Performance of Streptomyces rimosus biomass in biosorption of heavy metals from aqueous solutions

Accepted Manuscript Performance of Streptomyces rimosus biomass in biosorption of heavy metals from aqueous solutions

Mohamed Nasser Sahmoune PII: DOI: Reference:

S0026-265X(18)30522-8 doi:10.1016/j.microc.2018.05.009 MICROC 3157

To appear in:

Microchemical Journal

Received date: Revised date: Accepted date:

30 April 2018 7 May 2018 7 May 2018

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ACCEPTED MANUSCRIPT TITLE: Performance of Streptomyces rimosus biomass in biosorption of heavy

metals from aqueous solutions

Author: Mohamed Nasser Sahmoune

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Department of process engineering, Faculty of Engineering Sciences, University of Boumerdes, Algeria.

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Laboratory of Coatings, Materials and Environment, University of Boumerdes, Algeria

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(Corresponding author)

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E-mail: [email protected]

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ACCEPTED MANUSCRIPT

Abstract The removal of heavy metals by Streptomyces rimosus has been the subject of many investigations. This review paper focuses on the removal of heavy metals from aqueous solution through

Streptomyces

rimosus, produced from pharmaceutical industry as solid waste, as adsorbent, and discusses the effect

efficiency of

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of various process parameters like pH, temperature, metal concentration etc, on the metal removal this bacterium. The paper also evaluates the different kinetic, equilibrium, and

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thermodynamic models used in Streptomyces rimosus sorption of heavy metals. Biomass

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characterization and sorption mechanisms as well as elution of metal ions are also discussed. The literature revealed that Streptomyces rimosus had a good affinity for binding lead and iron compared

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with other heavy metals. The adsorption of heavy metals is well described by Langmuir isotherm, which expresses the existence of monolayer adsorption. The kinetic data followed both pseudo first order and

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pseudo second order models. Thermodynamic studies showed spontaneous and exothermic nature of the sorption processes in most case. Dilute acids (HCl and H2SO4) are quite effective in desorption of heavy

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metals. Ion exchange played the chief role in the adsorption mechanism of metal, and carboxyl groups

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are mainly involved in this mechanism.

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Keywords: Biosorption, Streptomyces rimosus, heavy metals, Equilibrium, Kinetics, Thermodynamic

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ACCEPTED MANUSCRIPT 1. Introduction Water pollution by heavy metals is one of the growing problems all over the world. High toxicity has been observed with several metals. Even at low concentrations, heavy metals can be accumulated through the food chain, thus posing a serious threat to humans, animals, and the environment [1 - 4]. Physicochemical methods such as activated carbon adsorption, ion exchange, membrane filtration, and chemical precipitation have been developed for the removal of heavy metals from wastewater [5 - 10]. However, the

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practical application of such processes is sometimes restricted due to technical or economical constraints.

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Nanocomposites adsorbents were applied to the removal of heavy metals from aqueous solution [11]. Ion imprinted polymers has been used for elimination of heavy metal ions at low concentrations in complicated

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matrices [12, 13]. Bioremediation processes for the removal of heavy metals have also received increasing attention [14 – 18].

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Over the last two decades, biosorption process has emerged as a cost effective and efficient alternative for water and wastewater treatment [19]. At present, biosorption field has been enriched by a vast amount of studies

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published in different journals [20 - 23]. Biosorption is a physico-chemical process which involves the removal of various pollutants, such as heavy metals from solution by biological materials [24 - 27].

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Different types of microorganisms, such as bacteria, algae, fungi and yeast cells have the ability to remove heavy

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metals from aqueous solutions [28 - 30]. Indeed, microorganisms interact with metal ions present in solution. For example, the employment of bacterial biomass for the metal removal treatment of effluents is a perspective suggested by many researches dealing with metal-bacteria interactions [23, 26, 31, 32]. Actinomycetes,

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particularly Streptomyces species have been tested for uptake metals with very encouraging results [23, 24, 33, 34]. Streptomyces species are stable and are not subject to the drastic treatments, and possess advantages such as

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low investment cost, and high treatment efficiencies [24]. Streptomyces rimosus strains belong to the most widespread microscopic filamentous bacteria in the environment. This strain is very often used to study variable processes, such as heavy metal adsorption or biosorption. Streptomyces rimosus is a genus of Gram-positive bacteria that grows in various environments, with a filamentous form [35 - 37]. A large fraction of Tetracycline antibiotics in the market is obtained from Streptomyces rimosus [38, 39]. In our previous study, we have demonstrated that waste product of antibiotic industries were able to remove 95 % of chromium ions by using dead Streptomyces rimosus [40, 41]. Our results were proved the natural affinity of

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ACCEPTED MANUSCRIPT Streptomyces rimosus compounds for chromium and could contribute to remove concentrations of chromium from wastewater [42, 43]. The aim of the present review work is to investigate the use of Streptomyces rimosus biomass as an adsorbent for removing heavy metals from aqueous solutions. A list of adsorption capacities of heavy metals for Streptomyces rimosus and the best isotherm and kinetic fitting models are provided. In addition, regeneration studies, thermodynamic studies, the mechanism of biosorption and the experimental conditions are also discussed in depth.

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As a result by reading this review, the researchers in the field of bacterial biosorbents and biosorption can get complete idea that in which direction they have to start and further move their research.

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2. Streptomyces rimosus structure

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The Streptomyces rimosus cell wall plays an important role in heavy metal biosorption. Cell wall is the first component that comes in contact with the metal ions [44, 45]. Streptomyces rimosus is a Gram-positive bacterium

polysaccharide chains and teichoic acids (Figure 1).

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[37]. The cell wall of Streptomyces rimosus contains two components: peptidoglycan, which is made from

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Peptidoglycan is a polymer consisting of a glycan (polysaccharide) backbone consisting of N-acetyl muramic acid and N-acety glucosamine with peptide side chains (amino acids and diaminopimelic acid) that are cross-linked

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through peptide bonds forming a three dimensional structure. The carboxyl groups on the peptide side chains are

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the anionic sites for metal binding. Teichoic acids are polyol phosphate polymers, with either ribitol or glycerol linked by phosphodiester bonds [5]. Teichoic acid may be covalently attached to the peptidoglycan [5]. Peptidoglycan and teichoic acids are the main binding sites for metal cations [46, 47].

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Either living or dead cells are able to adsorb metals although there are great differences in their uptake mechanisms [48, 49]. Bioaccumulation is based on the incorporation of metals inside the living cells [50, 51].

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The main disadvantages of using living cells are as follows: Living microorganisms need a continuous supply of nutrients, heavy metals can be very toxic for their metabolic process, temperature and pH may affect bacterial growth, and recovery of metals may be more complicated [5, 29]. The use of non-living biomass or dead cells has more advantages because it is not subjected to metal toxicity, absence of requirements for nutrients and can be easily immobilized in an inert matrix [52, 53]. Scanning Electron Microscopy (SEM) is a well-known microscope, which was increasingly used to examine biological specimens and other kind of micro-sized particles. Figure 2 shows SEM picture of the Streptomyces

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ACCEPTED MANUSCRIPT rimosus cell. SEM examination revealed that the surface of the biomass is porous and is compatible with good metal uptake characteristics [43]. The magnitude of electrostatic interaction between the sorbent surface and a metal ion is a function of electrokinetic potential (expressed usually as zeta potential). Zeta-potential measurements may provide useful information regarding the net effective charge on the biomass surface (positive or negative). Zeta potential is the potential at the junction of biomass and metal solution and is related to the mobility of the

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metal ion [54]. Selatnia et al. [55 - 57] showed that the zeta potential of S. rimosus strongly depends on the pH. The zeta potential values were negative over the whole investigated pH range, namely for pH from 2 to 10,

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where the electrokinetic potential varied from −90 to −60 mV. S. rimosus usually has a negative surface charge,

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which is attributed to the negative charge of organic functional groups resulting from the dissociation of H+ ions according to Eq (1) and Eq (2)

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R–COOH = R–COO- + H+ R–OH = RO- + H+

(1) (2)

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The S. rimosus biomass was deprotonated and negatively charged, indicating that the major binding sites are acidic groups. The biosorption process includes physicochemical interactions between metal ions and several

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anionic ligands present on the biomass like carboxyl, phosphoryl and carbonyl. The negative surface of the

positively charged metal.

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biomass confirms the presence of anionic sites; it indicates that Streptomyces rimosus has the potential to adsorb

One important characteristic of an adsorbent is the surface functional groups present, which are largely

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characterized by the FTIR spectroscopy method. Figure 3 shows the FTIR spectra of dead Streptomyces rimosus [34]. The main groups detected were carboxyl, amino, –CH stretch, C–O stretch, and OH groups. Moreover, a

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report by Sahmoune et al. [43] stated that the presence of carboxyl and carbonyl groups on the surface of the Streptomyces rimosus could be accountable for the binding of chromium. Selatnia et al. [55] used FTIR results to detect the presence of various functional groups on the surface of modified Streptomyces rimosus, which explains its surface mechanism complexity. The authors observed that after cadmium adsorption, a significant shift of the N–H stretching vibration peaks take place, which verifies the chemical interactions between Cd(II) and the amide groups on the biomass surface. The alteration of several peaks due to hydroxyl- and carboxyl-groups after biosorption of the heavy metals, were also noticed. These phenomena highlighted the fact that carboxyl, hydroxyl and amide groups were all engaged in the adsorption of cadmium.

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ACCEPTED MANUSCRIPT Selatnia et al. [56] studied the relationship between functional groups on the dried bacterium Streptomyces rimosus and its nickel adsorption capability. The authors utilized FTIR to analyze the functional groups in both untreated and NaOH treated Streptomyces rimosus biomass. The results indicate that carboxyl, amino, phosphate, amide and hydroxyl groups are dominant in the Streptomyces rimosus structure. In addition, the transmission spectra shift at certain wavenumbers confirms that several surface functional groups are involved in the binding of Ni(II). In order to understand the surface binding mechanism, it is therefore essential to identify the functional groups on

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the biomass. The FTIR spectroscopy technique was employed to expose the sorption binding mechanism of Pb(II) by dead Streptomyces rimosus [57]. Authors proved that the participation of (–NH), carboxylate

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anions (–COO−), hydroxy (–OH) and others (–C–N), (–C–O), (–C–H), (–C=O) in Pb(II) binding is evident.

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Tassist et al. [50] studied the biosorption mechanism of Al (III) by a mycelial biomass Streptomyces rimosus. The main groups detected were hydroxyl, methyl, carboxyl, amine, thiol and phosphate.

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X-ray fluorescence spectroscopy (XRFS) is an analytical technique that can be used to determine the chemical composition of a wide variety of sample types including solids, liquids, slurries and loose powders.

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Sahmoune et al. [41] exploited XRFS to determine the chemical composition of Streptomyces rimosus. Table 1 provides the chemical composition of Streptomyces rimosus . From the results, authors found that SiO2, Al2O3, K2O and organic matter are dominant in the Streptomyces rimosus composition.

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3. Factors affecting heavy metal removal Factors such as pH, initial metal ion concentration, adsorbent dose, agitation rate and other factors have various degrees of influence on the metal uptake by Streptomyces rimosus biomass. This section is intended to give a brief

3.1. Effect of pH

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discussion on these parameters.

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Numerous studies show that the biosorption of heavy metal from aqueous solution depends strongly on pH. Sahmoune et al. [40] studied the effect of pH on the biosorption of Cr (III) by dead bacterium S. rimosus and their results showed that chromium removal decreased with decreasing pH due to repulsive forces between metal cations in solution and biosorbent surface charged positively at pH values lower than 4.8 [40]. Sahmoune and Louhab [42] reported that the removal of chromium from aqueous solution by Streptomyces rimosus increased as pH was increased. Cr (III) starts precipitating at pH above 5 as Cr (OH)3. Cr (III) ions are precipitated out in alkaline pH range and do not contribute towards the biosorption. This gives the upper limit of pH to be studied . Thus pH has a direct influence on the mechanism and uptake of chromium by S. rimosus [42].

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ACCEPTED MANUSCRIPT Selatnia et al. [55, 56] examined the effect of initial pH on bacterial (dried S. rimosus) binding of heavy metals Cadmium and Nickel and they found maximum uptake at pH 8.0. They explained the higher uptakes at higher pH values by electrostatic attractions between positively charged metal cations and negatively charged cell surface. The adsorption percentage of metals in the lower pH levels (e.g., pH 2 or 3) was significantly low due to competition with the H+ ions for binding sites on the surface of bacteria; the increase in pH favoured metal sorption mainly because of the elevated levels of negatively charged groups on the cell surface.

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Tassist et al. [58] reported that Streptomyces rimosus adsorbed a maximal amount of aluminium at pH 4. Streptomyces rimosus cells could adsorb about 11.76 mg of aluminium per gram dry cells from the solution.

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Bakhti et al. [59] have also reported that maximum Ag (I) uptake in milligram of metal per gram of biomass for

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100 mg/l initial metal ion concentrations is at pH 8. The sorption of metal ions depends on solution pH, which influences electrostatic binding of ions to corresponding functional groups. An increase in pH increases the

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availability of negatively charged sites for electrostatic attraction of metal cation, thereby resulting in increase in adsorption capacity for metal cation.

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Chergui et al. [60] have reported that heavy metal uptake by dead S. rimosus biomass increases with increasing pH in the range 5 – 6 for Cd (II), 4 – 6 for Zn (II) and 3 – 6 for Cr (VI). Authors observed the deposition of cadmium, zinc and chromium. Precipitates render the study of the biosorptive binding difficult, so it is preferable

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to study biosorption at pH values where precipitation does not occur. pH of solution also influencing the process

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of precipitation.

In a study performed by Mameri et al. [61] for the removal of zinc by inactivated cells of bacterium S. rimosus

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showed the maximum biosorption capacity at pH 7.5 binding 80 mg metal g-1 dry biomass. They explained the enhancement of uptake of metal at basic pH in terms of ions exchange between the biomass and zinc ions. The ion

[61].

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exchange occurred due to the replacement of H+ and Na+ ions on functional groups by zinc ions in the bulk solution

3.2. Effect of initial metal ion concentration Initial concentration provides an important driving force to overcome all mass transfer resistances of the metal between the aqueous and solid phases. Hence a higher initial concentration of metal may enhance the adsorption process. Selatnia et al. [55] observed that although the uptake of uptake of Cd (II) adsorption by S. rimosus was lower at lower metal ion concentrations, the biosorptive capacity increased significantly at higher concentrations of metal.

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ACCEPTED MANUSCRIPT These results suggested the fact that on increasing the cadmium strength in solution, the free binding sites of bacterium are occupied by metal ions much faster than when the solution is dilute. On the other hand for Nickel metal ion biosorption by the same biomass, they found that the biosorptive capacity increased to a maximum of 32.6 mg g-1 at a residual metal ion concentration of 600 mg l-1 [56]. Bakhti et al. [59] investigated the effect of metal ion concentration on adsorption of silver using dried activated S. rimosus biomass. Uptake of the metal increased from 12 to 63 mg g-1with increasing silver concentration from 40

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to 200 mg l-1.

Chergui et al. [60] reported that uptake of each of the metal, Copper; Zinc; Chromium by S. rimosus increased

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with increasing metal ion concentration. The metal ion removal was highly concentration dependent.

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Mameri et al. [61] also investigated the effect of initial zinc metal concentration on the Zn (II) sorption using activated S. rimosus biomass. They found that the biosorptive capacity increased to a maximum of 80 mg g -1 at a

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residual zinc ion concentration of 200 mg l-1.

The increase in the biosorbent's loading capacity as a function of metal ion concentration was believed to be due

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to a high driving force for mass transfer. In agreement with this, a more concentrated solution should display better adsorption performance.

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3.3. Effect of adsorbent dose

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An increase in the biomass concentration generally increases the amount of solute biosorbed, due to the increased surface area of the biosorbent, which in turn increases the number of binding sites. Conversely, the quantity of biosorbed solute per unit weight of biosorbent decrease with increasing biosorbent dosage, which may be due to

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the complex interaction of several factors. An important factor at high sorbent dosages is that the available solute is insufficient to completely cover the available exchangeable sites on the biosorbent, usually resulting in low

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solute uptake [31].

Selatnia et al. [57] reported that the removal efficiency of lead by S. rimosus decreased from 90 to 30 % with increasing adsorbent dose from 1 to 10 g/l. In contrast, Tassist et al. [58] obtained the opposite behavior on the removal efficiency of Aluminium by S. rimosus. Authors revealed that the removal efficiency of Aluminium by S. rimosus biomass increased from 45 to 98 % with increasing adsorbent dose from 5 to 30 g/l. with more adsorbent present, the available adsorption sites or functional groups also increase. In turn, the amount of adsorbed heavy metal ions is increased, which brought about an improved adsorption efficiency.

3.4. Effect of agitation rate 8

ACCEPTED MANUSCRIPT Providing an adequate stirring rate in a batch biosorption process is important to overcome external mass transfer resistances so the effect of stirring rate on biosorption should be investigated. Mameri et al. [61] investigated the effect of shaking rate on the biosorption of Zinc using S. rimosus biomass with 140–250

m

selected range of particle size. They observed that uptake capacity of biomass increased from 4 to

28 mg g-1 with increasing shaking rate from 100 to 250 rpm. The results showed that there is a boundary layer surrounding the biomass particles and a decrease in its effect with increasing shaking rate [61].

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A similar observation has been reported in the investigation of biosorption of heavy metals (Cadmium, Nickel, Lead, Aluminium and Iron) using dead S. rimosus biomass [55 - 57, 62].For higher speeds the vortex phenomenon

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was encountered [60, 63].

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3.5. Effect of contact time

The evaluation of metal removal performance by S. rimosus biomass can be performed using kinetics studies to

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obtain information about the contact time needed to establish equilibrium. Generally, the biosorption increases with increase in contact time. Rapid metal biosorption by biological material is desirable to provide a short contact

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time between the metal bearing solution and Streptomyces rimosus biomass. Sahmoune et al. [41] examined the ability of nonliving biomass Streptomyces rimosus to adsorb chromium from

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aqueous solution. A greater amount of chromium was removed by this bacterium in the first 30 min (80%).

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However, more than 95% of Cr (III) uptake occurred within 80 min. Selatnia et al. [56] described adsorption study of Ni (II) onto untreated Streptomyces rimosus . Authors reported that nickel uptake by this adsorbent increased from 5 to 16.3 mg/g as the contact time by the biomass to remove

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nickel increased from 5 to 90 min and then remained almost constant. A contact time of 2 h was needed to establish equilibrium. The same behavior can be detected in a research performed by Bakhti et al. [59] sequestering silver

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by untreated Streptomyces rimosus. Equilibrium was reached within 2 h and was independent of initial silver concentration. Chergui et al. [60] reported the simultaneous biosorption of Cu (II), Zn (II), and Cr (VI) by Streptomyces rimosus biomass. The equilibrium was achieved within 90, 120 and 150 min for Cu (II), Zn (II), and Cr (VI), respectively, at 25 °C, 100 mg/l concentration and 3 g/l biomass dosage. However in another study by Mameri et al. [61], a longer contact time (4 h), is often needed for the attainment of equilibrium. Yous et al. [63] reported competitive biosorption of heavy metals from aqueous solutions onto Streptomyces rimosus. The biosorption of nickel and cadmium by S. rimosus is close of equilibrium after six (6)

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ACCEPTED MANUSCRIPT hours of contact time. Indeed, later, due to the decrease in the number of sorption sites on the adsorbent as well as adsorbate concentration, the sorption of adsorbate became slow [64].

3.6. Other factors Other factors that may have an influence on the biosorption of heavy metals by S. rimosus are temperature, size of the biosorbent and ionic strength. Temperature seems to affect biosorption only to a lesser extent within the range from 20 to 40 °C [65]. Physical damage to the biosorbent can be expected at higher temperatures. An increase in

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temperature has been found to reduce the biosorption capacity of the biomass S. rimosus [65].

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In contrast, Tassist et al. [58] obtained the opposite behavior for the temperature effect on adsorption capacity. Aluminium removal increased with increasing temperature. The positive effect of temperature can be related to

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the enhancement of the diffusion rate of aluminium through the boundary layer, and within internal pores of the sorbent particles.

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Biosorption kinetics is related with surface area of biosorbent directly so particle size is also one of the important factors which affect the biosorption capacity. Mameri et al. [61] studied the effect of biomass particle size on the

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biosorption of zinc using non living S. rimosus biomass with 22 – 140, 140 – 250,250 – 350 m selected ranges of particle size. They observed that biosorption capacity of biomass increased with decreasing particle size. This

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situation was explained by larger total surface area of smaller particles for the same amount of biomass [62].

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Similar trend was reported by Ammar [66].

Another important parameter in biosorption is the ionic strength, which influences the adsorption of solute to the biomass surface. The ionic strength influences a wide array of electrostatic interactions in the cell [67].

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Calcium chloride has been employed to elucidate the effect of ionic strength on chromium uptake by S. rimosus biomass [68]. Authors found that the presence of calcium chloride in the range of 0.05 – 0.15 g per 100 ml reduced

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the adsorption of Cr (III) [68].

4. Metal biosorption by S. rimosus 4.1. Biosorption isotherms Analysis of the isotherm data is important in order to develop an equation which accurately represents the results and which could be used for design purposes. The isotherm model give information about surface properties and the affinity of binding sites of S. rimosus cells as well as uptake mechanism. The isotherm model used in heavy metal removal by S. rimosus is given in Table 2. From Table 2, the adsorption data were found to best fit Langmuir model. The Langmuir equation is: [69]

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ACCEPTED MANUSCRIPT  bCe   qe  qmax   1  bCe  Where

qmax

(1)

is the maximum amount of metal adsorbed by S. rimosus to achieve complete monolayer coverage

of the adsorbent surface (mg/g) and b is the Langmuir affinity constant (l/mg). The variables

qe

(mg/g) and

Ce

(mg/l) are the amounts of metal adsorbed per unit weight of adsorbent and the equilibrium concentration,

qmax

is assumed to correspond to saturation of a fixed number of identical surface sites and b is

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The parameter

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respectively.

related to the adsorption energy.

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The Langmuir model suggests that uptake occurs on a homogeneous surface by monolayer sorption without interaction between adsorbed molecules. In addition, the model assumes uniform energies of adsorption onto the

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surface of bacterium biomass and no transmigration of the adsorbate [70].

Uptake of toxic metal ions may contribute to the detoxification of polluted environments. Therefore, the

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investigation of the metal capacity of S. rimosus is fundamental for the field application of biosorption because it gives information about the removal efficiency of metal ions in the process.

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Table 2 shows also the maximum metal capacities reported in literature by Streptomyces rimosus. From this Table,

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S. rimosus showed a good affinity for binding lead and iron compared with other heavy metals, which denotes that this biomass is a promising adsorbent for the treatment of wastewater containing heavy metals.

4.2. Biosorption kinetics

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The obtained kinetic information has a significant practical value for technological applications, since kinetic modelling successfully replaces time and material consuming experiments, necessary for process equipment

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design. Several kinetic models were applied to correlate the kinetic data of different metal ions adsorbed in S. rimosus biomass. Kinetic models used for biosorption of some selected heavy metals using S. rimosus are presented in Table 3. It can be observed that the kinetic data followed both pseudo first order and pseudo second order models. The pseudo-second-order kinetic model suggests that the rate limiting step in heavy metal biosorption is chemisorption, which involves valence forces through the sharing or exchange of electrons between sorbent and sorbate [71].The pseudo-first-order equation assumes that metal ions bind only to one active site of S. rimosus biomass surface [29]. 4.3. Modelling of column data

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ACCEPTED MANUSCRIPT When metal pollutant containing solution passes through a packed bed column, at the beginning, most of metal pollutant gets sorbed on biosorbent so metal pollutant concentration in the effluent remains either very low or in some cases is not detectable. As biosorption continues, metal pollutant concentration in the effluent rises, slowly at first, and then abruptly. When this abrupt rise or breakthrough occurs, the flow is stopped. The performance of continuous packed bed is described through the concept of the breakthrough curve. The successful design of a column sorption process requires the concentration-time profile or effluent breakthrough curve to be predicted;

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the maximum sorption capacity of a sorbent is also required in the design [72].

Addour et al. [73] studied zinc biosorption by S. rimosus biomass pretreated with sodium hydroxide in a packed

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bed column. They obtained zinc removal as 42 % from breakthrough curves for up to 3 h at 25 mg l-1 zinc

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concentration in the influent with an adjusted pH of 6.5 at 12.0 ml min-1 flow rate. The breakthrough data were fitted to the linearized Thomas model. Biosorption capacity of the beads for zinc was found to be 2.9 mg g -1 [73].

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4.4. Thermodynamic studies

Temperature is shown to affect adsorption capacity and is associated with several thermodynamic parameters [74].

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It is an indicator for the adsorption nature whether it is an endothermic or exothermic process. When adsorption capacity decreased with temperature, the process was claimed to be exothermic, and vice versa.

G0

values indicate the spontaneous and non-spontaneous sorption process.

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negative and positive

(G0 ) indicates the degree of spontaneity of the sorption process. The

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Standard Gibbs free energy change

The relation between Gibbs free energy, gas constant R (8.314 J/mol °K) and solution temperature, T, as well as adsorption equilibrium constant, Ka, is given by: (2)

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G0  RT ln Ka

temperature:

ln K a

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The enthalpy and entropy can be estimated from Van't Hoff equation which relates the equilibrium constant K a to

S 0 H 0  R RT

A positive

(3)

H 0 value signifies the endothermicity of a process and also shows high probability that the process

is chemisorption, while exothermic processes usually has negative on physical bonding. On the other hand, a positive

H 0 where the sorption is most likely to rely

S 0 value corresponds to the spontaneity in the adsorption

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ACCEPTED MANUSCRIPT process and a higher degree of randomness at the solid–liquid interface, whereas negative

S 0

values represent

the opposite phenomenon. Tassist et al. [58] reported the sorption of Al (III) onto S. rimosus biomass in batch experiments. The Gibbs free energy of adsorption (ΔG°) was determined to be between 1.07 and - 3.62 KJ/mol at temperature between 10 and 80 °C. The decrease in the ΔG° value with an increase in temperature favors the removal process of aluminium at high temperature. From values of ΔG°, ΔH° and ΔS° the adsorption process was found to be spontaneous, feasible

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and endothermic. The energy of activation calculated by the Arrhenius equation (Ea = 52.18 KJ/mol) indicated an adsorption process of a chemisorption [58].

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4.5. Mechanism and mass‐transfer processes

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Biosorption of metal ions takes place primarily on the outer surface of microorganisms and is the first step in the mechanism involved when interactions between metals and cell wall components take place

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[75]. Physical adsorption via electrostatic or van der Waals forces can retain metal ions on the outer surfaces of bacterial cells and thereafter make the adsorbed metal ions bind with chemical functional

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groups of biomolecules on the cell surface and then inside cellular structure through chemical interactions [76].

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In physical adsorption, a weak Van der Waals attraction is observed between an adsorbate and a surface. From a

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thermodynamic point of view, physical adsorption is spontaneous and exothermic [77]. In addition to physical adsorption, ion exchange and complexation are always believed to be the dominant mechanisms involved in metal biosorption [78]. Target metal ions can exchange reversibly with the protons, alkali,

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or alkali earth ions present on the bacterial cell surface during the ion-exchange process.

4): [79]

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There are four consecutive steps used to describe the mechanism of adsorption process. These are as follow (Figure

(1) Metal ions are transported to the liquid film or boundary layer from bulk liquid, surrounding the adsorbent (2) Metal ions are transported from boundary film to external surface of the adsorbent during the surface diffusion phenomenon (3) Metal ions ions are transferred from the surface to the intraparticle active sites of the adsorbent during the porediffusion phenomenon (4) Uptake of metal ion on the active sites, by sorption.

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ACCEPTED MANUSCRIPT The first and fourth steps do not belong to the rate controlling steps because in the first step there is no involvement of adsorbent and the fourth step is a very rapid process. Therefore, surface or pore-diffusion may be the rate controlling steps [80]. External mass diffusion and intraparticle diffusion models were used in order to investigate the mechanism of heavy metal sorption by S. rimosus and potential rate-controlling steps. A study by sahmoune et al. [40] revealed that both surface adsorption and pore diffusion are involved in chromium

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adsorption on S. rimosus. In order to understand how chromium binds to the S. rimosus biomass, it is essential to identify the functional groups responsible for chromium binding. Most of the functional groups involved in the

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binding process are found in cell walls. Various mechanisms such as electrostatic forces and ion-exchange must

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be taken into account while discussing the mechanism of chromium biosorption on S. rimosus biomass. Sahmoune and Louhab [42] reported that the acidity of the medium affects the competition ability of hydrogen

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ions with Cr (III) ions to active sites on the S. rimosus surface. Negligible biosorption could be found when the pH values were lower than 2.0. The maximum biosorption was found to be for Cr (III) ions at pH 4.8. When the

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pH values increased, biosorbent surfaces were more negatively charged and the biosorption of the metal ions with positive charge (Cr3+) process was reached maximum according to the ion-exchange mechanism. Selatnia et al. [55] highlighted the role of electrostatic attraction in the biosorption of cadmium on S. rimosus

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biomass. They performed their experiments at different initial cadmium concentrations and pH values. The value

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of pH increases with increase in contact time and initial Cd 2+ concentration. At values of pH less than 8, the carboxylic and phosphate groups on the surface of S. rimosus are deprotonated and adsorb cationic cadmium via

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electrostatic attractions. Selatnia et al. [46] proposed that the external mass transfer was the predominant mechanism of the sorption of Cd (II) on S. rimosus biomass.

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Bakhti et al. [59] removed Ag (I) metal ions by S. rimosus biomass from aqueous solution. The Ag (I) removal mechanism by S. rimosus involved direct biosorptive interaction with the biomass through ion exchange. The mechanism of ion exchange apparently prevails: this phenomenon occurred due to the replacement of Na + ions on functional groups by silver ions in the bulk solution. External mass transfer mechanism was suggested for Ag (I) sorption with S. rimosus biomass using Urano and Tachikawa model [50]. Chergui et al. [60] examined the mechanism involved for the removal of three heavy metals, i. e., Cu (II), Zn (II), and Cr (VI), by S. rimosus using a series of batch experiments. Ion exchange was claimed as the dominant mechanism.

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ACCEPTED MANUSCRIPT Selatnia et al.[62] examined the mechanism involved for the removal of iron by S. rimosus. Ion exchange was claimed as the dominant mechanism. Authors noticed that in the biosorption of iron ions on S. rimosus , the bond between the iron ions and the surface functional groups of the biomass formed as soon as H+ ions were released from the surface. Yous et al. [63] reported the kinetics of cadmium and nickel onto S. rimosus. Authors determined the values of external mass transfer and internal diffusion using Weber and Morris and Urano and Tachikawa models. The value

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of external mass transfer for Cd (II) and Ni (II) were 6.37×10-5 and 1.2×10-4 m s-1, respectively. The obtained intraparticle diffusion coefficients for cadmium and nickel ions were 9.9×10 -12 and 7.12×10-12 m2 s-1, respectively.

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External mass transfer was found to be the dominant mechanism in the biosorption of the two metals.

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Ion exchange is a reversible chemical reaction where an ion within a solution is replaced by a similarly charged ion attached onto an immobile solid particle. In general, the ion exchange mechanism can be represented by the following equation.

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M X   X HY  XH  MYX

HY

sorbed

M X .

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corresponds to the number of acid sites on the solid surface, M

Where

X

is metal ion, and

MYX

is the

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5. Desorption

(4)

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It can be seen from the literature review that dilute acids and bases are commonly used for desorption [81]. Desorption processes occurring after saturation of metal ions on biomass surface. Desorption of heavy metals is

metals by S. rimosus.

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mainly a function of pH. Dilute acids (HCl , H 2SO4 HNO3…) are generally quite effective in desorption of heavy

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Sahmoune et al. [41] reported that 95 % of Cr (III) desorption was resulted at approximately zero pH using HCl and H2SO4. Tassist et al. [58] recovered 96% of adsorbed Aluminium by using HCl at pH 1. Chergui [60] reported that HCl, HNO3 and H2SO4 at pH = 2 desorbed Cu (II) and Zn (II) from dead S. rimosus. Desorption data showed that nearly 55% of the Zn (II) adsorbed and 50% of the Cu (II) adsorbed on dead cells could be desorbed. Addour et al. [73] reported that Zn (II) was recovered around 90 % at 0.1 M HCl, whereas around 50 % was desorbed in 0.5 and 1.0 M HCl in column system.

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ACCEPTED MANUSCRIPT The major problem of desorption process is the disposal of the acid solution obtained which contain high concentration of heavy metals. One of the methods to tackle this problem is precipitation of metal from the aqueous solution using barium chloride [82].

6. Conclusion and future directions Biosorption of heavy metals is a potential approach against the conventional techniques. In the present review, S. rimosus can efficiently remove heavy metals from wastewaters. FTIR spectrums of S. rimosus revealed the

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presence of hydroxyl, amino and carboxylic groups. Scanning electron microscopy (SEM) of S. rimosus showed

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that the surface of the biomass is porous and is compatible with good metal uptake characteristics. Several factors, e.g., pH, temperature, ionic strength, and initial concentration including biosorbent dose, affect

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the biosorption to various extents. However pH is the major factor influencing biosorption. It has been generally reported that in highly acidic medium the removal of metal ions is almost negligible and it increases by increasing

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the solution pH up to a certain limit. The biosorption capacity increases as the initial metal ion concentration in the solution increases. The findings of S. rimosus indicate that the sorption percentage increased with increase in

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temperature up to 25°C.

Numerous empirical models for metal removal by S. rimosus have been employed to describe the biosorption

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equilibrium. Langmuir equation is the most popular and widely used model in a large number of studies, which

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reflected the monolayer adsorption behavior. The mechanism of metal biosorption on S. rimosus could be a chemical ion exchange and carboxyl groups are mainly involved in this mechanism. Most of the reported biosorption studies have been carried out in batch mode with detailed study of various

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isotherm and kinetic models; however, only few have adopted continuous column system. Thus, the priority of future research is the biosorption of heavy metals by S. rimosus in a fixed bed column and the application of this

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biosorbent for real industrial wastewater.

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Fig1. Cell wall of Streptomyces rimosus Taken from Ref [79]

Fig 2. SEM Image of the Streptomyces rimosus (Enlarging × 2000). Taken from Ref [79]

Fig.3. FTIR spectra of Streptomyces rimosus biomass. Taken from Ref [43]

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Figure 4: Steps used to describe the mechanism of biosorption process. Taken from Ref [79]

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Table 1. The chemical composition of Streptomyces rimosus

Constituents

SiO2

Al2O3

Fe2O3

CaO

MgO

MnO

Na2O

K2O

P2O5

TiO2

Percentage

48.300

8.390

2.150

1.330

0.200

0.049

2.449

2.980

1.060

1.095

Constituents

SO3

SrO

Rb2O

PbO

ZnO

CuO

NiO

BaO

Organic matter

Percentage

0.350

0.008

0.007

0.029

0.094

0.018

0.009

0.082

32.400

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by weight

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by weight

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Table 2: Equilibrium studies of sorption of some heavy metals on Streptomyces rimosus biomass

Langmuir

T ( °C)

Reference

25 25

Adsorption capacity (mg/g) 74 11.76

8 4

Langmuir Langmuir Langmuir Langmuir

8 11 6 4.8

25 25 25 20

64.9 16.5 29 83

[55] [63] [66] [41]

Langmuir Langmuir Langmuir Langmuir

10 6.5 11 Free pH 7.5

[59] [58]

25 25 25 25

125 32.9 28.5 137

[62] [56] [63] [57]

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80

[61]

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Langmuir

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Zn (II)

Cd (II) Cd (II) Cr (VI) Cr (III)

pH

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Fe (III) Ni (II) Ni (II) Pb (II)

Langmuir, and Freundlich Langmuir, Freundlich, and Dubinin–Radushkevich Langmuir, and Freundlich Langmuir, and Freundlich Langmuir Langmuir, Freundlich, and Temkin Langmuir, and Freundlich Langmuir, and Freundlich Langmuir, and Freundlich Langmuir, and Freundlich

Equilibrium model followed Langmuir Langmuir

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Ag(I) Al (III)

Isotherm model used

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Metal

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Table 3: Kinetic studies of sorption of some heavy metals on Streptomyces rimosus biomass

Fe (III) Ni (II) Ni (II) Pb (II) Zn (II)

60

Pseudo-second order

[55]

and pseudo-

360

Pseudo-second order

[63]

pseudo-second

300

and pseudo-

240

and pseudo-

120

and pseudo-

360

and pseudo-

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and pseudo-

Pseudo-second order

[41]

Pseudo-first order

[62]

Pseudo-first order

[56]

Pseudo-second order

[63]

180

Pseudo-first order

[57]

240

Pseudo-first order

[61]

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Cr (III)

[59] [58]

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Cd (II)

and pseudo-

Pseudo-first order Pseudo-second order

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Cd (II)

Reference

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Pseudo-first order Pseudo-first order second order Pseudo-first order second order Pseudo-first order second order Pseudo-first order , order, Elovich Pseudo-first order second order Pseudo-first order second order Pseudo-first order second order Pseudo-first order second order Pseudo-first order

Kinetic model followed

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Ag(I) Al (III)

Equilibrium time (min) 60 180

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Metal

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Highlights  Metal removal through biosorption is attractive  Streptomyces rimosus biomass as potential adsorbent  In this paper, biosorption of heavy metals by Streptomyces rimosus is reviewed  The need to switch batch to fixed columns studies for field applications  Ion exchange played the chief role in the adsorption mechanism of metal,

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Figure 1

Figure 2

Figure 3

Figure 4