the control and final concentration of metal in the supernatant [16].

Biomass Production and Biosorption using Washed BiomassThe same fermentation medium with no Cu (II) ion was used for the production of Bacilluscereus M1

16 biomass under the same environmental conditions stated before. After 24 h,

viable biomass was harvested by centrifugation at 5,000 rpm for 10 min at room temperatureand washed twice with normal saline. Washed cells (required amount) were transferred to50 ml normal saline solution containing 200 mg/L Cu (II) ion in a 250 ml Erlenmeyer flaskand incubated at 30°C, 120 rpm for 200 min. Experiments were carried out with wet biomassof the selected strain and results were calculated using dry biomass basis. According toVolesky, for scientific interpretation, the sorbent material dry-weight basis is preferred [17].

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Preparation of Dry CellsWashed biomass from a measured amount of whole-cell broth was placed in a previouslyweighed aluminium cup and dried at 70°C overnight. It was weighed again and the weightof the dry cell mass was calculated by finding the difference.

Estimation of CopperConcentration of copper in the supernatant was estimated using an atomic absorptionspectrophotometer (Chemito Technologies Pvt. Ltd., India, Model No. AA203, Wavelength:324.7 nm, Slit width: 0.5 nm).

Biosorption IsothermThe Langmuir model [18] qe = qmb · Ce/(1 + b · Ce) may be rearranged as

Ce/qe = 1/b · qm + Ce/qm (1)

where Ce is the equilibrium concentration (mg/L), qe the adsorbed amount of metal ion pergram of biomass at equilibrium (mg/g), qm the maximum amount of metal ion per unitweight of biomass to form a complete mono layer on the surface bound at high Ce (mg/L), and b a constant related to the affinity of binding sites (l/mg). A plot of Ce/qe vs. Ceshould indicate a straight line of slope 1/qm and an intercept of 1/bqm. The Freundlichmodel equation [19] qe = k · Ce

1/n is conveniently used in linear form as

ln qe = ln k + (1/n) ln Ce (2)

where k and n are Freundlich constants characteristics of the system [20]; k is relativeindicator of adsorption capacity (1/g) and n indicates intensity of adsorption.

Kinetic ModellingFirst order rate expression [21-23] based on sorption capacity is generally expressed as

– log10 (qe – qt)/qe = K1t/2 · 3 (3)

where K1 is the rate constant of first order biosorption (min–1).Pseudo second order equation is also based on sorption capacity of the solid phase

[23, 24] as

1/(qe – qt) = 1/q + K2t (4)

t/qt = 1/h + (1/qe)t (5)

where h = K2 qe2 can be regarded as the initial sorption rate as t → 0. If pseudo second

order kinetics is applicable, the plot of t/qt vs. t gives a linear relationship, which allowscomputation of qe and K2 values.

Results and Discussion

Effects of Environmental Conditions on Copper Biosorption using Growing Cells ofBacillus cereus M1

16

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Effect of Inoculum VolumeThe effect of inoculum concentration onCu (II) ion uptake by the selected bacterialstrain was studied using differentconcentration of inoculum (range 1-5%, v/v). Biosorption of Cu (II) ion increasedwith increase in inoculum concentrationupto 3% and then Cu (II) ion uptakedecreased with increase in inoculumvolume (Fig. 1). For further studies 3%inoculum volume was selected. Cu (II) ionaccumulation depends on the amount ofbiomass produced. Production of biomassmay be increased with increase in inoculumvolume upto a limit due to the limitingamount of nutrient in the medium.

Effect of pHThe effect of pH on Cu (II) ion uptake wasinvestigated maintaining pH of the mediumin the range 4.5 to 6.5. Figure 2 shows thatbiosorption of Cu (II) ions increased withincrease in pH upto 6.0 (68%), and then itdecreased with an increase in pH. At higherpH values (> 6.0), Cu ions get precipitateddue to high hydroxyl ion consumption inthe medium. A decrease in metal uptake atlow pH levels suggests low biomassformation. Moreover, cations and protonscompete for the same site. The pH 6.0 wasselected for further studies on biosorption.In 2004, Savvaidis et al. [25] reported thatcopper biosorption by Pseudomonas cepacia from a 10 mM copper solution was maximumat pH 7.0. In 2001, Wong et al. [26] studied copper biosorption using Micrococcus sp.and optimum pH for biosorption was found to be 6.0. In 2006, Sannasi et al. [27] alsoreported optimum pH for sorption of Cu (II) by Bacillus sp. as 5.0 ± 0.1.

Effect of Medium VolumeBiosorption of Cu (II) ion was studied using different volume of medium (pH 6.0) viz: 40,45, 50, 55, 60 and 70 ml containing 50 mg/L Cu (II) ion at 30°C for 24 h. A 24 h cellsuspension was used as inoculum. Accumulation was maximum (70.8% out of 50 mg/L)when 50 ml medium in 250 ml Erlenmeyer flask was used (Fig. 3). The low removalpercentage using 40 ml medium volume is probably due to small biomass formation. Whenthe medium volume is high (e.g. 60 and 70 ml), the aeration rate is decreased and probably

70

60

50

40

30

20

10

00 1 2 3 4 5 6

Inoculum volume (%)

% r

emov

al o

f C

u (I

I)

Fig. 1. Consumption of Cu (II) at differentinoculum volume by Bacillus cereusM1

16.

80

70

60

50

40

30

20

10

04 4.5 5 5.5 6 6.5 7

pH

% r

emov

al o

f C

u (I

I)

Fig. 2. Accumulation of Cu (II) at differentinitial pH by the selected strain.

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inhibits growth of the organism and, in turn, removal of Cu (II) ion from the medium. At50 ml medium volume, both biomass production and aeration rate are optimum for biosorptionof Cu (II) ion.

Effect of Initial Metal Ion ConcentrationCu (II) ion biosorption by Bacillus cereus M1

16 was carried out using different initialconcentration of Cu (II) ions (range: 25-125 mg/L), other conditions remaining the same.Percent removal of copper ion was more or less in the same range when initial Cu (II)concentration was varied in the range of 25-75 mg/L. Then it decreased with increase ininitial Cu (II) concentration, probably, due to toxicity of metal ion (Fig. 4). Cu (II) ionconcentration of 75 mg/L was selected as optimum for further biosorption study.

Experiments with Washed CellsThe relation between washed and dry biomass was studied. The ratio between wet anddry cell was found to be 5.5:1. All experiments were carried out using washed cells (wet),but interpretations were cited on a dry cell weight basis. For scientific interpretation, thesorbent material in terms of dry basis is preferred [17].

Fig. 3. Effect of medium volume on Cu (II) removal by Bacillus cereus M116.

8070605040302010

030 40 50 60 70 80

Medium volume (ml)

% r

emov

al o

f C

u (I

I)

Fig. 4. Influence of initial metal ion concentration on adsorption of Cu (II) byBacillus cereus M1

16.

9080706050403020100

0 20 40 60 80 100 120 140Initial metal ion concentration (mg/L)

% r

emov

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f C

u (I

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Effect of pH and Time Course of BiosorptionThe effect of pH (range: 3.0-4.5) on Cu (II) ion uptake by washed cells (2.727 g/L in drycell basis) of the selected strain was studied using 50 ml solution containing 200 mg/LCu (II) ion in 250 ml Erlenmeyer flask and Cu (II) incubating at 30°C for 3 h at 120 rpm.Uptake was maximum at pH 3.5 (Fig. 5). The pH dependence of metal uptake was due tothe various functional groups present on bacterial cell wall. There was a clear competitionfor the biomass adsorption sites between the Cu (II) and protons since ion exchange isthe main sorption mechanism. Biosorption of Cu (II) ion was rapid and occurred duringthe first 10 min of sorption (86.25%) but, thereafter, equilibrium was reached at 180 min(Fig. 5). Metal binding sites were saturated within 180 min. In 2005, Ray et al. [28]observed that the biosorption of Pb(II) ion using Bacillus cereus M1

16 was rapid duringthe first 30 min of sorption and, thereafter, it remained constant. Within the first 10 min,95% of the total Pb (II) accumulation was observed.

100

95

90

85

80

75

70

% r

emov

al o

f C

u (I

I)

pH 3.0

pH 3.5

pH 4.0

pH 4.5

0 100 200 300Time (min)

(a)

75

70

65

60

55

50

q va

lue

(mg/

g)pH 3.0

pH 3.5

pH 4.0

pH 4.5

0 100 200 300Time (min)

(b)

Fig. 5. Effect of initial pH on Cu (II) biosorption using washed biomass of selected strain.

Effect of Biomass Concentration on BiosorptionThe Cu (II) ion uptake by washed cells of the selected strain was studied using differentamount of biomass (1.363-10.9 g/L) using 50 ml solution (pH 3.5) containing 200 mg/L Cu(II) ion in a 250 ml Erlenmeyer flask at 30°C and 120 rpm for 200 min. With increase inbiomass concentration, biosorption increased up to 8.18 g/L dry biomass (Fig. 6). Availabilityof Cu (II) adsorption sites increases with increasing cell mass concentration, but due toagglomeration of biomass total adsorption sites are not available and Cu (II) adsorptiondecreased.

Effect of TemperatureBiosorption of Cu (II) was carried out using washed cells of Bacillus cereus M1

16 atdifferent temperatures (20-37°C) and biomass concentration as 8.18 g/L, other conditionsremaining the same. It was found (Fig. 7) that maximum Cu (II) ion uptake was observedat 30°C.

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Influence of Initial Copper Concentration on Cu (II) BiosorptionBiosorption was carried out with different initial Cu (II) ion concentration (100-300 mg/L)at biomass concentration (dry weight) of 8.18 g/L with other conditions remaining thesame. The amount of adsorption of Cu (II) ion per unit mass of biosorbent increased withan increase in initial Cu (II) ion concentration (range: 100-300 mg/L), but percent adsorptiondecreased with increase in initial Cu (II) concentration (Fig. 8) due to saturation of metalbinding sites of the biosorbent. At 180 min of incubation maximum adsorption (99.16%)of Cu (II) was observed using 100 mg/L initial Cu (II) concentration.

Fig. 6. Effect of biomass concentration on adsorption of Cu (II) by Bacillus cereus M116.

105

100

95

90

85

80

75

70

% r

emov

al o

f C

u (I

I)1.363 g/L2.727 g/L5.45 g/L8.18 g/L10.9 g/L

0 100 200 300Time (min)

(a)

140

120

100

80

60

40

20

0

1.363 g/L2.727 g/L5.45 g/L8.18 g/L10.9 g/L

q va

lue

(mg/

g)

0 100 200 300Time (min)

(b)

Fig. 7. Effect of temperature on adsorption of Cu (II) by washed biomass.

% r

emov

al o

f C

u (I

I)

0 100 200Time (min)

(a)

105

100

95

90

85

80

75

70

20°C

25°C

30°C

37°C

20°C

25°C

30°C

37°C

0 100 200Time (min)

(b)

39

37

35

33

31

29

27

25

q va

lue

(mg/

g)

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Adsorption IsothermThe equilibrium sorption isotherm is important in the design of a biosorption system.Equilibrium studies in biosorption indicate the capacity of the sorbent. The solution pH wasconstant at 3.5 during the biosorption process. The plot of ln qe vs. ln Ce (Fig. 9) is a straightline having slope l/n and intercept ln K. The applicability of the Langmuir adsorptionisotherm has also been analysed by plotting Ce/qe vs. Ce (Fig. 10). Values of Langmuirand Freundlich adsorption coefficients and correlation coefficients show that the Langmuirmodel (R2 = 0.9898) best fits the experimental data (Table 1). In 1999, Puranik et al. [29]

102

100

98

96

94

92

90

88

86

84

820 100 200 300

Time (min)(a)

% r

emov

al o

f C

u (I

I)

100 ppm

200 ppm

250 ppm

300 ppm

Fig. 8. Effect of initial metal ion concentration on bioaccumulation of Cu (II) byBacillus cereus M1

16.

0 100 200 300Time (min)

(b)

100 ppm

200 ppm

250 ppm

300 ppm

60

55

50

45

40

35

30

25

20

15

q va

lue

(mg/

g)

Fig. 9. Application of Freundlich isotherm to the adsorption data of Cu (II) adsorbedonto the washed biomass of Bacillus cereus M1

16.

4.1

3.9

3.7

3.5

3.3

3.1

2.9

2.7

2.5– 2 – 1 0 1 2 3 4

ln Ce

y = 0.2166 x + 3.2534R2 = 0.8898

ln q

e

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reported sorption characteristics qmax = 68 mg/g using Citrobacter species and theequilibrium of Cu (II) biosorption followed the Langmuir isotherm model very well witha maximum biosorption capacity (qmax) at 52.1 mg of Cu (II)/g of dry cell at pH 6.0.

Kinetics of AdsorptionThe kinetics were investigated with a constant adsorbent concentration of 8.18 mg/L at30°C with four different initial Cu (II) concentration of 100, 200, 250, 300 ppm at differenttime interval up to 200 min (Fig. 11). Pseudo-second-order model based on the equationt/qt = 1/h + (1/qe)t was applied as it considers the rate limiting step as the formation ofchemisorptive bond involving sharing or exchange of electrons between the adsorbateand adsorbent. The plot of t/qt vs. t (Fig. 11) yielded very good straight lines (correlationcoefficient, R2 = 1.0). The second-order rate constants were in the range of 1.437 × 10–1 to4.59 × 10–2 g/mg/min.

ConclusionGrowing and washed biomass of Bacillus cereus M1

16 were found to be efficient foradsorption of Cu (II) from dilute solution. The characterisation of Cu uptake showed thatCu binding is dependent on initial pH, temperature, initial Cu (II) ion concentration andbiomass concentration. The experimental results were analysed using Langmuir andFreundlich equations. Correlation coefficients (R2) show that the Langmuir model fit best

Fig. 10. Application of Langmuir isotherm to the adsorption data of Cu (II) adsorbedonto the washed biomass of Bacillus cereus M1

16.

0.6

0.5

0.4

0.3

0.2

0.1

00 5 10 15 20 25

Ce (mg/L)

Ce/

q e (g

/L)

y = 0.0198 x + 0.0193R2 = 0.9898

Table 1. Sorption isotherm coefficients of Langmuir and Freundlich models

Freundlich Langmuir

R2

0.9898

1/n

0.22

K (L/g)

25.88

R2

0.8898

qm (mg/gm)

50.50

b (L/mg)

1.03

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to the experimental data. The overall adsorption rate showed that the kinetics of adsorptionof Cu (II) on Bacillus cereus M1

16 was best described by the pseudo-second-order model.The results showed that this method of accumulation of Cu (II) ion is very promisingcompared to a more conventional process.

Nomenclatureb Langmuir constant, L/mgC Concentration of metal in solution, mg/LCe Liquid-phase concentration of metal at equilibrium, mg/Lh Initial sorption rateK Constant, relative indicator of adsorption capacity, L/gK1 First-order rate constant, min–1

K2 Second-order rate constant, g/mg/min1/n Constant, intensity of the adsorptionqe Metal uptake at equilibrium, mg/g biomassqm Maximum theoretical metal uptake, mg/g biomassqt Metal uptake at anytime, mg/g biomassR2 Correlation coefficientt Time, min

Fig. 11. Pseudo second order adsorption kinetics of Cu (II) on the washed biomass atdifferent initial metal ion concentration at 30°C.

12

10

8

6

4

2

00 50 100 150 200 250

Time (min)

t/qt (

min

/mg/

g)100 mg/L150 mg/L200 mg/L250 mg/L300 mg/LLinear (100 mg/L)Linear (150 mg/L)Linear (200 mg/L)Linear (250 mg/L)Linear (300 mg/L)

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