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+3
+5
Biosorption of arsenite (As ) and arsenate (As ) from aqueous solution by Arthrobacter sp. biomass ab
a
c
a
Kumar Suranjit Prasad , A. L. Ramanathan , Jaishree Paul , Vaidyanathan Subramanian & d
Ram Prasad a
School of Environmental Sciences, Jawaharlal Nehru University, New Delhi, India
b
Department of Environmental Biotechnology, ARIBASSardar Patel University, New Vallabh Vidyanagar, Anand, Gujarat, India c
School of Life sciences, Jawaharlal Nehru University, New Delhi, India
d
Amity Institute of Microbial Technology, Amity University, Noida, India Accepted author version posted online: 25 Mar 2013.Published online: 29 Apr 2013.
To cite this article: Kumar Suranjit Prasad, A. L. Ramanathan, Jaishree Paul, Vaidyanathan Subramanian & Ram Prasad +3
+5
(2013) Biosorption of arsenite (As ) and arsenate (As ) from aqueous solution by Arthrobacter sp. biomass, Environmental Technology, 34:19, 2701-2708, DOI: 10.1080/09593330.2013.786137 To link to this article: http://dx.doi.org/10.1080/09593330.2013.786137
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Environmental Technology, 2013 Vol. 34, No. 19, 2701–2708, http://dx.doi.org/10.1080/09593330.2013.786137
Biosorption of arsenite (As+3 ) and arsenate (As+5 ) from aqueous solution by Arthrobacter sp. biomass Kumar Suranjit Prasada,b∗ , A.L. Ramanathana , Jaishree Paulc , Vaidyanathan Subramaniana and Ram Prasadd a School
of Environmental Sciences, Jawaharlal Nehru University, New Delhi, India; b Department of Environmental Biotechnology, ARIBAS, Sardar Patel University, New Vallabh Vidyanagar, Anand, Gujarat, India; c School of Life sciences, Jawaharlal Nehru University, New Delhi, India; d Amity Institute of Microbial Technology, Amity University, Noida, India
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(Received 19 August 2012; final version received 8 March 2013 ) In this study we investigated the role of arsenic-resistant bacteria Arthrobacter sp. biomass for removal of arsenite as well as arsenate from aqueous solution. The biomass sorption characteristics were studied as a function of biomass dose, contact time and pH. Langmuir, Freundlich and Dubinin-Radushkevich (D-R) models were applied to describe the biosorption isotherm. The Langmuir model fitted the equilibrium data better than the Freundlich isotherm. The biosorption capacity of the biomass for As+3 and As+5 was found to be 74.91 mg/g (pH 7.0) and 81.63 mg/g (pH 3.0), respectively using 1 g/L biomass with a contact time of 30 min at 28◦ C. The mean sorption energy values calculated from the D-R model indicated that the biosorption of As+3 and As+5 onto Arthrobacter sp. biomass took place by chemical ion-exchange. The thermodynamic parameters showed that the biosorption of As+3 and As+5 ions onto Arthrobacter sp. biomass was feasible, spontaneous and exothermic in nature. Kinetic evaluation of experimental data showed that biosorption of As+3 and As+5 followed pseudo-second-order kinetics. Fourier transform infrared spectroscopy (FT-IR) analysis indicated the involvement of possible functional groups (−OH, −C=O and −NH) in the As+3 and As+5 biosorption process. Bacterial cell biomass can be used as a biosorbent for removal of arsenic from arsenic-contaminated water. Keywords: arsenite; arsenate; biosorption; bioremediation; FT-IR spectroscopy; kinetics
1. Introduction Worldwide reports of subsurface water contamination with arsenic have become a serious public health-related issue. Unfortunately, the severity of this problem has been mainly noticed in developing countries, e.g. the eastern part of India and Bangladesh, Nepal, Inner Mongolia, Cambodia, Thailand, Argentina and Chile, and also in developed nations such as the USA. [1] In and around India in areas such as East Bengal and West Bengal and some areas of North Bihar (Gangatic plain), over 40 million people are being exposed to more than 50 ppb of arsenic whereas, according to the Environmental Protection Agency, the limit is set at 10 ppb. Out of 4 million tube wells in Bangladesh, 1.2 million have been found to contain more than 50 ppb of arsenic and 7600 people are afflicted with chronic arsenicosis. [2] In these developing countries more than 10 ppb of arsenic is still being consumed due to a lack of alternate access to water. [3] Studies have demonstrated an association between high levels of arsenic in drinking water with a significant increase in the risk of cancer for the affected population. [4] Two forms of arsenic are commonly present in natural water, i.e. 3− +3 arsenite (AsO3− 3 ) and arsenate (AsO4 ), referred to As
∗ Corresponding
author. Email: [email protected]
© 2013 Taylor & Francis
and As+5 , respectively. Pentavalent species mostly predominate and are stable in oxidizing aerobic environments such as surface water and shallow ground water, while trivalent arsenite predominates in moderately reducing anaerobic environments such as deep-seated groundwater. [5] Besides the natural phenomenon of release of arsenic due to weathering of rocks and volcanic activity, various anthropogenic activities such as use of pesticides, wood preservatives, dye stuffs and other chemicals containing arsenic are the major sources of water contamination. [6] Numerous materials have been tested for removal of toxic ions from aqueous solutions over the last two decades. [7] However, only a limited number of studies have investigated the use of adsorbents obtained from biological sources, e.g. Penicillium sp., [8] Aspergillus nidulans, [9, 10] Zr-loaded diacetic acid chelating resin, [11] Acacia nilotica, [12] orange juice residue [13] and Zr(IV) loaded orange waste [14] for arsenic removal. Metals are generally non-biodegradable, but can be transformed through sorption, methylation, complexation and by changes in their valence state. These transformations affect the mobility and bioavailability of metals. Microorganisms that affect the
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reactivity and mobility of metals can be used to detoxify some metals and prevent further metal contamination. [15] Katsoyiannis and Zouboulis [16] conducted studies with iron-oxidizing bacteria for removing both arsenite and arsenate. The results indicate that both forms of arsenic could be efficiently removed to an acceptable level of concentration, i.e. less than 10 ppb. This removal was related to a combination of the oxidation of As+3 to As+5 and biosorption of arsenic to the microorganisms. In another experiment, strain ULPAs1, an arsenite oxidizer, was entrapped into calcium alginate beads and investigations were carried out upon oxidation as well as removal of arsenic from growth media. [17] Anaerobic microbial mobilization and biotransformation of arsenate adsorbed onto activated alumina has been studied. [18] The role of sulphate-reducing bacteria for removal of arsenic has also been examined. [19] Recently, studies related to biosorption of arsenic from aqueous solution by Acidithiobacillus ferrooxidans BY-3, [20] Staphylococcus xylosus [21] and Rhodococcus sp.WB-12 [22] have been carried out. Pagnanelli et al. [23] studied biosorption of metals copper, cadmium and iron ions on Arthrobacter sp. biomass. The Arthrobacter sp. is a gram-positive bacterium possessing arsenite oxidizing ability using a membrane-bound enzyme, arsenite oxidase. [24] The Gram-positive bacterial cell wall is thicker than the cell wall of Gram-negative bacteria and harbours a greater number of functional groups that may act as sorption sites for varieties of aqueous chemical species. [25] The present study is an attempt to determine the utility of an Arthrobacter sp. biomass by studying its biosorption characteristics for As+3 and As+5 .
2. Materials and methods 2.1. Biomass preparation The isolate Arthrobacter sp. was inoculated into minimal culture media (MM1). The composition of minimal media is (g/L): (NH4 )2 SO4 , 1.0 g; KH2 PO4 , 0.5 g; KCl, 0.05 g; Ca(NO3 )2 , 0.1 g; NaHCO3 , 0.5 g and 0.04% (w/v) yeast extract. One mL of trace element solution was added to 1 L of culture medium followed by final adjustment of pH to 7.8. Incubation of culture was carried out by placing a culture flask onto an orbital rotatory shaker (Kuhner AG, Switzerland), operating at 220 rpm for 16 h at 28◦ C. Bacterial cells cultured in MM1 were centrifuged at 5000 rpm for 5 min at 4◦ C. Cells were harvested in their log phase when optical density of culture broth reached 0.35 at a wavelength of 600 nm. Pellets were washed with milliQ water for removal of contaminating components that may occur in the culture medium. Cells were heat-killed using an autoclave and resuspended in milliQ followed by freeze-drying using lyophilizer (Labconco, Kansas, USA). Freeze-dried nonviable cells of Arthrobacter sp. served as sorbent for the biosorption studies of arsenite (As+3 ) and arsenate (As+5 ) ions.
2.2.
Reagents for arsenic determination and FT-IR analysis Arsenite (As+3 ) standard (1000 mg/L) stock solution was prepared by dissolving 1.73 g of NaAsO2 in 1.0 L of 0.1% ascorbic acid solution. Similarly, arsenate (As+5 ) standard (1000 mg/L) stock solution was prepared by dissolving 4.16 g of Na2 HAsO4 .7H2 O in 1.0 L of de-ionized water. All of the chemicals were procured from Sigma Chemicals Co. (St. Louis, USA) unless otherwise mentioned. All experiments were done in triplicate and repeated twice to test precision. The data were statistically analysed by means and standard deviation. Speciation of arsenic As+3 and As+5 was carried out in two stages, firstly estimation of total arsenic As(T) followed by arsenite (As+3 ). The quantity of arsenate (As+5 ) was determined by subtracting values of arsenite from total arsenic (As+5 = As(T) – As+3 ). Estimation of arsenic was performed with atomic absorption spectrophotometer-hydride vapour generation (AAS-HVG) (Shimadzu, Japan). Concentrated HCl (5 M) and citric acid (0.1 M) were used for As(T) and As+3 , respectively. Hydride generation (arsine) from total arsenic occurred after reduction of samples with HCl and NaBH4 (pH < 1) while arsine from As+3 was generated by reducing samples with NaBH4 and citric acid (pH ≥ 5). Concentrations of NaBH4 and NaOH were 6.0 g/L and 2.0 g/L, respectively. This pH-dependent generation of arsine was principally used for arsenic speciation. [26] An electrode-less discharge lamp (EDL) was used as a radiation source. Acetylene, air and argon gas were used as a source of fuel, oxidant and carrier gas, respectively. Analysis of arsenic was carried out using the following set-up: wavelength 193.7 nm, band pass 1 nm, lamp current 8.0 mA, flame condition was standard lean flame for hydride analysis, fuel 1.2–1.3 L/min, air minimum flow. Flame conditions were optimized every day before use for maximum sensitivity. Arsenic-loaded biomass for Fourier transform infrared (FT-IR) analysis was prepared by incubating 50 mg of freeze-dried cells with 50 mL of 100 mg/L As+3 at pH 7.0 and As+5 at pH 3.0 for 60 min. A disc of 100 mg KBr containing dried 1% Arthrobacter sp. cells served as the material for recording transmission spectra. Spectra were recorded in the range 400–4000 cm−1 using a FT-IR spectrometer (Spectrum GX, Perkin Elmer, USA) with a resolution of 0.15 cm−1 to evaluate functional groups that might be involved in the sorption process. 2.3. Biosorption optimization The biosorption experiments were carried out at batch scale by adding different amounts of sorbent (biomass) to 50 mL of either As+3 or As+5 buffered solution. Flasks containing a mixture of sorbate and sorbent were placed onto a rotatory orbital shaker operating at 110 rpm until equilibrium time was reached. The solution of sorbate that did not contain bacterial biomass for sorption acted as a blank in this study. An aliquot of sample was collected over an intermittent
Environmental Technology
the biosorption processes. [27] The biosorption of As+5 is at a maximum at pH 3 where 91% of adsorbate was found to be sorbed onto the biomass. However, in an alkaline condition, i.e at pH 9, biosorption was lower at 67% of As+5 . The biosorption yield for As+3 was at a maximum when 88% of the adsorbate was found to be adsorbed at pH 7 (Figure 1(a)). Taking these observations into account, all biosorption experiments were carried out at pH 7 for As+3 and pH 3 for As+5 . A similar trend of sorption of As+3 and As+5 has been observed by several other researchers using different kinds of sorbents. The dominant species of As+5 in 2− the above-mentioned pH range are H2 AsO− 4 and HAsO4 ions, which can be sorbed onto the sorbent by substituting hydroxyl ions or coordination of hydroxyl groups with the sorbate. [28] The predominant monoanionic (H2 AsO− 3 ) and neutral (H3 AsO3 ) species are thus considered to be responsible for the biosorption of As+3 , substituting hydroxyl ions or water molecules. The neutral species (H3 AsO3 ) cannot undergo electrostatic interaction with the adsorbent. However, such species can interact with the unprotonated amino groups. [21] It is evident from Figure 1 that biosorption of arsenic decreases with a further increase in pH. The decrease in arsenic biosorption can be attributed to the competition between the hydroxyl ions, present at higher pH, and arsenic species for biosorption sites. In addition, the carboxyl, hydroxyl and amide groups of the biomass will be negatively charged under alkaline conditions. Development of overall negative charges to molecules of the sorbent builds an environment of repulsion between the negatively charged sorbent and anionic species of arsenic, leading to reduced sorption efficiency. [29] The effect of contact time on biosorption of arsenite and arsenate onto Arthrobacter sp. biomass was studied using biomass doses of 1 g/L and sorbate 100 mg/L at 28◦ C (Figure 1(b)). Sorption of
period followed by filtration using 0.22 μ m filter paper. Finally the prepared sample was preserved in a frozen state, until quantification of arsenic was performed. The optimization for maximum sorption of arsenite and arsenate was tested at various pH ranging from 2 to 10, contact time 5, 10, 15, 30, 45 and 60 min, sorbent concentration 0.25, 0.5, 1.0, 1.5 and 2 g/L, and sorbate concentration 25, 50, 100, 150 and 200 mg/L. The amount of As +3 and As+5 ions sorbed was calculated as a percentage as in Equation (1): Sorption (%) =
(Ci − Cf ) × 100 Ci
(1)
(Ci − Cf )V M
(2)
where Ci and Cf are the initial and final concentrations of As+3 and As+5 ions in the aqueous solution (mg/L), respectively. V is the volume (L) of test solution; and M is the mass of biosorbent (g) used. The pH was kept constant by dissolving sorbate into 20 mM of different buffer solution, i.e. for pH 2 (KCl/HCl), pH 3 (glycine/HCl), pH 4–5 (sodium acetate/acetic acid), pH 6 (citric acid/sodium citrate), pH 7–9 (Tris.Cl) and pH 10 (borax/NaOH) After completion, desorption was carried out by treating the biomass with 20 mL of 0.5 M HCl, 1 M HCl, 0.5 M HNO3 and M HNO3 . 3. Results and discussion 3.1. Effect of pH, contact time and biomass doses The solution pH, which affects the biosorption performance of the biosorbent, is an important controlling parameter in
60
As +5
(a)
90
(c)
55 As +3
85
qe (mg/g)
Biosorption (%)
95
80 75 70
As +3 As +5
50 45
40 35
65
30 0
2
4
6
8
10
0
0.5
pH 90
(b)
1
1.5
2
2.5
Biosorbent(g/L)
60
95
(d)
55
85 50
80
qe (mg/g)
Biosorption (%)
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The biosorption capacity qe is expressed as the amount of As+3 and As+5 ions sorbed per g of sorbent (mg/g), and calculated as follows: qe (mg/g) =
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75 70
As +3 As +5
65 60
45 As +3
40
As +5
35 30
55 0
20
40
Time (min)
60
0
50
100 150 200 250 300 350 400 450
Sorbate(mg/L)
Figure 1. Effect of (a) pH, (b) contact time on biosorption of arsenite and arsenate onto Arthrobacter sp. biomass (metal concentration: 100 mg/L, sorbate concentration: 1 g/L at 28◦ C). Effect of (c) biosorbent Arthrobacter sp. biomass doses and (d) effect of sorbate, arsenite and arsenate concentration on overall biosorption processes at 28◦ C. The error bars represent standard deviations.
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arsenate (85.67%) and arsenite (78.38%) was observed after mixing sorbate and sorbent for a period of 30 min. A lichen biomass is reported to have similar sorption characteristics for removal of arsenite and arsenate. [30] Figure 1(c) shows the pattern for absorption of arsenite and arsenate at different doses of biomass. Data indicates a reduction in sorption of the analyte upon an increase in the amount of biomass beyond 1 g/L. Maximum sorption occurred when 1 g/L of the biomass was subjected to sorption studies. Similarly, an increase in analyte (As+3 and As+5 ) concentration to more than 100 mg/L, when the biomass dose was 1 g/L, did not enhance overall sorption in the batch sorption model (Figure 1(d)). Either an increase in contact time of absorption or an increase in sorbate concentration seems to indicate similar behaviour of the biomass with respect to arsenic uptake. 3.2. FT-IR analysis The FT-IR spectroscopy method was applied to obtain information on the nature of possible biomass–metal ion interactions as presented in Figure 2. The broad and strong bands at 3434 cm−1 were due to bounded hydroxyl (−OH) or amine (−NH) groups in the biomass. Peaks observed at 2926 cm−1 can be assigned to the −CH group of the biomass. Peaks at 1646, 1546 and 1403 cm−1 were attributed to a stretching vibration of the carboxyl group (−C=O). The bands observed at 1083 cm−1 were assigned to C−O stretching of alcohols and carboxylic acids. The asymmetrical stretching vibration at 3434 cm−1 shifted to 3428 and 3433 cm−1 for As+3 - and As+5 -treated biomass. Similarly, the carboxyl peaks at 1645, 1546 and 1453 cm−1 shifted to 1640 and 1456 cm−1 for As+3 -treated and 1650, 1548 and 1452 cm−1 for As+5 -treated biomass, respectively. The peak of the C−O group at 1083 cm−1 shifted to 1081 and 1079 cm−1 for As+3 - and As+5 -treated biomass. The results indicated the involvement of carboxyl
(−COOH), hydroxyl (−OH) and amine (−NH) groups in the biosorption of As+3 and As+5 onto Arthrobacter sp. biomass. The peak shift in the fingerprint region, i.e. 554– 600 cm−1 for As+3 and 616 cm−1 for As+5 indicated the involvement of aromatic amino acids during biosorption of arsenic. Peaks at 794 cm−1 for As+3 and 846 and 740 cm−1 for As+5 -treated biomass appeared in addition to the control. According to Gadsden [31] and Niua et al. [32], these two peaks are characteristic of inorganic arsenic compounds in the biomass. 3.3. Adsorption isotherms The distribution of metal ions between the liquid phase and biosorbent in the equilibrium adsorption process can be described by several isotherms, based on a set of assumptions related to the heterogeneity or homogeneity of adsorbents, the type of coverage and the possibility of interaction between the adsorbent species. The biosorption isotherms were investigated using three equilibrium models, namely the Langmuir, Freundlich and DubininRadushkevich (D-R) isotherm models. The Langmuir sorption isotherm is most widely used isotherm model for the biosorption of a solute from a liquid solution. The Langmuir model assumes that the uptake of metal ions on to a solid is a monolayer adsorption process, without any interaction between sorbed ions. Langmuir isotherm can be defined according to the following formula: qe =
q m KL C e 1 + K L Ce
(3)
where qe is the equilibrium metal ion concentration on the adsorbent (mg/g), Ce is the equilibrium metal ion concentration in the solution (mg/L), qm is the monolayer biosorption capacity of the adsorbent (mg/g) and KL is the Langmuir biosorption constant (L/mg), relating to the
Figure 2. Fourier transform infrared spectroscopy (FT-IR) spectra of (a) untreated, (b) As+3 -treated and (c) As+5 -treated Arthrobacter sp. biomass.
free energy of biosorption. Figure 3(a), indicates the nonlinear relationship between the quantity (mg) of As+3 and As+5 ions sorbed per unit mass (g) of Arthrobacter sp. biomass. The coefficients of determination (R2 ) were found to be 0.9568 for As+3 and 0.964 As+5 biosorption. These results indicate that the biosorption of the metal ions onto the isolate biomass fitted well with the Langmuir model. It can be assumed that the sorption of As+3 and As+5 ions occurred due to involvement of functional groups or binding sites present on the surface of the biomass, a monolayer biosorption. The maximum biosorption capacity (qm ) of isolate biomass was found to be 74.91 mg/g for As+3 and 81.63 mg/g for As+5 . The KL value was calculated as 0.019 L/mg for As+3 and 0.017 L/mg for As+5 biosorption. The biosorption capacity (qm , mg/g) of the isolate biomass for As+3 and As+5 ions with respect to various other biosorbents is presented in Table 1. The sorption capacity of Arthrobacter sp.15b isolate biomass for As+3 and As+5 was found to be higher than for the majority of other biosorbents reported in the literature. The Freundlich model assumes a heterogeneous adsorption surface and active sites with different energy. This isotherm can be explained by following formula: qe =
Kf Ce1/n
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intensity, which varies with the heterogeneity of the material. A Freundlich isotherm was obtained by plotting qe vs. Ce values, which showed a nonlinear relationship between the two (Figure 3(b)). Values of Kf and 1/n were found to be 3.1 and 0.47 for As+3 and 3.05 and 0.49 for As+5 biosorption, respectively. The 1/n values, between 0 and 1, indicate that the biosorption of As+3 and As+5 onto the isolate biomass was favourable under the studied conditions. However, the R2 value was 0.906 for As+3 and 0.917 for As+5 biosorption. These results suggested that the Freundlich model was not able to describe adequately the relationship between the amounts of sorbed metal ions and their equilibrium concentration in the solution. The Langmuir isotherm model best fitted the equilibrium data since it presented a higher R2 value than the Freundlich model. The physical or chemical natures of biosorption processes were studied by analysing the equilibrium data using the D-R isotherm model. The linear form of the D-R isotherm model is presented by the following equation: ln qe = ln qm − βε 2
(5)
where qe is the amount of metal ions adsorbed on per unit weight of biomass (mg/g) , qm is the maximum biosorption capacity (mg/g) , β is the activity coefficient related to mean biosorption energy (mol2 /J2 ) and ε is the Polanyi potential (ε = RT ln(1 + 1/Ce ). The D-R isotherm model
(4)
where Kf is a constant relating the biosorption capacity and 1/n is an empirical parameter relating to biosorption 100
(a)
90 80
qe (mg/g)
70 60
ε 2 × 10 8 (J2/mol 2)
50 40
1.5 -7
As +3
30
-7.5
As +5
10 0 0
50
100
150
200
250
Ce (mg/L) 100
(b)
90
ln qe (mol/g)
20
3.5
5.5
(c)
7.5 As +3 As +5
-8 -8.5 -9 -9.5 -10
80
-10.5
70
qe (mg/g)
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Environmental Technology
-11
60 50
K
40 30
As +3
20
As +5
10 0 0
50
100
150
200
250
Ce (mg/L)
Figure 3. (a) Langmuir isotherm plots for biosorption of arsenite and arsenate onto Arthrobacter sp.15b biomass. (b) Freundlich isotherm plots for biosorption of arsenite and arsenate onto Arthrobacter sp.15b biomass. (c) Dubinin-Radushkevich (D-R) isotherm plots for biosorption of arsenite and arsenate onto Arthrobacter sp. biomass. In all cases, biomass dosages 1 g/L; contact time 30 min; pH 7 for As+3 ; pH 3 for As+5 ; temperature 28◦ C). The error bars represent standard deviations.
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Adsorbent/biosorbent
As+3
pH
As+5
pH
References
Zr(IV)-loaded LDA chelating agent Fe(III)-treated biomass (Staphylococcus xylosus) Powder of stem of Acacia nilotica Lichen (Xanthoria parietina) Macrofungus (Inonotus hispidus) Fungal biomass (Penicillium purpurogenum) Phosphorylated orange waste (POW) Green algae (Ulothrix cylindricum) Bacterial biomass (Arthrobacter sp.)
49.15 54.35 – 63.8 51.9 35.6 70.43 67.2 74.91
9 7 – 6 6 5 8 6 7
88.73 61.34 50.8 60.3 59.6 – 67.43 – 81.63
4 3 7.5 – 2 – 2 – 3
Balaji et al. [11] Aryal et al. [21] Baig et al. [12] Sari and Tuzen [30] Sari and Tuzen [29] Say et al. [8] Ghimire et al. [13] Tuzen et al. [35] Present study
1 E=√ −2β
2
3.4. Biosorption kinetic models In order to evaluate biosorption dynamics, kinetic constants can be used to optimize the residence time of a biosorption process. Pseudo-first-order and pseudo-second-order kinetic models were used to analyse the sorption rate of As +3 and As+5 on Arthrobacter sp. biomass. The pseudo-first order rate equation is given as log qe − k1 t log(qe − qt ) = (7) 2.303 where qe (mg/g) is the amount of metal ions sorbed at equilibrium, qt is the amount of metal sorbed at any time (mg/g) and k1 is the rate constant of the equation (min−1 ). The biosorption rate constant k1 can be determined experimentally by plotting log(qe − qt ) vs. t. Experimental data were also tested with the pseudo-second-order equation [33] t 1 1 t (8) = + 2 qt k2 q e qe where k2 is the equilibrium rate constant (g/mg/min). Both of these kinetic models are presented in Figure 4(a)
y = -0.0409x + 1.5709 R² = 0.8166 As +3
1.6 1.4
As +5
1.2 1
Linear (As +3)
0.8
Linear (As +5)
0.6 0.4
(6)
The adsorption process is regarded as being chemical in nature when values lie between 8 and 16 kJ/mol, similarly adsorption is physical in nature when the value of E is less than 8 kJ/mol. [29] The mean biosorption energy was calculated as 10.10 and 10.85 kJ/mol for the biosorption of As+3 and As+5 ions, respectively. Biosorption processes of both metal ions onto Arthrobacter sp. biomass occurred due to a chemical ion-exchange mechanism, since the sorption energies lay within 8–16 kJ/mol.
(a)
1.8
log (qe-qt )
well fitted the equilibrium data since the R2 value was found to be 0.9931 and 0.9922 for As+3 and As+5 , respectively (Figure 3(c)). The qm value was found using the intercept of the plots as 1.29 × 10−3 and 1.13 × 10−3 mol/g for As+3 and As+5 , respectively. The biosorption mean free energy (E, kJ/mol) gives information about the nature of adsorption, i.e. physical or chemical. The mean biosorption energy (E, kJ/mol) is expressed as follows:
y = -0.0326x + 1.4271 R ² = 0.8406
0.2 0 0
10
20
30
40
50
Time (min) 30 (b)
25 y = 0.5585x + 0.7323 R ² = 0.9935
20
t/q t
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Table 1. Comparative evaluation of biosorption capacity (mg/g) of Arthrobacter sp. for As+3 and As+5 with different biosorbency for arsenic removal.
15
As +3 As +5
10
Linear (As +3) Linear (As +5) y = 0.5038x + 0.5437 R ² = 0.9934
5 0 0
10
20
30
40
50
Time (min) Figure 4. Biosorption kinetic models for metals uptake. (a) Pseudo-first-order model for As+3 and As+5 ; (b) pseudo-second-order model for As+3 and As+5 . The error bars represent standard deviations.
and (b), whereas different rate constants are shown in Table 2. The values of correlation coefficient of the pseudosecond-order model were found to be 0.9935 for As+3 and 0.9934 for As+5 , which is higher than the pseudofirst-order-model, i.e. 0.8166 and 0.8406. Compared to the pseudo-first-order equation, the pseudo-second-order model can explain the biosorption kinetic behaviour of As+3 and As+5 onto Arthrobacter sp. biomass satisfactorily with a good correlation coefficient.
Environmental Technology Table 2. Kinetic parameters for biosorption of As+3 or As+5 onto Arthrobacter sp.
Arsenic As+3 As+5
8 7.8
Pseudo-second-order
7.6 7.4
K1 (min−1 )
R21
K2 (g/mg min)
R22
0.0115 0.0179
0.8166 0.8404
0.00906 0.00921
0.9935 0.9934
ln K D
Pseudo-first-order
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y = 2.8095x - 2.0345 R² = 0.9913
7.2 7 As +3
6.8 y = 1.7125x +1.2008 6.6
Table 3. Influence of various eluents on the desorption of As+3 and As+5 from Arthrobacter sp.
6.4
3
Recovery (%)
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Eluent 0.5 M HCl 1 M HCl 0.5 M HNO3 1 M HNO3
As+3
As+5
78.35 ± 4.21 91.17 ± 4.85 65.52 ± 4.13 72.46 ± 3.89
68.27 ± 3.52 88.56 ± 4.21 56.81 ± 3.46 66.39 ± 3.65
3.1
3.2
3.3
3.4
3.5
3.6
10–3 (1/T), K –1
Figure 5. Plot of ln KD vs. 1/T for the estimation of thermodynamic parameters for biosorption of arsenite and arsenate onto Arthrobacter sp. biomass. The error bars represent standard deviations.
Data are means ± standard deviations.
3.5. Desorption efficiency Desorption of adsorbed ions onto Arthrobacter sp. was carried out by using different concentrations of HCl and HNO3 . Recovery of adsorbed metal ions from the biomass is shown in Table 3. The highest recovery was found to be 91.17% for As+3 and 88.56% for As+5 using 1 M HCl, whereas 1 M HNO3 could release 72.46% of As+3 and 66.39% of As+5 . The study suggests that 1 M HCl readily stripped off the sorbed metal ions from isolate biomass. In addition, the high stability of Arthrobacter sp. biomass permitted operation of the adsorption-elution process 10 times with a decrease of about 18–25% recovery of As+3 and 26–35% for As+5 . 3.6. Biosorption thermodynamics Thermodynamic behaviour of the biosorption of As+3 and As+5 ions onto Arthrobacter sp. biomass, and thermodynamic parameters including the change in free energy (G ◦ ), enthalpy (H ◦ ) and entropy (S ◦ ) have been studied. The change in free energy (G ◦ ) was calculated from the following equation: G ◦ = −RT ln KD
As +5
R² = 0.9916
(9)
where R is the universal gas constant (8.314 J/mol K), T is temperature (K) and KD (qe /Ce ) is the distribution coefficient. The enthalpy (H ◦ ) and entropy (S ◦ ) parameters were estimated from the following equation: ◦ H ◦ S − (10) ln KD = T RT The H ◦ and S ◦ were calculated from the slope and intercept of the plot of ln KD versus 1/T yields [34] and shown in Figure 5. Gibbs free energy change (G ◦ ) was found to be −19.42, −19.11, −18.75 and −18.23 kJ/mol
for As+3 biosorption and −18.83, −18.46, −18.19 and −17.99 kJ/mol for the biosorption of As+5 at 20, 30, 40 and 50◦ C, respectively. The negative G ◦ values indicated the thermodynamically feasible and spontaneous nature of the biosorption. The decrease in G ◦ values with an increase in temperature suggested a lesser feasibility of biosorption at high temperatures. The enthalpy of biosorption H ◦ parameter was found to be −23.42 and −26.75 kJ/mol for As+3 and As+5 biosorption, respectively. The negative H ◦ indicates the exothermic nature of biosorption at 20 to 50◦ C. The enthalpy or the heat of biosorption ranging from 2.1–20.9 KJ/mol corresponds to physical sorption, whereas ranging from 20.9–418 KJ/mol is regarded as chemical sorption. [35] Therefore the H ◦ value suggests that the biosorption process of As+3 and As+5 on Arthrobacter sp. biomass occurred due to chemisorption. The S ◦ parameter was found to be −16.49 J/mol K for As+3 biosorption and −27.34 J/mol K for As+5 biosorption. The negative S ◦ value suggested a decrease in the randomness at the solid/solution interface during the biosorption process. 4. Conclusions The biosorption capacity of Arthrobacter sp. biomass was found to be 74.91 for As+3 and 81.63 mg/g for As+5 at optimal experimental conditions. Sorption of arsenite as well as arsenate onto bacterial biomass is found to be higher than that of previously studied biomass. The mean free energy values evaluated from the D-R isotherm model indicates that biosorption primarily occurred due to the ion-exchange behaviour of freeze-dried cells. The absorption pattern fitted well with the Langmuir model and followed pseudo-second-order kinetics. FT-IR analysis indicated involvement of functional groups (−OH, −NH, −C=O and −COO−) during biosorption processes. Regeneration properties of biomass further suggests its potential for development into a filtration system for removal of contamination of arsenic from aqueous solution. To the best of
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our knowledge, the present study for the first time reported a detailed study of sorption kinetics of As+3 and As+5 by Gram-positive arsenic-resistant Arthrobacter sp. isolate.
Acknowledgements KSP is thankful to the Council of Scientific and Industrial Research, India, New Delhi for the PhD grant. The first author is also grateful to Dr CL Patel, Chairman, Chautar Vidyamandal and SICART (Sophisticated Instrumentation Centre for Applied Research and Testing) Anand, Gujarat for analysis of samples. JP is thankful to University Grant Commission, New Delhi, for financial support.
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References [1] Twarakavi NKC, Kaluarachchi JJ. Arsenic in the shallow ground waters of conterminous United States: assessment, health risks, and costs for MCL compliance. J Am Water Resour Assoc. 2006;42:275–294. [2] Milton AH, Hasan Z, Rahman A, Rahman M. Chronic arsenic poisoning and respiratory effects in Bangladesh. J Occup Health. 2001;43:136–140. [3] Polizzotto ML, Kocar BD, Benner SG, Sampson M, Fendorf S. Near-surface wetland sediments as a source of arsenic release to ground water in Asia. Nature. 2008;454:505–508. [4] Bates MN, Smith AH, Hopenhayn-Rich C. Arsenic ingestion and internal cancers: a review. Am J Epidemiol. 1992;135:462–476. [5] Malik AH, Khan ZM, Mahmood Q, Nasreen S, Ahmed Bhatti Z. Perspectives of low cost arsenic remediation of drinking water in Pakistan and other countries. J Hazard Mater. 2009;168:1–12. [6] Nriagu JO. Arsenic poisoning through the ages. In: Frankenberger WT Jr., editor. Environmental chemistry of arsenic. New York: Marcel Dekker; 2001. p. 1–26. [7] Mohan D, Pittman CU Jr. Arsenic removal from water/wastewater using adsorbents-a critical review. J Hazard Mater. 2007;142:1–53. [8] Say R, Yilmaz N, Denizli A. Biosorption of cadmium, lead, mercury and arsenic ions by the fungus Penicillium purpurogenum. Sep Sci Technol. 2003;38:2039–2053. [9] Maheswari S, Murugesan AG. Biosorption of As(III) ions from aqueous solution using dry, heat-treated and NaOH-treated Aspergillus nidulans. Environ Technol. 2011;32:211–219. [10] Maheswari S, Murugesan AG. Remediation of arsenic in soil by Aspergillus nidulans isolated from an arseniccontaminated site. Environ Technol. 2009;30:921–926. [11] Balaji T, Yokoyama T, Matsunaga H. Adsorption and removal of As(V) and As(III) using Zr-loaded lysine diacetic acid chelating resin. Chemosphere. 2005;59:1169–1174. [12] Baig JA, Kazi TG, Shah AQ, Kandhro GA, Afridi HI, Khan S, Kolachi NFJ. Biosorption studies on powder of stem of Acacia nilotica: removal of arsenic from surface water. J Hazard Mater. 2010;178:941–948. [13] Ghimire KN, Inoue K, Makino K, Miyajima T. Adsorptive removal of arsenic using orange juice residue. Sep Sci Technol. 2002;37:2785–2799. [14] Biswas BK, Inoue JIK, Ghimire KN, Harada H, Ohto K, Kawakita H. Adsorptive removal of As(V) and As(III) from water by a Zr(IV)-loaded orange waste gel. J Hazard Mater. 2008;154:1066–1074. [15] Ahmann D, Roberts AL, Krumholz LR, Morel FM. Microbe grows by reducing arsenic. Nature. 1994;371:750.
[16] Katsoyiannis IA, Zouboulis AI. Application of biological processes for the removal of arsenic from ground waters. Water Res. 2004;38:17–26. [17] Simeonova DD, Micheva K, Muller DAE, Lagarde F, Lett MC, Groudeva VI, Lièvremont D. Arsenite oxidation in batch reactors with alginate-immobilized ULPAs1 strain. Biotechnol Bioeng. 2005;91:441–446. [18] Wang S, Zhao X. On the potential of biological treatment for arsenic contaminated soils and groundwater. J Environ Manage. 2009;90:2367–2376. [19] Teclu D, Tivchev G, Laing M, Wallis M. Bioremoval of arsenic species from contaminated waters by sulphatereducing bacteria. Water Res. 2008;42:4885–4893. [20] Lei Y, Yin H, Zhang S, Leng F, Nan W, Li H. Biosorption of inorganic and organic arsenic from aqueous solution by Acidithiobacillus ferrooxidans BY-3. J Hazard Mater. 2010;178:209–217. [21] Aryal M, Ziagova M, Kyriakides ML. Study on arsenic biosorption using Fe(III)- treated biomass of Staphylococcus xylosus. Chem Eng J. 2010;162:178–185. [22] Prasad KS, Srivastava P, Subramanian V, Paul J. Biosorption of As(III) ion on Rhodococcus sp.WB-12: biomass characterization and kinetic studies. Sep Sci Technol. 2011;46:2517–2525. [23] Pagnanelli F, Papini MP, Toro L, Trifoni M, Vegliò F. Biosorption of metal ions on Arthrobacter sp.: biomass characterization and biosorption modeling. Environ Sci Technol. 2000;34:2773–2778. [24] Prasad KS, Subramanian V, Paul J. Purification and characterization of arsenite oxidase from Arthrobacter sp. Biometals. 2009;22:711–721. [25] Chubar N, Behrends T, Cappellen PV. Biosorption of metals (Cu2+ , Zn2+ ) and anions (F− , H2 PO− 4 ) by viable and autoclaved cells of the Gram-negative bacterium Shewanella putrefaciens. Colloid Surf B. 2008;65:126–133. [26] Maity S, Chakravarty S, Thakur P, Gupta KK, Bhattacharjee S, Roy BC. Evaluation and standardization of a simple HGAAS method for rapid speciation of As (III) and As (V) in some contaminated groundwater samples of West Bengal, India. Chemosphere. 2004;54:1199–1206. [27] Volesky B. Biosorption of heavy metals. Boca Raton: CRC Press; 1990. [28] Boddu VM, Abburib K, Talbottc JL, Smitha ED, Haaschd R. Removal of arsenic (III) and arsenic (V) from aqueous medium using chitosan-coated biosorbent. Water Res. 2008;42:633–642. [29] Sarı A, Tuzen M. Biosorption of As(III) and As(V) from aqueous solution by macrofungus (Inonotus hispidus) biomass: equilibrium and kinetic studies. J Hazard Mater. 2009;164:1372–1378. [30] Sarı A, Tuzen M. Biosorption of As(III) and As(V) from aqueous solution by lichen (Xanthoria parietina) biomass. Sep Sci Technol. 2010;45:463–471. [31] Gadsden JA. Infrared spectra of minerals and related inorganic compounds. London: Butterworths; 1975, p.180. [32] Niua CH, Volesky B, Daniel C. Biosorption of arsenic (V) with acid-washed crab shells. Water Res. 2007;41:2473– 2478. [33] Ho YS, McKay G. Pseudo-second order model for sorption processes. Process Biochem. 1999;34:451–465. [34] Ranjan D, Talat M, Hasan SH. Biosorption of arsenic from aqueous solution using agricultural residue ‘rice polish’. J Hazard Mater. 2009;166:1050–1059. [35] Tuzen M, Sarı A, Mendil D, Uluozlu OD, Soylak M, Dogan M. Characterization of biosorption process of As(III) on green algae Ulothrix cylindricum. J Hazard Mater. 2009;165:566–572.
Environmental Technology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tent20
+3
+5
Biosorption of arsenite (As ) and arsenate (As ) from aqueous solution by Arthrobacter sp. biomass ab
a
c
a
Kumar Suranjit Prasad , A. L. Ramanathan , Jaishree Paul , Vaidyanathan Subramanian & d
Ram Prasad a
School of Environmental Sciences, Jawaharlal Nehru University, New Delhi, India
b
Department of Environmental Biotechnology, ARIBASSardar Patel University, New Vallabh Vidyanagar, Anand, Gujarat, India c
School of Life sciences, Jawaharlal Nehru University, New Delhi, India
d
Amity Institute of Microbial Technology, Amity University, Noida, India Accepted author version posted online: 25 Mar 2013.Published online: 29 Apr 2013.
To cite this article: Kumar Suranjit Prasad, A. L. Ramanathan, Jaishree Paul, Vaidyanathan Subramanian & Ram Prasad +3
+5
(2013) Biosorption of arsenite (As ) and arsenate (As ) from aqueous solution by Arthrobacter sp. biomass, Environmental Technology, 34:19, 2701-2708, DOI: 10.1080/09593330.2013.786137 To link to this article: http://dx.doi.org/10.1080/09593330.2013.786137
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Environmental Technology, 2013 Vol. 34, No. 19, 2701–2708, http://dx.doi.org/10.1080/09593330.2013.786137
Biosorption of arsenite (As+3 ) and arsenate (As+5 ) from aqueous solution by Arthrobacter sp. biomass Kumar Suranjit Prasada,b∗ , A.L. Ramanathana , Jaishree Paulc , Vaidyanathan Subramaniana and Ram Prasadd a School
of Environmental Sciences, Jawaharlal Nehru University, New Delhi, India; b Department of Environmental Biotechnology, ARIBAS, Sardar Patel University, New Vallabh Vidyanagar, Anand, Gujarat, India; c School of Life sciences, Jawaharlal Nehru University, New Delhi, India; d Amity Institute of Microbial Technology, Amity University, Noida, India
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(Received 19 August 2012; final version received 8 March 2013 ) In this study we investigated the role of arsenic-resistant bacteria Arthrobacter sp. biomass for removal of arsenite as well as arsenate from aqueous solution. The biomass sorption characteristics were studied as a function of biomass dose, contact time and pH. Langmuir, Freundlich and Dubinin-Radushkevich (D-R) models were applied to describe the biosorption isotherm. The Langmuir model fitted the equilibrium data better than the Freundlich isotherm. The biosorption capacity of the biomass for As+3 and As+5 was found to be 74.91 mg/g (pH 7.0) and 81.63 mg/g (pH 3.0), respectively using 1 g/L biomass with a contact time of 30 min at 28◦ C. The mean sorption energy values calculated from the D-R model indicated that the biosorption of As+3 and As+5 onto Arthrobacter sp. biomass took place by chemical ion-exchange. The thermodynamic parameters showed that the biosorption of As+3 and As+5 ions onto Arthrobacter sp. biomass was feasible, spontaneous and exothermic in nature. Kinetic evaluation of experimental data showed that biosorption of As+3 and As+5 followed pseudo-second-order kinetics. Fourier transform infrared spectroscopy (FT-IR) analysis indicated the involvement of possible functional groups (−OH, −C=O and −NH) in the As+3 and As+5 biosorption process. Bacterial cell biomass can be used as a biosorbent for removal of arsenic from arsenic-contaminated water. Keywords: arsenite; arsenate; biosorption; bioremediation; FT-IR spectroscopy; kinetics
1. Introduction Worldwide reports of subsurface water contamination with arsenic have become a serious public health-related issue. Unfortunately, the severity of this problem has been mainly noticed in developing countries, e.g. the eastern part of India and Bangladesh, Nepal, Inner Mongolia, Cambodia, Thailand, Argentina and Chile, and also in developed nations such as the USA. [1] In and around India in areas such as East Bengal and West Bengal and some areas of North Bihar (Gangatic plain), over 40 million people are being exposed to more than 50 ppb of arsenic whereas, according to the Environmental Protection Agency, the limit is set at 10 ppb. Out of 4 million tube wells in Bangladesh, 1.2 million have been found to contain more than 50 ppb of arsenic and 7600 people are afflicted with chronic arsenicosis. [2] In these developing countries more than 10 ppb of arsenic is still being consumed due to a lack of alternate access to water. [3] Studies have demonstrated an association between high levels of arsenic in drinking water with a significant increase in the risk of cancer for the affected population. [4] Two forms of arsenic are commonly present in natural water, i.e. 3− +3 arsenite (AsO3− 3 ) and arsenate (AsO4 ), referred to As
∗ Corresponding
author. Email: [email protected]
© 2013 Taylor & Francis
and As+5 , respectively. Pentavalent species mostly predominate and are stable in oxidizing aerobic environments such as surface water and shallow ground water, while trivalent arsenite predominates in moderately reducing anaerobic environments such as deep-seated groundwater. [5] Besides the natural phenomenon of release of arsenic due to weathering of rocks and volcanic activity, various anthropogenic activities such as use of pesticides, wood preservatives, dye stuffs and other chemicals containing arsenic are the major sources of water contamination. [6] Numerous materials have been tested for removal of toxic ions from aqueous solutions over the last two decades. [7] However, only a limited number of studies have investigated the use of adsorbents obtained from biological sources, e.g. Penicillium sp., [8] Aspergillus nidulans, [9, 10] Zr-loaded diacetic acid chelating resin, [11] Acacia nilotica, [12] orange juice residue [13] and Zr(IV) loaded orange waste [14] for arsenic removal. Metals are generally non-biodegradable, but can be transformed through sorption, methylation, complexation and by changes in their valence state. These transformations affect the mobility and bioavailability of metals. Microorganisms that affect the
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reactivity and mobility of metals can be used to detoxify some metals and prevent further metal contamination. [15] Katsoyiannis and Zouboulis [16] conducted studies with iron-oxidizing bacteria for removing both arsenite and arsenate. The results indicate that both forms of arsenic could be efficiently removed to an acceptable level of concentration, i.e. less than 10 ppb. This removal was related to a combination of the oxidation of As+3 to As+5 and biosorption of arsenic to the microorganisms. In another experiment, strain ULPAs1, an arsenite oxidizer, was entrapped into calcium alginate beads and investigations were carried out upon oxidation as well as removal of arsenic from growth media. [17] Anaerobic microbial mobilization and biotransformation of arsenate adsorbed onto activated alumina has been studied. [18] The role of sulphate-reducing bacteria for removal of arsenic has also been examined. [19] Recently, studies related to biosorption of arsenic from aqueous solution by Acidithiobacillus ferrooxidans BY-3, [20] Staphylococcus xylosus [21] and Rhodococcus sp.WB-12 [22] have been carried out. Pagnanelli et al. [23] studied biosorption of metals copper, cadmium and iron ions on Arthrobacter sp. biomass. The Arthrobacter sp. is a gram-positive bacterium possessing arsenite oxidizing ability using a membrane-bound enzyme, arsenite oxidase. [24] The Gram-positive bacterial cell wall is thicker than the cell wall of Gram-negative bacteria and harbours a greater number of functional groups that may act as sorption sites for varieties of aqueous chemical species. [25] The present study is an attempt to determine the utility of an Arthrobacter sp. biomass by studying its biosorption characteristics for As+3 and As+5 .
2. Materials and methods 2.1. Biomass preparation The isolate Arthrobacter sp. was inoculated into minimal culture media (MM1). The composition of minimal media is (g/L): (NH4 )2 SO4 , 1.0 g; KH2 PO4 , 0.5 g; KCl, 0.05 g; Ca(NO3 )2 , 0.1 g; NaHCO3 , 0.5 g and 0.04% (w/v) yeast extract. One mL of trace element solution was added to 1 L of culture medium followed by final adjustment of pH to 7.8. Incubation of culture was carried out by placing a culture flask onto an orbital rotatory shaker (Kuhner AG, Switzerland), operating at 220 rpm for 16 h at 28◦ C. Bacterial cells cultured in MM1 were centrifuged at 5000 rpm for 5 min at 4◦ C. Cells were harvested in their log phase when optical density of culture broth reached 0.35 at a wavelength of 600 nm. Pellets were washed with milliQ water for removal of contaminating components that may occur in the culture medium. Cells were heat-killed using an autoclave and resuspended in milliQ followed by freeze-drying using lyophilizer (Labconco, Kansas, USA). Freeze-dried nonviable cells of Arthrobacter sp. served as sorbent for the biosorption studies of arsenite (As+3 ) and arsenate (As+5 ) ions.
2.2.
Reagents for arsenic determination and FT-IR analysis Arsenite (As+3 ) standard (1000 mg/L) stock solution was prepared by dissolving 1.73 g of NaAsO2 in 1.0 L of 0.1% ascorbic acid solution. Similarly, arsenate (As+5 ) standard (1000 mg/L) stock solution was prepared by dissolving 4.16 g of Na2 HAsO4 .7H2 O in 1.0 L of de-ionized water. All of the chemicals were procured from Sigma Chemicals Co. (St. Louis, USA) unless otherwise mentioned. All experiments were done in triplicate and repeated twice to test precision. The data were statistically analysed by means and standard deviation. Speciation of arsenic As+3 and As+5 was carried out in two stages, firstly estimation of total arsenic As(T) followed by arsenite (As+3 ). The quantity of arsenate (As+5 ) was determined by subtracting values of arsenite from total arsenic (As+5 = As(T) – As+3 ). Estimation of arsenic was performed with atomic absorption spectrophotometer-hydride vapour generation (AAS-HVG) (Shimadzu, Japan). Concentrated HCl (5 M) and citric acid (0.1 M) were used for As(T) and As+3 , respectively. Hydride generation (arsine) from total arsenic occurred after reduction of samples with HCl and NaBH4 (pH < 1) while arsine from As+3 was generated by reducing samples with NaBH4 and citric acid (pH ≥ 5). Concentrations of NaBH4 and NaOH were 6.0 g/L and 2.0 g/L, respectively. This pH-dependent generation of arsine was principally used for arsenic speciation. [26] An electrode-less discharge lamp (EDL) was used as a radiation source. Acetylene, air and argon gas were used as a source of fuel, oxidant and carrier gas, respectively. Analysis of arsenic was carried out using the following set-up: wavelength 193.7 nm, band pass 1 nm, lamp current 8.0 mA, flame condition was standard lean flame for hydride analysis, fuel 1.2–1.3 L/min, air minimum flow. Flame conditions were optimized every day before use for maximum sensitivity. Arsenic-loaded biomass for Fourier transform infrared (FT-IR) analysis was prepared by incubating 50 mg of freeze-dried cells with 50 mL of 100 mg/L As+3 at pH 7.0 and As+5 at pH 3.0 for 60 min. A disc of 100 mg KBr containing dried 1% Arthrobacter sp. cells served as the material for recording transmission spectra. Spectra were recorded in the range 400–4000 cm−1 using a FT-IR spectrometer (Spectrum GX, Perkin Elmer, USA) with a resolution of 0.15 cm−1 to evaluate functional groups that might be involved in the sorption process. 2.3. Biosorption optimization The biosorption experiments were carried out at batch scale by adding different amounts of sorbent (biomass) to 50 mL of either As+3 or As+5 buffered solution. Flasks containing a mixture of sorbate and sorbent were placed onto a rotatory orbital shaker operating at 110 rpm until equilibrium time was reached. The solution of sorbate that did not contain bacterial biomass for sorption acted as a blank in this study. An aliquot of sample was collected over an intermittent
Environmental Technology
the biosorption processes. [27] The biosorption of As+5 is at a maximum at pH 3 where 91% of adsorbate was found to be sorbed onto the biomass. However, in an alkaline condition, i.e at pH 9, biosorption was lower at 67% of As+5 . The biosorption yield for As+3 was at a maximum when 88% of the adsorbate was found to be adsorbed at pH 7 (Figure 1(a)). Taking these observations into account, all biosorption experiments were carried out at pH 7 for As+3 and pH 3 for As+5 . A similar trend of sorption of As+3 and As+5 has been observed by several other researchers using different kinds of sorbents. The dominant species of As+5 in 2− the above-mentioned pH range are H2 AsO− 4 and HAsO4 ions, which can be sorbed onto the sorbent by substituting hydroxyl ions or coordination of hydroxyl groups with the sorbate. [28] The predominant monoanionic (H2 AsO− 3 ) and neutral (H3 AsO3 ) species are thus considered to be responsible for the biosorption of As+3 , substituting hydroxyl ions or water molecules. The neutral species (H3 AsO3 ) cannot undergo electrostatic interaction with the adsorbent. However, such species can interact with the unprotonated amino groups. [21] It is evident from Figure 1 that biosorption of arsenic decreases with a further increase in pH. The decrease in arsenic biosorption can be attributed to the competition between the hydroxyl ions, present at higher pH, and arsenic species for biosorption sites. In addition, the carboxyl, hydroxyl and amide groups of the biomass will be negatively charged under alkaline conditions. Development of overall negative charges to molecules of the sorbent builds an environment of repulsion between the negatively charged sorbent and anionic species of arsenic, leading to reduced sorption efficiency. [29] The effect of contact time on biosorption of arsenite and arsenate onto Arthrobacter sp. biomass was studied using biomass doses of 1 g/L and sorbate 100 mg/L at 28◦ C (Figure 1(b)). Sorption of
period followed by filtration using 0.22 μ m filter paper. Finally the prepared sample was preserved in a frozen state, until quantification of arsenic was performed. The optimization for maximum sorption of arsenite and arsenate was tested at various pH ranging from 2 to 10, contact time 5, 10, 15, 30, 45 and 60 min, sorbent concentration 0.25, 0.5, 1.0, 1.5 and 2 g/L, and sorbate concentration 25, 50, 100, 150 and 200 mg/L. The amount of As +3 and As+5 ions sorbed was calculated as a percentage as in Equation (1): Sorption (%) =
(Ci − Cf ) × 100 Ci
(1)
(Ci − Cf )V M
(2)
where Ci and Cf are the initial and final concentrations of As+3 and As+5 ions in the aqueous solution (mg/L), respectively. V is the volume (L) of test solution; and M is the mass of biosorbent (g) used. The pH was kept constant by dissolving sorbate into 20 mM of different buffer solution, i.e. for pH 2 (KCl/HCl), pH 3 (glycine/HCl), pH 4–5 (sodium acetate/acetic acid), pH 6 (citric acid/sodium citrate), pH 7–9 (Tris.Cl) and pH 10 (borax/NaOH) After completion, desorption was carried out by treating the biomass with 20 mL of 0.5 M HCl, 1 M HCl, 0.5 M HNO3 and M HNO3 . 3. Results and discussion 3.1. Effect of pH, contact time and biomass doses The solution pH, which affects the biosorption performance of the biosorbent, is an important controlling parameter in
60
As +5
(a)
90
(c)
55 As +3
85
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Biosorption (%)
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As +3 As +5
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40 35
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30 0
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4
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0
0.5
pH 90
(b)
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(d)
55
85 50
80
qe (mg/g)
Biosorption (%)
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The biosorption capacity qe is expressed as the amount of As+3 and As+5 ions sorbed per g of sorbent (mg/g), and calculated as follows: qe (mg/g) =
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75 70
As +3 As +5
65 60
45 As +3
40
As +5
35 30
55 0
20
40
Time (min)
60
0
50
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Sorbate(mg/L)
Figure 1. Effect of (a) pH, (b) contact time on biosorption of arsenite and arsenate onto Arthrobacter sp. biomass (metal concentration: 100 mg/L, sorbate concentration: 1 g/L at 28◦ C). Effect of (c) biosorbent Arthrobacter sp. biomass doses and (d) effect of sorbate, arsenite and arsenate concentration on overall biosorption processes at 28◦ C. The error bars represent standard deviations.
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arsenate (85.67%) and arsenite (78.38%) was observed after mixing sorbate and sorbent for a period of 30 min. A lichen biomass is reported to have similar sorption characteristics for removal of arsenite and arsenate. [30] Figure 1(c) shows the pattern for absorption of arsenite and arsenate at different doses of biomass. Data indicates a reduction in sorption of the analyte upon an increase in the amount of biomass beyond 1 g/L. Maximum sorption occurred when 1 g/L of the biomass was subjected to sorption studies. Similarly, an increase in analyte (As+3 and As+5 ) concentration to more than 100 mg/L, when the biomass dose was 1 g/L, did not enhance overall sorption in the batch sorption model (Figure 1(d)). Either an increase in contact time of absorption or an increase in sorbate concentration seems to indicate similar behaviour of the biomass with respect to arsenic uptake. 3.2. FT-IR analysis The FT-IR spectroscopy method was applied to obtain information on the nature of possible biomass–metal ion interactions as presented in Figure 2. The broad and strong bands at 3434 cm−1 were due to bounded hydroxyl (−OH) or amine (−NH) groups in the biomass. Peaks observed at 2926 cm−1 can be assigned to the −CH group of the biomass. Peaks at 1646, 1546 and 1403 cm−1 were attributed to a stretching vibration of the carboxyl group (−C=O). The bands observed at 1083 cm−1 were assigned to C−O stretching of alcohols and carboxylic acids. The asymmetrical stretching vibration at 3434 cm−1 shifted to 3428 and 3433 cm−1 for As+3 - and As+5 -treated biomass. Similarly, the carboxyl peaks at 1645, 1546 and 1453 cm−1 shifted to 1640 and 1456 cm−1 for As+3 -treated and 1650, 1548 and 1452 cm−1 for As+5 -treated biomass, respectively. The peak of the C−O group at 1083 cm−1 shifted to 1081 and 1079 cm−1 for As+3 - and As+5 -treated biomass. The results indicated the involvement of carboxyl
(−COOH), hydroxyl (−OH) and amine (−NH) groups in the biosorption of As+3 and As+5 onto Arthrobacter sp. biomass. The peak shift in the fingerprint region, i.e. 554– 600 cm−1 for As+3 and 616 cm−1 for As+5 indicated the involvement of aromatic amino acids during biosorption of arsenic. Peaks at 794 cm−1 for As+3 and 846 and 740 cm−1 for As+5 -treated biomass appeared in addition to the control. According to Gadsden [31] and Niua et al. [32], these two peaks are characteristic of inorganic arsenic compounds in the biomass. 3.3. Adsorption isotherms The distribution of metal ions between the liquid phase and biosorbent in the equilibrium adsorption process can be described by several isotherms, based on a set of assumptions related to the heterogeneity or homogeneity of adsorbents, the type of coverage and the possibility of interaction between the adsorbent species. The biosorption isotherms were investigated using three equilibrium models, namely the Langmuir, Freundlich and DubininRadushkevich (D-R) isotherm models. The Langmuir sorption isotherm is most widely used isotherm model for the biosorption of a solute from a liquid solution. The Langmuir model assumes that the uptake of metal ions on to a solid is a monolayer adsorption process, without any interaction between sorbed ions. Langmuir isotherm can be defined according to the following formula: qe =
q m KL C e 1 + K L Ce
(3)
where qe is the equilibrium metal ion concentration on the adsorbent (mg/g), Ce is the equilibrium metal ion concentration in the solution (mg/L), qm is the monolayer biosorption capacity of the adsorbent (mg/g) and KL is the Langmuir biosorption constant (L/mg), relating to the
Figure 2. Fourier transform infrared spectroscopy (FT-IR) spectra of (a) untreated, (b) As+3 -treated and (c) As+5 -treated Arthrobacter sp. biomass.
free energy of biosorption. Figure 3(a), indicates the nonlinear relationship between the quantity (mg) of As+3 and As+5 ions sorbed per unit mass (g) of Arthrobacter sp. biomass. The coefficients of determination (R2 ) were found to be 0.9568 for As+3 and 0.964 As+5 biosorption. These results indicate that the biosorption of the metal ions onto the isolate biomass fitted well with the Langmuir model. It can be assumed that the sorption of As+3 and As+5 ions occurred due to involvement of functional groups or binding sites present on the surface of the biomass, a monolayer biosorption. The maximum biosorption capacity (qm ) of isolate biomass was found to be 74.91 mg/g for As+3 and 81.63 mg/g for As+5 . The KL value was calculated as 0.019 L/mg for As+3 and 0.017 L/mg for As+5 biosorption. The biosorption capacity (qm , mg/g) of the isolate biomass for As+3 and As+5 ions with respect to various other biosorbents is presented in Table 1. The sorption capacity of Arthrobacter sp.15b isolate biomass for As+3 and As+5 was found to be higher than for the majority of other biosorbents reported in the literature. The Freundlich model assumes a heterogeneous adsorption surface and active sites with different energy. This isotherm can be explained by following formula: qe =
Kf Ce1/n
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intensity, which varies with the heterogeneity of the material. A Freundlich isotherm was obtained by plotting qe vs. Ce values, which showed a nonlinear relationship between the two (Figure 3(b)). Values of Kf and 1/n were found to be 3.1 and 0.47 for As+3 and 3.05 and 0.49 for As+5 biosorption, respectively. The 1/n values, between 0 and 1, indicate that the biosorption of As+3 and As+5 onto the isolate biomass was favourable under the studied conditions. However, the R2 value was 0.906 for As+3 and 0.917 for As+5 biosorption. These results suggested that the Freundlich model was not able to describe adequately the relationship between the amounts of sorbed metal ions and their equilibrium concentration in the solution. The Langmuir isotherm model best fitted the equilibrium data since it presented a higher R2 value than the Freundlich model. The physical or chemical natures of biosorption processes were studied by analysing the equilibrium data using the D-R isotherm model. The linear form of the D-R isotherm model is presented by the following equation: ln qe = ln qm − βε 2
(5)
where qe is the amount of metal ions adsorbed on per unit weight of biomass (mg/g) , qm is the maximum biosorption capacity (mg/g) , β is the activity coefficient related to mean biosorption energy (mol2 /J2 ) and ε is the Polanyi potential (ε = RT ln(1 + 1/Ce ). The D-R isotherm model
(4)
where Kf is a constant relating the biosorption capacity and 1/n is an empirical parameter relating to biosorption 100
(a)
90 80
qe (mg/g)
70 60
ε 2 × 10 8 (J2/mol 2)
50 40
1.5 -7
As +3
30
-7.5
As +5
10 0 0
50
100
150
200
250
Ce (mg/L) 100
(b)
90
ln qe (mol/g)
20
3.5
5.5
(c)
7.5 As +3 As +5
-8 -8.5 -9 -9.5 -10
80
-10.5
70
qe (mg/g)
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Environmental Technology
-11
60 50
K
40 30
As +3
20
As +5
10 0 0
50
100
150
200
250
Ce (mg/L)
Figure 3. (a) Langmuir isotherm plots for biosorption of arsenite and arsenate onto Arthrobacter sp.15b biomass. (b) Freundlich isotherm plots for biosorption of arsenite and arsenate onto Arthrobacter sp.15b biomass. (c) Dubinin-Radushkevich (D-R) isotherm plots for biosorption of arsenite and arsenate onto Arthrobacter sp. biomass. In all cases, biomass dosages 1 g/L; contact time 30 min; pH 7 for As+3 ; pH 3 for As+5 ; temperature 28◦ C). The error bars represent standard deviations.
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Adsorbent/biosorbent
As+3
pH
As+5
pH
References
Zr(IV)-loaded LDA chelating agent Fe(III)-treated biomass (Staphylococcus xylosus) Powder of stem of Acacia nilotica Lichen (Xanthoria parietina) Macrofungus (Inonotus hispidus) Fungal biomass (Penicillium purpurogenum) Phosphorylated orange waste (POW) Green algae (Ulothrix cylindricum) Bacterial biomass (Arthrobacter sp.)
49.15 54.35 – 63.8 51.9 35.6 70.43 67.2 74.91
9 7 – 6 6 5 8 6 7
88.73 61.34 50.8 60.3 59.6 – 67.43 – 81.63
4 3 7.5 – 2 – 2 – 3
Balaji et al. [11] Aryal et al. [21] Baig et al. [12] Sari and Tuzen [30] Sari and Tuzen [29] Say et al. [8] Ghimire et al. [13] Tuzen et al. [35] Present study
1 E=√ −2β
2
3.4. Biosorption kinetic models In order to evaluate biosorption dynamics, kinetic constants can be used to optimize the residence time of a biosorption process. Pseudo-first-order and pseudo-second-order kinetic models were used to analyse the sorption rate of As +3 and As+5 on Arthrobacter sp. biomass. The pseudo-first order rate equation is given as log qe − k1 t log(qe − qt ) = (7) 2.303 where qe (mg/g) is the amount of metal ions sorbed at equilibrium, qt is the amount of metal sorbed at any time (mg/g) and k1 is the rate constant of the equation (min−1 ). The biosorption rate constant k1 can be determined experimentally by plotting log(qe − qt ) vs. t. Experimental data were also tested with the pseudo-second-order equation [33] t 1 1 t (8) = + 2 qt k2 q e qe where k2 is the equilibrium rate constant (g/mg/min). Both of these kinetic models are presented in Figure 4(a)
y = -0.0409x + 1.5709 R² = 0.8166 As +3
1.6 1.4
As +5
1.2 1
Linear (As +3)
0.8
Linear (As +5)
0.6 0.4
(6)
The adsorption process is regarded as being chemical in nature when values lie between 8 and 16 kJ/mol, similarly adsorption is physical in nature when the value of E is less than 8 kJ/mol. [29] The mean biosorption energy was calculated as 10.10 and 10.85 kJ/mol for the biosorption of As+3 and As+5 ions, respectively. Biosorption processes of both metal ions onto Arthrobacter sp. biomass occurred due to a chemical ion-exchange mechanism, since the sorption energies lay within 8–16 kJ/mol.
(a)
1.8
log (qe-qt )
well fitted the equilibrium data since the R2 value was found to be 0.9931 and 0.9922 for As+3 and As+5 , respectively (Figure 3(c)). The qm value was found using the intercept of the plots as 1.29 × 10−3 and 1.13 × 10−3 mol/g for As+3 and As+5 , respectively. The biosorption mean free energy (E, kJ/mol) gives information about the nature of adsorption, i.e. physical or chemical. The mean biosorption energy (E, kJ/mol) is expressed as follows:
y = -0.0326x + 1.4271 R ² = 0.8406
0.2 0 0
10
20
30
40
50
Time (min) 30 (b)
25 y = 0.5585x + 0.7323 R ² = 0.9935
20
t/q t
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Table 1. Comparative evaluation of biosorption capacity (mg/g) of Arthrobacter sp. for As+3 and As+5 with different biosorbency for arsenic removal.
15
As +3 As +5
10
Linear (As +3) Linear (As +5) y = 0.5038x + 0.5437 R ² = 0.9934
5 0 0
10
20
30
40
50
Time (min) Figure 4. Biosorption kinetic models for metals uptake. (a) Pseudo-first-order model for As+3 and As+5 ; (b) pseudo-second-order model for As+3 and As+5 . The error bars represent standard deviations.
and (b), whereas different rate constants are shown in Table 2. The values of correlation coefficient of the pseudosecond-order model were found to be 0.9935 for As+3 and 0.9934 for As+5 , which is higher than the pseudofirst-order-model, i.e. 0.8166 and 0.8406. Compared to the pseudo-first-order equation, the pseudo-second-order model can explain the biosorption kinetic behaviour of As+3 and As+5 onto Arthrobacter sp. biomass satisfactorily with a good correlation coefficient.
Environmental Technology Table 2. Kinetic parameters for biosorption of As+3 or As+5 onto Arthrobacter sp.
Arsenic As+3 As+5
8 7.8
Pseudo-second-order
7.6 7.4
K1 (min−1 )
R21
K2 (g/mg min)
R22
0.0115 0.0179
0.8166 0.8404
0.00906 0.00921
0.9935 0.9934
ln K D
Pseudo-first-order
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y = 2.8095x - 2.0345 R² = 0.9913
7.2 7 As +3
6.8 y = 1.7125x +1.2008 6.6
Table 3. Influence of various eluents on the desorption of As+3 and As+5 from Arthrobacter sp.
6.4
3
Recovery (%)
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Eluent 0.5 M HCl 1 M HCl 0.5 M HNO3 1 M HNO3
As+3
As+5
78.35 ± 4.21 91.17 ± 4.85 65.52 ± 4.13 72.46 ± 3.89
68.27 ± 3.52 88.56 ± 4.21 56.81 ± 3.46 66.39 ± 3.65
3.1
3.2
3.3
3.4
3.5
3.6
10–3 (1/T), K –1
Figure 5. Plot of ln KD vs. 1/T for the estimation of thermodynamic parameters for biosorption of arsenite and arsenate onto Arthrobacter sp. biomass. The error bars represent standard deviations.
Data are means ± standard deviations.
3.5. Desorption efficiency Desorption of adsorbed ions onto Arthrobacter sp. was carried out by using different concentrations of HCl and HNO3 . Recovery of adsorbed metal ions from the biomass is shown in Table 3. The highest recovery was found to be 91.17% for As+3 and 88.56% for As+5 using 1 M HCl, whereas 1 M HNO3 could release 72.46% of As+3 and 66.39% of As+5 . The study suggests that 1 M HCl readily stripped off the sorbed metal ions from isolate biomass. In addition, the high stability of Arthrobacter sp. biomass permitted operation of the adsorption-elution process 10 times with a decrease of about 18–25% recovery of As+3 and 26–35% for As+5 . 3.6. Biosorption thermodynamics Thermodynamic behaviour of the biosorption of As+3 and As+5 ions onto Arthrobacter sp. biomass, and thermodynamic parameters including the change in free energy (G ◦ ), enthalpy (H ◦ ) and entropy (S ◦ ) have been studied. The change in free energy (G ◦ ) was calculated from the following equation: G ◦ = −RT ln KD
As +5
R² = 0.9916
(9)
where R is the universal gas constant (8.314 J/mol K), T is temperature (K) and KD (qe /Ce ) is the distribution coefficient. The enthalpy (H ◦ ) and entropy (S ◦ ) parameters were estimated from the following equation: ◦ H ◦ S − (10) ln KD = T RT The H ◦ and S ◦ were calculated from the slope and intercept of the plot of ln KD versus 1/T yields [34] and shown in Figure 5. Gibbs free energy change (G ◦ ) was found to be −19.42, −19.11, −18.75 and −18.23 kJ/mol
for As+3 biosorption and −18.83, −18.46, −18.19 and −17.99 kJ/mol for the biosorption of As+5 at 20, 30, 40 and 50◦ C, respectively. The negative G ◦ values indicated the thermodynamically feasible and spontaneous nature of the biosorption. The decrease in G ◦ values with an increase in temperature suggested a lesser feasibility of biosorption at high temperatures. The enthalpy of biosorption H ◦ parameter was found to be −23.42 and −26.75 kJ/mol for As+3 and As+5 biosorption, respectively. The negative H ◦ indicates the exothermic nature of biosorption at 20 to 50◦ C. The enthalpy or the heat of biosorption ranging from 2.1–20.9 KJ/mol corresponds to physical sorption, whereas ranging from 20.9–418 KJ/mol is regarded as chemical sorption. [35] Therefore the H ◦ value suggests that the biosorption process of As+3 and As+5 on Arthrobacter sp. biomass occurred due to chemisorption. The S ◦ parameter was found to be −16.49 J/mol K for As+3 biosorption and −27.34 J/mol K for As+5 biosorption. The negative S ◦ value suggested a decrease in the randomness at the solid/solution interface during the biosorption process. 4. Conclusions The biosorption capacity of Arthrobacter sp. biomass was found to be 74.91 for As+3 and 81.63 mg/g for As+5 at optimal experimental conditions. Sorption of arsenite as well as arsenate onto bacterial biomass is found to be higher than that of previously studied biomass. The mean free energy values evaluated from the D-R isotherm model indicates that biosorption primarily occurred due to the ion-exchange behaviour of freeze-dried cells. The absorption pattern fitted well with the Langmuir model and followed pseudo-second-order kinetics. FT-IR analysis indicated involvement of functional groups (−OH, −NH, −C=O and −COO−) during biosorption processes. Regeneration properties of biomass further suggests its potential for development into a filtration system for removal of contamination of arsenic from aqueous solution. To the best of
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our knowledge, the present study for the first time reported a detailed study of sorption kinetics of As+3 and As+5 by Gram-positive arsenic-resistant Arthrobacter sp. isolate.
Acknowledgements KSP is thankful to the Council of Scientific and Industrial Research, India, New Delhi for the PhD grant. The first author is also grateful to Dr CL Patel, Chairman, Chautar Vidyamandal and SICART (Sophisticated Instrumentation Centre for Applied Research and Testing) Anand, Gujarat for analysis of samples. JP is thankful to University Grant Commission, New Delhi, for financial support.
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