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Biosorption of nickel(II) and copper(II) ions from aqueous solution by Streptomyces coelicolor A3(2)

Biosorption of nickel(II) and copper(II) ions from aqueous solution by Streptomyces coelicolor A3(2)
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  Colloids and Surfaces B: Biointerfaces 34 (2004) 105–111 Biosorption of nickel(II) and copper(II) ions from aqueoussolution by  Streptomyces coelicolor   A3(2) Ayten Öztürk a , ∗ , Tuba Artan a , Ahmet Ayar b a  Department of Biology, Faculty of Sciences and Arts, Nigde University, Nigde 51200, Turkey b  Department of Chemistry, Faculty of Sciences and Arts, Nigde University, Nigde 51200, Turkey Accepted 24 November 2003 Abstract The biosorption of nickel(II) and copper(II) ions from aqueous solution by dried  Streptomyces coelicolor   A3(2) was studied as a functionof concentration, pH and temperature. The optimum pH range for nickel and copper uptake was 8.0 and 5.0, respectively. At the optimalconditions, metal ion uptake was increased as the initial metal ion concentration increased up to 250mgl − 1 . At 250mgl − 1 copper(II) ionuptake was 21.8% whereas nickel(II) ion uptake was found to be as high as 7.3% compared to those reported earlier in the literature. Metalion uptake experiments were carried out at different temperatures where the best ion uptake was found to be at 25 ◦ C. The characteristics of the adsorption process were investigated using Scatchard analysis at 25 ◦ C. Scatchard analysis of the equilibrium binding data for metal ionson  S. coelicolor   A3(2) gave rise to a linear plot, indicating that the Langmuir model could be applied. However, for nickel(II) ion, divergencefrom the Scatchard plot was evident, consistent with the participation of secondary equilibrium effects in the adsorption process. Adsorptionbehaviour of nickel(II) and copper(II) ions on the  S. coelicolor   A3(2) can be expressed by both the Langmuir and Freundlich isotherms. Theadsorption data with respect to both metals provide an excellent fit to the Freundlich isotherm. However, when the Langmuir isotherm modelwas applied to these data, a good fit was obtained for the copper adsorption only and not for nickel(II) ion.© 2004 Elsevier B.V. All rights reserved. Keywords: Streptomyces coelicolor   A3(2); Biosorption; Scatchard analysis; Adsorption isotherms 1. Introduction Heavy metal pollution is spreading throughout the worldwith the expansion of industrial activities, nickel and copperare known to be commonly used heavy metals [1]. Many in-dustries, especially plating and battery, release heavy metalslike nickel and copper in wastewaters. These metals, whichfind many useful applications in our life, are very harmfulif they are discharged into natural water resources and maypose finally a serious health hazard [2–4]. Such environ-mental constraints have forced especially the metal platingindustry to reduce their emissions to water systems, other-wise mass usage of metals could cause severe environmen-tal problems. Consequently, industrial wastewaters containhigh levels of heavy metals and in order to avoid water pollu-tion treatment is needed before disposal. Therefore, effectiveremoval of heavy metals from wastewaters and industrialwastes still remains a major topic of present research [5]. ∗ Corresponding author.  E-mail address: (A. Öztürk). Metal removal treatment systems using micro-organismsisacheapandpracticalalternativetoconventionalprocesses,since low cost sorbent materials are used. Micro-organismsbased technologies must compete with both operational andeconomical terms in existing metal removal treatment sys-tems. Non-living biomass appears to present specific advan-tages in comparison to the use of living micro-organisms.For instance, the former may be obtained with much lower(if any) cost (it is considered basically as waste), it is notsubjected to metal toxicity, the nutrient supply is not nec-essary as well as their greater binding capacities for toxicmetals. Micro-organism–metal interactions are divided intotwo processes energy-dependent (bioaccumulation) andenergy-independent (biosorption) [6–12]. Both mechanisms may be used to remove metal ions from industrial wastestreams [13,14]. These interactions between the metal andother classes of binding sites on the biosorbent during thebiosorption process could be either specific or non-specificbinding. The characteristics of the adsorption process can beinvestigated using Scatchard analysis. When the Scatchardplot is a straight line it means that there is no change in the 0927-7765/$ – see front matter © 2004 Elsevier B.V. All rights reserved.doi:10.1016/j.colsurfb.2003.11.008  106  A. Öztürk et al./Colloids and Surfaces B: Biointerfaces 34 (2004) 105–111 affinity of the binding sites for the metal over the range of concentration used. wheareas a curved plot indicates thatbinding sites are present with a metal affinity dependent onthe metal concentration [15]. Metal sorption performance depends on some external factors such as pH, temperature,other metals, organic materials and cell metabolic productsin solution [12]. However, biosorption of single-solute of  heavy metals using micro-organisms is affected by severalfactors such as temperature, pH and initial metal concen-tration.In this work, we aimed to study the removal of toxic met-als from solutions by  Streptomyces coelicolor   A3(2). Thisstrain which produces several antibiotics such as methyleno-mycin and actinorhodin may be considered as a potentialpharmaceutical wastes [16,17]. However, the sorption abil-ity of this strain was not studied before. Our study was per-formed on free biosorbent using nickel(II) and copper(II)as the metals of interest. The basic objective of the studyis to contribute to the understanding and modelling of theequilibria of adsorption processes. For this purpose, variousfactors affecting the adsorption, such as treatment time, ini-tial pH of the solution and metal ion concentration, wereinvestigated by the batch equilibration technique. 2. Material and method 2.1. Culture and growth conditionsS. coelicolor   A3(2) strain was grown and maintained onGYM Streptomyces medium, which contained 4g glucose,4g yeast extract and 10g malt extract per liter. The pHwas adjusted to 7.2 with dilute potassium hydroxide.  Strep-tomyces  strain was cultivated in 500ml Erlenmayer flaskscontaining 200ml of medium and were shaken in an or-bital rotary shaker at 100rpm, for 15 days at 28 ◦ C. Cultureswere harvested by means of centrifugation at 13,000rpm for5min and were washed three times with distilled water. Thepellet was soaked in petri dishes and dried at 70 ◦ C for 24h. 2.2. Preparation of metal solutions Test solutions containing single nickel(II) and copper(II)ions were prepared from analytical grade chemicals (nickelnitrate and copper sulphate). The concentrations of bothmetal ions prepared from stock solutions ranged from 25to 250mgl − 1 . Before mixing the micro-organisms, the pHof each test solution was adjusted to the required value byusing 1M NaOH and HNO 3  or H 2 SO 4 . 2.3. Biosorption experiments The biosorption experiments were carried out using thebatch equilibrium technique at different pH and temperaturevalues. Equilibrium biosorption was determined by using1gl − 1 of the dried and ground bacterium suspension sampleto which different initial metal concentrations was added.Solution concentrations were varied from 25 to 250mgl − 1 and were agitated on a shaker for 8h which is more thanample time for adsorption equilibrium. Samples were takenat definite intervals for their residual metal ion concentra-tions in the solution. Solid–liquid separation was performedby centrifugation (13,000rpm for 5min) and analysed forthe remaining metal ions spectrophotometrically at 460 and320nm using sodium diethyl dithiocarbamate as the com-plexing agent, respectively [18]. For each sample a blank test without micro-organisms was also performed to avoidconfusion between biosorption and possible metal precipi-tation. However, biosorption experiments were carried outas duplicates and values used in calculations were the arith-metic averages of experimental data. 3. Results and discussion The results are given as a unit of adsorbed and unadsorbedmetal ion concentration per gram of dried biosorbent in so-lution at equilibrium. Adsorption yield (Ad%) is defined asthe ratio of adsorbed quantity of metal ion per gram of bac-terium at equilibrium to the initial amount of metal ions andis calculated from Eqs. (1) and (2).Ad%  = q eq XC 0 (1) q  = C eq C 0 X (2)where  X   is the bacterium concentration (gl − 1 ),  q eq  is theadsorbed metal ion quantity per gram of micro-organism atequilibrium (mgg − 1 ),  C  0  is the initial metal ion concentra-tion at equilibrium (mgl − 1 ) and  C  eq  is the residual metalion concentration at equilibrium (mgl − 1 ). 3.1. Effect of pH on nickel(II) and copper(II) biosorption Earlier studies on heavy metal biosorption have shownthat pH was the single most important parameter affectingthe biosorption process [6,19]. Fig. 1 shows the uptake of  nickel(II) and copper(II) ions at different initial pH valuesusing S.coelicolor  A3(2).Themaximumuptakeofnickel(II)ion was obtained at an initial pH 8.0, while the maximumuptake of copper(II) ion was at 5.0. The nickel speciationwas not studied about pH 8.0 because of the precipitationof Ni(OH) 2 . This was clearly evident from the high uptakevalue of 99.4% at pH 11.0. However, it is believed that dif-ferent pH binding profiles for nickel(II) and copper(II) ionsare due to the nature of the chemical interactions of eachmetal with the bacterial cells. The metal-binding propertiesof Gram-positive bacteria, such as actinomycetes (i.e.  Strep-tomyces ), are largely due to the existence of specific anionicpolymers in the cell wall structure, consisting mainly of pep-tidoglycan, teichoic or teichuronic acids.   A. Öztürk et al./Colloids and Surfaces B: Biointerfaces 34 (2004) 105–111  107Fig. 1. The effect of initial pH on equilibrium adsorption of metal ions( C  0 : 150mgl − 1 ,  X  : 1.0gl − 1 , temperature: 25 ◦ C). Duetothishighfixedanioniccontentof  S.coelicolor  ,theymay exhibit large sorption capacities, which could be of animportant aspect for its industrial application as biosorbentspecially the nickel ions, since they belongs to the transitionmetal ions that have high affinity not only to surface ligands,such as phosphoryl, SO 32 − RNH 2  and R 2 NH, but also tocarbonyl (COO − ) groups too [11]. 3.2. Effect of contact time and concentration on uptake of nickel(II) and copper(II) ions Fig. 2 shows the effect of treatment time on the adsorptionof nickel(II) and copper(II) ions onto biosorbent from aque-ous solutions. Time of contact of adsorbate and adsorbent isof great importance in adsorption since contact time dependson the nature of the system used. Microbial metal uptake bynon-living cells, which is metabolism-independent passivebinding process to cell walls (adsorption), and to other ex-ternal surfaces, it is generally considered as a rapid process,taking place within a few minutes [20]. Therefore, for nickel or copper-bacterium system the adsorption was achievedwithin 5min as is shown in Fig. 2. The initial metal ion concentration remarkably influenced the equilibrium metaluptake and adsorption yield as shown in Table 1. The higher Table 1Equilibrium adsorbed quantities and adsorption yields of each metal ion obtained at different initial metal ion concentrations a Nickel(II) Copper(II) C  0  (mgl − 1 )  q eq  (mgg − 1 ) b Ad%  C  0  (mgl − 1 )  q eq  (mgg − 1 ) Ad%35.6 2.70 ( ± 0.005) 7.5 32.2 16.4 ( ± 0.04) 50.953.3 4.11 ( ± 0.004) 7.7 54.9 26.6 ( ± 0.03) 48.5114.1 8.71 ( ± 0.004) 7.6 97.0 37.2 ( ± 0.03) 38.3147.5 11.1 ( ± 0.04) 7.5 144.9 42.0 ( ± 0.05) 28.9194.5 14.5 ( ± 0.02) 7.4 208 47.0 ( ± 0.01) 22.5255.6 18.8 ( ± 0.005) 7.3 221 48.4 ( ± 0.03) 21.8 a  X  : 1.0gl − 1 , temperature: 25 ◦ C, agitation rate: 100rpm, pH is equal to optimum value for each metal ion. b Each value is an arithmetical average of a duplicate experimental data.Fig. 2. Time variations of adsorption of metal ions ( C  0 : 150mgl − 1 eachinitial metal ion concentration,  X  : 1.0gl − 1 , temperature: 25 ◦ C). is the initial concentration of the metal ion, the larger is theamount of metal ion taken up. When the initial copper(II)concentrationwasincreasedfrom25to250mgl − 1 ,theload-ing capacity has increased from 16.4 to 48.4mgg − 1 . Themaximum nickel(II) loading capacity at 250mgl − 1 of thebiosorbent was found to be 18.8mgg − 1 . The increase of loading capacities of biosorbents with the increase of metalion concentration could be attributed to higher probabilityof interaction between metal ions and biosorbents. Adsorp-tion yields determined at different initial metal ion concen-trations are given in Table 1. As is seen from this table high adsorption yields were observed at lower concentrations of metal ions, accordingly the uptake percentage of nickel wasminimum (7.3%,mgl − 1 ) when the concentration was maxi-mum 7.5%. Similarly the uptake of copper(II) ion minimumwas at 21.8%,mgl − 1 when the maximum was 50.9%. 3.3. Effect of temperature on biosorption of metal ions The effect of temperature on the equilibrium metal up-take was less significant than pH. In general, maximuminitial adsorption yields were found at temperatures be-tween 20 and 30 ◦ C. Adsorption is an exothermic reactionand therefore uptake of pollutants by adsorption process  108  A. Öztürk et al./Colloids and Surfaces B: Biointerfaces 34 (2004) 105–111 Table 2Comparison between the results of this work and others found in the literatureMetal Biosorbent a Operating conditions  q Hc (mgg − 1 ) ReferencespH  T   ( ◦ C)  C  b (mgl − 1 )  X   (gl − 1 )Copper  Streptomyces noursei  (1) 5.5 30 0.6–65 (i) 3.5 9 [23]Copper  Pseudomonas syringae  (1) n.a. d 22 0–13 (i) 0.28 25.4 [24]Copper  Cladosporium resinae  (2) 5.5 25 1–320 (i) 1 16 [20]Copper  Aureobasid pullulans  (2) 5.5 25 1–320 (i) 1 6 [20]Copper  Aspergillus niger   (2) 5 n.a. 100 (e) n.a. 4 [25]Copper  Ganoderma lucidum  (2) 5 n.a. 5–50 (e) n.a. 24 [25]Copper  Penicillum digitatum  (2) 5.5 25 10–50 (e) 6.5 3 [26]Copper  Saccharomyces cerevisiae  (3) 4 25 3.2 (i) 2 0.8 [27]Copper  Arthrobacter   sp. (1) 3.5–6 30 180 (e) 0.4 148 [28]Copper  Chlorella vulgaris  (4) 4 25 100 (i) 0.75 37.6 [29]Copper  Chlorella fusca  (4) 6 20 6.3 (i) n.a. 3.2 [30]Copper  Chlorella vulgaris  (4) 6 25 20 (i) 1 7.5 [31]Copper  Spirulina platensis  (4) 6 25 20 (i) 1 10.0 [31]Copper  Chlorella vulgaris  (4) 5 25 5 (i) 1 1.8 [32]Copper  Scenedemus quadricauda  (4) 4 25 5 (i) 1 2.8 [32]Copper  Chlorella vulgaris  (4) 4.5 25 100 (i) 1 40.0 [19]Copper  Scenedemus obliquus  (4) 4.5 25 100 (i) 1 20.0 [19]Copper  Synechocystis  sp. (4) 4.5 25 100 (i) 1 23.4 [19]Copper  Streptomyces coelicolor   5 25 150 (i) 1 42 This work Nickel  Streptomyces coelicolor   8 25 150 (i) 1 11.1 This work Nickel  Chlorella vulgaris  (4) 5 25 100 (i) 1 42.3Nickel  Scenedemus obliquus  (4) 5 25 100 (i) 1 18.7Nickel  Synechocystis  sp. (4) 5 25 100 (i) 1 15.8Nickel  Pseudomonas syringae  (1) n.a. 22 0–12 (i) 0.28 6 [24]Nickel  Streptomyces noursei  (1) 5.9 30 0.6–60 (i) 3.5 0.8 [23]Nickel  Rhizopus arrhizus  (2) 6–7 n.a. 10–600 (i) 3 18.7 [33]Nickel  Ascophyllum nodosum  (4) 6 25 200 (e) n.a. 70 [34]Nickel  Fucus vesiculosus  (4) 3.5 25 200 (e) n.a. 17 [34]Nickel  Arthrobacter   sp. (1) 5–5.5 30 150 (e) 1.4 13 [28] a 1: Bacterium; 2: fungus; 3: yeast; 4: alga. b i: Initial metal concentration; e: metal equilibrium concentration. c q H  highest value experimentally observed of the specific uptake. d n.a.: Not available. decreases as reaction temperature increases. However, inour work the maximum adsorption ( q eq ) for both nickel(II)and copper(II) ions were found to be at 25 ◦ C as is indicatedin Fig. 3. When our results (Table 2) are compared with Fig. 3. The effect of temperature on the 150mgl − 1 each initial metal ionconcentration (  X  : 1.0gl − 1 ). those reported in the literatures, the values of nickel(II) andcopper(II) specific uptake is found to be significantly higherthan those given elsewhere. 3.4. Adsorption isotherms The contact time of 15min and pH values of 8.0 and 5.0were chosen as the experimental conditions for the determi-nation of adsorption isotherms of nickel(II) and copper(II)ions (Fig. 4). The adsorption isotherms show that the amount of metals adsorbed increases as their equilibrium concen-tration increases in solution. As evident from these data,the adsorption isotherms of nickel(II) ion were steeper thanthe corresponding isotherm for copper(II) ion, indicating agreater affinity of nickel on  S. coelicolor   A3(2).To evaluate and compare the saturation capacities of   S.coelicolor   A3(2) toward the two heavy metal ions, the ad-sorption isotherms were analysed and fitted using Scatchardequation (Fig. 5). The Scatchard analysis is used here not only to estimate the adjustable parameters, but also to havea preliminary analysis about the number of site types andtheir relative affinity for metal ions. The presence of more   A. Öztürk et al./Colloids and Surfaces B: Biointerfaces 34 (2004) 105–111  109Table 3Adsorption isotherm parameters for nickel(II) and copper(II) ions on  S. coelicolor   A3(2)Metal ions Langmuir isotherm Scatchard analysis Freundlich isotherm  A s  (mgg − 1 )  K  b  (lmg − 1 )  r  2 K  b  q m  (mgg − 1 )  r  2 k   (mgg − 1 ) 1/  n r  2 Nickel(II) 416.6 1.85  ×  10 − 4 0.80 1.84  ×  10 − 4 418.5 0.79 0.08 0.98 0.99Copper(II) 66.66 0.011 0.99 0.0098 72.24 0.94 2.88 0.53 0.95 than one inflection point on a plot based on Scatchard anal-ysis usually indicates the presence of more than one type of binding site. When the Scatchard plot showed a deviationfrom linearity, greater emphasis was placed on the analysisof the adsorption data in terms of the Freundlich model, inorder to construct the adsorption isotherms of the ligands atparticular concentrations in solutions. Fig. 4 shows the ad-sorption isotherms of metals on  S. coelicolor   A3(2), whilstFig. 5 presents the adsorption characteristics assessed fromthe Scatchard plot. Equilibrium binding data for metals gaverise to a linear plot, indicating that the Langmuir modelcould be applied for adsorption process [21,22]. In the ad-sorptions of metals, Scatchard analysis of the equilibriumbinding data for metal ions on  S. coelicolor   A3(2) gave riseto a linear plot, indicating that the Langmuir model couldbe applied. However, for nickel(II) ion, divergence from theScatchard plot was evident, consistent with the participationof secondary equilibrium effects in the adsorption process.To test the fit of data, the Freundlich and Langmuirisotherm models were applied to this study. The linearisedFreundlich isotherm model isln q  =  ln k  +  1 /n ln C where q istheamountoftheadsorbedligandsperunitweightof adsorbent at the equilibrium concentration  C  ,  k   is a Fre-undlich constant related to the adsorption capacity and 1/  n  isrelated to the adsorption intensity of a adsorbent. The valuesof   k   and 1/  n  were evaluated from the intercept and the slope,respectively, of the linear plot of ln  q  versus ln  C   based on Fig. 4. Isotherms for the equilibrium binding of metal ions on  S. coelicolor  A3(2). experimental data. The linearised Langmuir isotherm modelis Cq = 1 K b A s + CA s where  K  b  and  A s  are the adsorption binding constant andsaturation capacity, respectively. These constants were eval-uated from the intercept and the slope of the linear plot of  C   /  q  versus  C   based on experimental data.Adsorption constants, metal-binding constant and corre-lation coefficients for the metals were calculated from Lang-muir, Freundlich isotherms and Scatchard analysis are givenin Table 3. The adsorption data with respect to both metalsprovide an excellent fit to the Freundlich isotherm (Fig. 6). Fig. 5. Scatchard plots for nickel and copper adsorption by  S. coelicolor  A3(2).
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