The Past, Present, and Future Trends of Biosorption - Springer Link

Biotechnology and Bioprocess Engineering 2010, 15: 86-102 DOI/10.1007/s12257-009-0199-4

=

The Past, Present, and Future Trends of Biosorption Donghee Park1, Yeoung-Sang Yun2, and Jong Moon Park3* 1

Department of Environmental Engineering, Kyungpook National University, Daegu 702-701, Korea 2 Environmental Biotechnology National Research Lab, School of Chemical Engineering, Research Institute of Industrial Technology, Chonbuk National University, Jeonju 561-756, Korea 3 Advanced Environmental Biotechnology Research Center, Department of Chemical Engineering, School of Environmental Science and Engineering, Pohang University of Science and Technology, Pohang 790-784, Korea= Abstract The discovery and further development of biosorption phenomena provide a basis for a whole new technology aimed at the removal of various pollutants or the recovery of valuable resources from aqueous systems. Today, biosorption is one of the main components of environmental and bioresource technology. Since the status of scientific development of a technology can be reflected through analyses of the literatures pertaining to it, in this review, we qualitatively examine almost all aspects of biosorption research. A range of subjects are covered, including the initial history, raw materials, mechanisms, instrumental tools, process factors, modification and immobilization methods, recovery and regeneration, continuous processes, commercial application, and modeling studies of biosorption. Finally, we summarized the important considerations of the current research on biosorption, as well as the suggestions for its future directions. We believe that this review will prove to be useful for scientists and engineers in the performance of their research into biosorption. © KSBB = = = =

hÉóïçêÇëW=~ÇëçêÄÉåíI=ÄáçëçêÄÉåíI=ÄáçëçêéíáçåI=ÜÉ~îó=ãÉí~äëI=ÇóÉëI=éêÉÅáçìë=ãÉí~äë=

INTRODUCTION Rapid industrialization and urbanization have resulted in the generation of large quantities of aqueous effluents, many of which contain high levels of toxic pollutants [1,2]. Various physicochemical and biological processes are usually employed to remove pollutants from industrial wastewaters before discharge into the environment [3]. In the case of treatment of adsorptive pollutants like heavy metals and ionic dyes, however, most of the conventional treatment processes, especially chemical precipitation or coagulation, become less effective and more expensive when the adsorbates are in a low concentration range [5-7]. Although ionexchange resins and activated carbons have long been recognized as effective commercial adsorbents for treating industrial wastewaters containing adsorptive pollutants, their high cost and low efficiency have limited their commercial use in actual industrial scenarios [2]. Since any type of solid material has the capacity to adsorb pollutants to some degree, a number of industrial inorganic *Corresponding author Tel: +82-54-279-2275 Fax: +82-54-279-2699 e-mail: [email protected]

wastes, such as ash, or natural inorganic materials like clay, synthetic materials like zeolite, as well as, living or nonliving biomass/biomaterials, have been investigated as cheap adsorbents capable of replacing the well-known, but more expressive ones [8-15]. Considering their cost and efficiency, biomass-based adsorbents or biosorbents as they are commonly called, are the most attractive alternatives to ionexchange resins and activated carbons [2]. The use of biosorbents for the removal of toxic pollutants or for the recovery of valuable resources from aqueous wastewaters, is one of the most recent developments in environmental or bioresource technology [2,7,16,17]. The major advantages of this technology over conventional ones include not only its low cost, but also its high efficiency, the minimization of chemical or biological sludges, the ability to regenerate biosorbents, and the possibility of metal recovery following adsorption [7]. Although biosorption of heavy metals or dyes has become a popular environmentally driven research topic, it represents only one particular application of the sorption process. In his recent review paper, Bohumil Volesky, a pioneer in the field, defined ‘biosorption’ as the property of certain biomolecules (or types of biomass) to bind and concentrate selected ions or other molecules from aqueous solutions [7]. As opposed to a

Biotechnol. Bioprocess Eng. 87=

much more complex phenomenon of bioaccumulation based on active metabolic transport, biosorption by dead biomass (or by some molecules and/or their active groups) is passive and occurs primarily due to the ‘affinity’ between the biosorbent and adsorbate [7]. Since Hecker first reported a quantitative study on the copper uptake by fungal spores of Trilletia tritici and Ustilago crameri in 1902 [18,19], over 3,000 research articles on biosorption have been published in various journals in many countries. In addition, about 70 review papers and some books have appeared that deal with biosorption phenomena, equilibrium and kinetic modeling, reactor operation, and application to real industries [20-22]. However, for general readers, access to these special books or perusal of the large number of papers available on this topic is challenging. The aim of this review, therefore, is to summarize and encapsulate the past and present trends in biosorption research, by examining the primary subjects pertaining to biosorption research. Finally, we discuss future directions of biosorption, as mentioned by specialists in this area, and presented our own opinions on the prospects of this research area.

FUNDAMENTAL REVIEW The Initial History of Biosorption

Although the ability of living microorganisms to take up metals from aqueous solution was investigated as early as 18th and 19th centuries [23], it is only during the last 3 decades that living or non-living microorganisms have been used as adsorbents for removal and recovery of materials from aqueous solutions. The earliest technological applications of biosorption techniques involved sewage and waste treatment [24]. It was also investigated for use in renovating wastewater generated by the chemical industry [25]. The first patent for a biosorption apparatus used for biological treatment of wastewater was registered by the Ames Crosta Mills & Company Ltd. in 1973 [26]. Scientists in life sciences primarily focused on the toxicological effects and accumulation of heavy metals in microorganisms, while environmental scientists and engineers used this capability of microorganisms as a means of monitoring heavy metal pollution, as well as, for removal/recovery of metals from metal-bearing wastewaters [19]. Some review papers have reported that the first quantitative study on metal biosorption was done by L. Hecke, who reported on the copper uptake by fungal spores of T. tritici and U. crameri in 1902 [18,19]. Similar studies were also reported by F. Pichler and A. Wobler in 1922, in which uptake of Ag, Cu, Ce, and Hg by corn smut were evaluated [19]. Ruchloft first reported that activated sludge efficiently removed even radioactive metals like plutonium-239 from contaminated domestic wastewater in 1949 [27], and the first patent on the use of biosorption technology for removing uranium or thorium ions from aqueous suspension/solution was granted to B. Volesky and M. Tsezos in 1982 [28]. Goodman and Roberts (1971) reported the practical use of

biosorption technology for monitoring trace heavy metals in the environment [29]. Neufeld and Hermann (1975) studied the kinetics of biosorption by activated sludge and reported rapid uptakes of Cd, Hg, and Zn in the first few min, followed by a slow uptake over the next 3 h [30]. Friedmann and Dugan (1968) used a pure culture of Zoogloea for a metal-binding study [31]. Extensive screening of microorganisms for metal uptake had been carried out by A. Nakajima and his coworkers (1978), who reported that the ability of microorganisms to accumulate uranium ions was in the order of: actinomycetes > bacteria > yeast > fungi [32,33]. Gould and Genetelli (1984) examined the competition between metal ions for binding sites of anaerobic sludge, and reported a binding affinity order of: Cu > Cd > Zn > Ni [34]. Y. Chiu and his coworkers (1976) analyzed biological sorption of uranium on mycelia of Penicillium C-1 [35], while M. Tsezos and B. Volesky (1981) focused on biosorptive removal of uranium and thorium by dead fungal biomass of Rhizopus arrhizus [36]. Steen and Karickhoff (1981) reported uptake of hydrophobic organic pollutants by mixed microbial populations [37]. At this point, it should be noted that there was some confusion prevalent in the literature regarding the use of terms ‘bioaccumulation’ and ‘biosorption’, based on the state of the biomass used in this research at the time [2]. The early studies prior to 1980 have been reviewed in detail by Muraleedharan et al. [19]. As pioneers in this area, B. Volesky and M. Tsezos also provide their viewpoints on the initial history of biosorption research in their special review papers [7,38]. Types of Biomass or Biomaterials

Adsorptive pollutants like metals and dyes can be removed by living microorganisms, but can also be removed by dead biological material [39]. Feasibility studies for large-scale applications have demonstrated that biosorptive processes using non-living biomass are in fact more applicable than the bioaccumulative processes that use living microorganisms, since the latter require a nutrient supply and complicated bioreactor systems [2]. In addition, maintenance of a healthy microbial population is difficult due to toxicity of the pollutants being extracted, and other unsuitable environmental factors like temperature and pH of the solution being treated. Recovery of valuable metals is also limited in living cells since these may be bound intracellularly. For these reasons, attention has been focused on the use of non-living biomass as biosorbents [2,23]. As mentioned above, dead biomass has advantages over living microorganisms. However, many attributes of living microorganisms remain unexploited in an industrial context and are all worthy of further attention since they may be of use for specific applications [39,40]. A. Malik mentioned that, when pure biosorptive metal removal is not feasible, application of a judicious consortium of growing metalresistant cells can ensure better removal through a combination of bioprecipitation, biosorption, and continuous uptake of metals after physical adsorption [40]. This type of ap-

88

proach may lead to simultaneous removal of toxic metals, organic pollutants, and other inorganic impurities [40]. To control the size of the current review, however, we have chosen to focus on single biosorption processes in this review and to avoid discussion of hybrid processes combined with biosorption. The first major challenge faced by biosorption researchers was to select the most promising types of biomass from an extremely large pool of readily available and inexpensive biomaterials [41]. When choosing biomass, for large-scale industrial uses, the main factor to be taken into account is its availability and cheapness [6,42,43]. Considering these factors, native biomass can come from (i) industrial wastes, which should be available free of charge; (ii) organisms easily obtainable in large amounts in nature; and (iii) organisms that can be grown quickly or specially cultivated or propagated for biosorption purposes [6,43]. A broad range of biomass types have been tested for their biosorptive capacities under various conditions at this point in time, but there are no limits to exploration of new biomass types having low cost and high efficiency. Biosorptive capacities of various biomass types have been quantitatively compared in many review papers [2,16,43-56]. In some cases, the uptake of heavy metals by biomass reached as high as 50% of its dry weight [6,42]. Biosorbents primarily fall into the following categories: bacteria, fungi, algae, industrial wastes, agricultural wastes, natural residues, and other biomaterials (Table 1). Since it is impossible to quantitatively compare the hundreds of biosorbents reported thus far in the literature, we instead introduce useful review papers that have done these types of comparisons of biosorptive capacities of various biosorbents for various pollutants as part of their aims and scope. For example, extensive comparisons of biosorptive capacities of various types of bacterial biosorbents have been done by Malik [40], Veglio and Beolchini [53], Vijayaraghavan and Yun [2], and Volesky and Holan [43]. Mehta and Gaur compared biosorptive capacities of algae for heavy metals [51]. Wilde and Benemann summarized biosorptive capacities of microalgae [55], while Romera et al. summarized those of macroalgae (i.e., seaweed) [56]. In the case of fungi, Sağ comprehensively summarized biosorptive capacities of fungi and fungal cellular components like chitin and chitosan [52]. Varma et al. [57] and Gerente et al. [58] also summarized the biosorptive capacities of chitin/chitosan and its many derivatives. Some researchers briefly compared the biosorptive capacities of agricultural wastes for heavy metals [5963]. The utilization of plant-derived biomass as adsorbents was also reviewed in the literature [44,54]. Crini reviewed the use of polysaccharide-based materials as adsorbents [5], while O’Connell et al. reviewed cellulose-based adsorbents [64]. Some researchers have extensively compared various biosorbents for specific heavy metals such as cadmium [48], copper [65], or uranium [66]. Mack et al. reviewed the use of biosorbents for recovery of precious metals like gold, platinum, and palladium [49]. Andrès et al. reviewed microbial biosorbents as a means of concentrating rare earth elements like europium, lanthanum, scandium, and ytterbium

Table 1. Types of native biomass that have been used for preparing biosorbents Category

Examples

Bacteria

Gram-positive bacteria (_~Åáääìë sp., `çêóåÉÄ~ÅíÉJ êáìã sp., ÉíÅK), gram-negative bacteria EbëJ ÅÜÉêáÅÜá~ sp., mëÉìÇçãçå~ë sp., ÉíÅK), cyanobacteria (^å~Ä~Éå~ sp., póåÉÅÜçÅóëíáë sp., ÉíÅK)

Fungi

Molds (^ëéÉêÖáääìë sp., oÜáòçéìë sp., ÉíÅK), mushrooms (^Ö~êáÅìë sp., qêáÅÜ~éíìã sp., ÉíÅK), and yeast (p~ÅÅÜ~êçãóÅÉë sp., `~åÇáÇ~ sp., ÉíÅ.)

Algae

Micro-algae (`äçêÉää~ sp., `Üä~ãóÇçãçå~ë sp., ÉíÅK), macro-algae (green seaweed (båíÉêçãçêJ éÜ~ sp., `çÇáìã sp., ÉíÅK), brown seaweed (p~êJ Ö~ëëìã sp., bÅâäçåá~ sp., ÉíÅK), and red seaweed (dÉáäÇáìã sp., mçêéÜóê~=sp., ÉíÅK))

Industrial wastes

Fermentation wastes, food/beverage wastes, activated sludges, anaerobic sludges, ÉíÅK

Agricultural wastes

Fruit/vegetable wastes, rice straws, wheat bran, soybean hulls, ÉíÅK

Natural residues Plant residues, sawdust, tree barks, weeds, ÉíÅK Others

Chitosan-driven materials, cellulose-driven materials, ÉíÅK

[67]. Wang and Chen compared biosorptive capacities of a given amount of biomass from Saccharomyces cerevisiae, according to species of heavy metals [68]. It should be noted that the biosorptive capacity of a certain type of biosorbent depends on its pretreatment methods, as well as, on experimental conditions like pH and temperature. When comparing biosorptive capacities of biosorbents for a target pollutant, therefore, the experimental data of each researcher should be carefully considered in light of these factors. After choosing a form of cheap and abundant biomass, the biosorbent capability for removing a target pollutant can be derived through simple chemical and/or physical method(s). Although simple cutting and/or grinding of dried biomass may yield stable biosorbent particles, some types of biomass have to be either immobilized in a synthetic polymer matrix and/or grafted onto an inorganic support material like silica to yield particles with the required mechanical properties [41]. New biosorbents can be manipulated for better efficiency and for multiple reuses to increase their economic attractiveness, compared with conventional adsorbents like ion-exchange resins or activated carbons [6]. Fig. 1 shows alternative process pathways to produce biosorbent materials that are effective and durable in repeated long-term applications, which was suggested by Vieira and Volesky [6]. Mechanisms of Pollutants Removal by Biosorbents

As shown in Table 1, there are many types of biosorbents derived from various forms of raw biomass, including bacteria, fungi, yeasts, and algae. The complex structure of raw biomass implies that there are many ways, by which these


A

B

Fig. 2. Biosorption mechanisms as classified by Veglio and Beolchini [53]. (A) Classified according to the dependence on the cellular metabolism. (B) Classified according to the location where biosorption occurs. Fig. 1. Schematic diagram for processing different types of native biomass into biosorbents. This diagram was modified from that suggested by Vieira and Volesky [6].

biosorbents remove various pollutants, but these are not yet fully understood. For example, the structure and functional aspects of extracellular polymeric substances (EPS) of microorganisms are related with their roles in metal biosorption [69]. Thus, there are many chemical/functional groups that can attract and sequester pollutants, depending on the choice of biosorbent. These can consist of amide, amine, carbonyl, carboxyl, hydroxyl, imine, imidazole, sulfonate, sulfhydryl, thioether, phenolic, phosphate, and phosphodiester groups [6,62,70]. However, the presence of some functional groups does not guarantee successful biosorption of pollutants, as steric, conformational, or other barriers may also be present [42]. The importance of any given group for biosorption of a certain pollutant by a certain biomass depends on various factors, including the number of reactive sites in the biosorbent, accessibility of the sites, chemical state of the sites (i.e. availability), and affinity between the sites and the particular pollutant of interest (i.e. binding strength) [6]. The understanding of the mechanisms by which biosorbents remove pollutants is very important for the development of biosorption processes for the concentration, removal, and recovery of the pollutants from aqueous solutions [19]. When the chemical or physiological reactions occurring during biosorption are known, the rate, quantity, and specificity of the pollutant uptake can be manipulated through the specification and control of process parameters. Biosorption of metals or dyes occurs mainly through interactions such as ion exchange, complexation, adsorption by physical forces, precipitation and entrapment in inner spaces [62]. Fig. 2 shows biosorption mechanisms classified by Veglio and Beolchini according to their metabolic dependency or the site of biosorption [53].

Instrumentation for Biosorption Research

Information on the active sites involved in the binding of pollutants can be obtained through use of a number of sophisticated analytical tools, including infrared absorption spectroscopy or Fourier transformed infrared spectroscopy (IR or FTIR), scanning electron microscopy (SEM), transmission electron microscopy (TEM), energy dispersive Xray spectroscopy (EDS), X-ray diffraction (XRD) analysis, electron spin resonance spectroscopy (ESR), nuclear magnetic resonance (NMR), X-ray photoelectron spectroscopy (XPS), X-ray absorption spectroscopy (XAS), thermogravimetric analysis (TGA), and differential scanning calorimetry (DSC), among others [46,57,68]. Table 2 shows a brief summary of the analytical techniques available in biosorption research. Many of these analytical techniques require costly equipment and are very expensive to carry out as routine measurements. In addition, the type of information that they yield may not always be what is necessary for understanding and evaluating the biosorption phenomenon of interest [7]. However, different techniques can often provide distinctive, but complementary, information on biosorption of a target pollutant; thus, combining different techniques can optimize the exploration of biosorption mechanisms [68]. Process Factors Influencing Biosorption

For the industrial application of biosorption technology for pollutant removal, it is very important to investigate the removal efficiency of a given biosorbent for the target pollutant. Pollutant uptake can involve different types of biosorption processes that will be affected by various physical and chemical factors, and these factors will determine the overall biosorption performance of a given biosorbent, (i.e. its uptake rate, its specificity for the target, and the quantity of target removed). For this reason, the first step of almost all research has been to examine the individual and/or coopera-

90

Table 2. Analytical techniques used in biosorption research Analytical techniques

Remarks

Table 3. Effects of batch processing factors on biosorptive removal of adsorptive pollutants, such as metals or dyes Process factors

Effects on biosorption of pollutants

Atomic absorption spectroscopy (AAS)

Determine metal concentration in aqueous phase

Inductively coupled plasma (ICP)

Determine metal concentration in aqueous phase

UV-Vis spectrophotometer

Determine metal or dye concentration in aqueous phase by measuring its color intensity

Scanning electron microscope (SEM)

Visual confirmation of surface morphology of the biosorbent

Transmission electron microscope (TEM)

Visual confirmation of inner morphology of biomass, especially cells

Energy dispersive X-ray spectroscopy (EDS)

Element analysis and chemical characterization of metal bound on the biosorbent

Initial pollutant conc. ↑ It increases the quantity of biosorbed pollutant per unit weight of biosorbent, but decreases its removal efficiency.

X-ray diffraction (XRD) analysis

Crystallographic structure and chemical composition of metal bound on the biosorbent

Biosorbent dosage ↑

It decreases the quantity of biosorbed pollutant per unit weight of biosorbent, but increases its removal efficiency.

Electron spin resonance spectroscopy (ESR)

Determine active sites of the biosorbent

Biosorbent size ↓

Nuclear magnetic resonance (NMR)


It is favorable for batch process due to higher surface area of the biosorbent, but not for column process due to its low mechanical strength and clogging of the column.

Fourier transformed infrared spectroscopy (FT-IR)


Agitation speed ↑

Potentiometric titration

Determine active sites of the biosorbent and its amounts

It enhances biosorptive removal rate of adsorptive pollutant by minimizing its mass transfer resistance, but may damage physical structure of biosorbent.

X-ray photoelectron spectroscopy (XPS)

Determine oxidation state of metal bound on the biosorbent and its ligand effects

X-ray absorption spectroscopy (XAS)

Determine oxidation state of metal bound on biosorbent and its coordination environment

Thermogravimetric analysis (TGA)

Characterize thermal stability of the biosorbent

Differential scanning calorimetry (DSC)

Characterize thermal stability of the biosorbent

tive effect(s) of various factors on biosorption [23,46,48,51, 71,72]. In the case of batch biosorption processes for removing adsorptive pollutants such as ionic metals or dyes, the important factors include solution pH, temperature, ionic strength, initial pollutant concentration, biosorbent dosage, biosorbent size, agitation speed, and also the coexistence of other pollutants. Of these factors, the pH appears to be the most important regulator of the biosorptive process. The pH affects the solution chemistry of the pollutants themselves, the activity of functional groups in the biosorbents, and the competition with coexisting ions in solution [2]. In general, as solution pH increases, the biosorptive removal of cationic metals

Solution pH ↑

It enhances biosorptive removal of cationic metals or basic dyes, but reduces that of anionic metals or acidic dyes.

Temperature ↑

It usually enhances biosorptive removal of adsorptive pollutant by increasing surface activity and kinetic energy of the adsorbate, but may damage physical structure of biosorbent.

Ionic strength ↑

It reduces biosorptive removal of adsorptive pollutant by competing with the adsorbate for binding sites of biosorbent.

Other pollutant conc. ↑ If coexisting pollutant competes with a target pollutant for binding sites or forms any complex with it, higher concentration of other pollutant(s) will reduce biosorptive removal of the target pollutant.

or basic dyes is enhanced, while that of anionic metals or acidic dyes is reduced. In some cases, a higher pH will cause precipitation of cationic metals, making neutral conditions essential in this case. Temperature seems to affect biosorption to a lesser extent within the range from 20 to 35oC [53]. Biosorptive removal of most adsorptive pollutants is endothermic, thus higher temperature usually enhances biosorptive removal of the adsorbate through increases in its surface activity and kinetic energy [2]. However, higher temperature can also cause physical damage to the biosorbent; thus, room temperature is usually desirable for the biosorption processes. Unlike controlled laboratory conditions, industrial effluents contain various pollutants including the target, one of interest. Thus there is need for investigation of the inhibitory effects of ionic strength and competing ions. These factors influence biosorptive removal of a target pollutant by competing with the adsorbate for binding sites, by changing its activity, or by forming complexes with it [2]. The effects of other process factors on the biosorptive removal of adsorptive pollutants are briefly summarized in Table 3.


Table 4. Modification methods for converting raw biomass into better biosorbents Category Physical modification Chemical modification

Detailed methods Autoclaving, steam, thermal drying, lyophilization, cutting, grinding, ÉíÅK

Pretreatment (washing)

Acids (HCl, H2SO4, HNO3, H3PO4, citric acid, ÉíÅK), Alkalis (NaOH, KOH, NH4OH, Ca(OH)2, ÉíÅK), Organic solvents (methanol, ethanol, acetone, toluene, formaldehyde, epichlorohydrin, salicylic acid, NTA, EDTA, SDS, L-cysteine, Triton X-100, ÉíÅK), and Other chemicals (NaCl, CaCl2, ZnCl2, Na2CO3, NaHCO3, K2CO3, (NH4)2SO4, H2O2, NH4CH3COO, ÉíÅK)

Enhancement of binding groups

Amination of hydroxyl group, carboxylation of hydroxyl group, phosphorylation of hydroxyl group, carboxylation of amine group, amination of carboxyl group, saponification of ester group, sulfonation, xanthanation, thiolation, halogenation, oxidation, ÉíÅK

Elimination of inhibiting groups

Decarboxylation/elimination of carboxyl group, deamination/elimination of amine group, ÉíÅK=

Graft polymerization High energy radiation grafting (using γ-irradiation, microwave radiation, electro-magnetic radiation, ÉíÅK); Photochemical grafting (with/without sensitizers like benzoin ethyl ether, acrylated azo dye and aromatic ketones under UV light); and Chemical initiation grafting (using ceric ion, permanganate ion, ferrous ammonium nitrate/H2O2, KMnO4/citric acid, ÉíÅK) Cell modification (during growth)

Culture optimization Optimization of culture conditions for enhancing biosorptive capacity of cells Genetic engineering Over-expression of cysteine-rich peptides (glutathione, phytochelatins, metallothioneins, ÉíÅK); and Expression of hybrid proteins on the surface of cells

Modification of Biomass for Better Biosorbency

As the biosorption process primarily occurs on the surface of the biomass, its surface modification can greatly alter its biosorptive capacity and function [2,54,70]. A number of chemical, physical, and other modification methods have been employed for this objective in the literature. In some cases, a target chemical group present in a form of biomass will be chemically modified to characterize the biosorption mechanism connected with that group. A good example of this would be the physical and/or chemical activation of raw biomass for conversion into chars or activated carbons [73,74], but further detail is beyond the aims and scope of this review. Table 4 shows a number of modification methods that can be found in the literature for preparing better biosorbents. Normally, physical modification is very simple and inexpensive, but is generally less effective than chemical modification. Among various chemical modification methods, chemical pretreatment (washing) has been preferred due to its simplicity and efficiency [2]. In many cases, acid-washing can enhance the capacity of biosorbents for cationic metals or basic dyes, through extraction of soluble organic or inorganic components from raw biomass and/or by changing its biochemistry. However, some chemicals can cause serious mass losses of the biosorbent (i.e. structural damage), as well as a drop in the biosorptive capacity. Vast improvements in the biosorptive capacity of a biosorbent can be obtained through enhancement or modification of its functional groups [2,54]. Amine, carboxyl, hydroxyl, sulfonate, thiol, and phosphonate groups are known binding sites for metals or dyes; thus, these groups can be newly formed, or their amounts increased, to enhance biosorptive capacity [54]. Raw biomass may also have certain

groups that inhibit biosorption of a target pollutant; thus, chemical elimination of the inhibiting groups will produce a better biosorbent [2]. Another efficient way to introduce binding groups onto the surface of a biosorbent is the grafting of long polymer chains onto the surface of raw biomass, via direct grafting or through polymerization of monomers, such as acrylic acid, acrylamide, acrylonitrile, ethylenediamine, hydroxylamine, glycidyl monomers, and urea [64]. According to the methodology for creating active sites (free radical or ionic chemical groups) for initiating polymerization reactions, there are 3 types of typical initiation methods that have been used, including high energy radiation, and photochemical and chemical initiation grafting (Table 4). In fact, since many researchers in this area (i.e. graft copolymerization) have preferred to use terms ‘adsorption’ and ‘adsorbent’ instead of ‘biosorption’ and ‘biosorbent’, information regarding these types of modification has been missed by researchers who search for the latter terms. Extensive and detailed information concerning graft copolymerization has been presented in a recent review by O’Connell et al. [64]. Lastly, in the cases that utilize microbial biomass, the biosorptive capacity can be enhanced by optimizing culture conditions or by using genetic engineering techniques at some stage of cultivation. Genetic modification would be feasible especially when genetically-engineered microorganism have been used in a fermentation process [2]. In summary, excellent biosorbents can be prepared from various raw biomass forms using the above-mentioned techniques. However, modifications increase the commercial cost of the biosorbents, bringing these closer to the price range of man-made ion-exchange resins. It should not be forgotten that the major advantage of biosorbents is their low cost relative to commercial adsorbents like ion-exchange

92

Table 5. Immobilization methods of biomass for use in process application Category

Detailed methods

Cell immobilization (on inert support material)

Immobilization of living cells on inert supports (sand, glass bead, paper or textile-making fibers, polymers, activated carbon, ÉíÅK) in a stage of cultivation; fåJëáíì immobilization of living biosorbents on inert supports within biosorption process reactors

Entrapment (within polymeric matrix)

Alginate, polyacrylamide, polyethylenine, polysulfone, polyurethane, polyhydroxyethylmethaacrylate, ÉíÅK

Cross-linking (using chemical linker)

Formaldehyde, glutaralhehyde, glutaric dialdehyde, divinylsulfone, formaldehyde-urea mixtures, epichlorohydrin (EPI), ethylene glycol diglycidiyl ether (EGDE), iminodiacetic acid, nitriloacetic acid, vinylketones, epoxides, organic diisocyanates, genipin, ÉíÅK

resins or activated carbons. Immobilization of Biomass for Process Application

Although some biosorbents have been shown to have greater adsorptive capacity than conventional ion-exchange resins, their uses in industrial applications are hinden by problems associated with the physical character of the biosorbents [2,23,50]. Microbial biosorbents are particularly problematic as they are such small particles, with low density, poor mechanical strength, and little rigidity. When used in column processes, difficulty in solid-liquid separation, possible biomass swelling, clogging, poor regeneration/reuse, and development of high pressure drop all can occur [2,53]. Fortunately, however, many of these problems can be overcome by use of immobilization techniques [50,53,67,71,75]. In addition, the immobilization procedure converts the biomass into a spherical shape, allowing it to be used like conventional adsorbents. Sizes ranges from 0.5 to 1.5 mm, with a good external porosity, and chemical and physical resistance, can generally be achieved for commercial adsorbent particles [67]. Immobilization of biomass is required for its use in conventional reactor technology in larger systems, especially in packed or fluidized bed reactors [75]. Of course, there are a few exceptions; such as when highly rigid and efficient biomass (e.g. seaweeds) is available, in which case a raw/unprocessed form may be used in a biosorption process without any prior immobilization step [2]. The use of flotation for separation of metal-loaded biomass from aqueous suspensions may also overcome the need for immobilization [76]. Various techniques have been used for the immobilization of biomass (Table 5), and in general can be divided into 3 categories; cell immobilization on inert supports, entrapment within a polymeric matrix, and cross-linking. Microbial biomass can be immobilized on various inert supports at

specific stages of its cultivation [50,53]. If living cells are directly used for a biosorption process, these can be easily immobilized within the process, in situ, and other pollutants may be removed simultaneously [39,76]. Small particles or powders of biomass can be easily immobilized within various polymeric matrixes [50,53]. This entrapment method has some benefits, including the control of particle size, high biomass loading, minimal clogging, and easy liquid separation and regeneration of the biosorbent [2]. Among various polymeric matrixes, alginate gel and polyacrylamide gel have been the most extensively used in laboratory studies, owing to their simple and rapid experimental protocols for encapsulation [50,51,67]. Cross-linking techniques employing chemical linkers have been also used by many researchers and these have sometimes resulted in the favorable modification of functionality of biosorbents [53,57,71]. Together with the cost of modifying raw biomass, the cost of its immobilization (if required) is an important factor in determining the overall cost of the commercial biosorbent produced. Various strategies for reducing/minimizing these steps have to be developed in order for these to be applied successfully and economically in industrial applications. The Biosorption Process

The application of biosorption in continuous processes has received increasing attention from researchers because of its potential industrial roles [67]. In fact, the decision of whether to use batch or continuous processes is a function of hydraulic flow, physical characters of the biosorbent(s), the types of target pollutant(s), space availability, and invested capital. If the flow rate is low, a simple manual batch process is the most economical [77]. Many different types of process configurations, such as stirred tank reactors, up-flow or downflow packed bed reactors, fluidized bed reactors, rotating contactors, trickle filters and air-lift reactors, have been proposed and investigated for their industrial practicality [40,75,77]. Most of these have been used in applications that employ living microorganisms for removal of metal contaminants from complex industrial wastewaters [40,78]. Among the continuous biosorption reactors, the down-flow packed bed reactor should theoretically be the most cost effective system, due to its complete dependence upon gravitational forces to transfer the water body through the bed. However, it is less easy to control effluent retention times within this type of reactor [77]. Consequently, the up-flow packed bed reactor, commonly called a column reactor, has been more extensively used in laboratory study, owing to its high operational yield and the relative ease of scaling up procedures to industrial capacities [2,7]. In fact, column biosorption reactor is a simple and reproducible method, and is commonly used to assess the pollutant removal performances of a biosorbent operating in a continuous mode. B. Volesky and his coworkers have long studied this type of biosorption reactor and detailed information has been described several times in their papers [7,41,43,79]. Stirred tank reactors may be operated in combination with a membrane system for liquid-solid separation. Fluidized


Table 6. Desorption methods for regeneration of biosorbenets and recovery of metals or dyes Category

Detailed methods

Physical microwaving, heating, ÉíÅK Acids (HCl, H2SO4, HNO3, H3PO4, acetic acid, Nondestructive Chemical ÉíÅK); Alkalis (NaOH, NH4OH, ÉíÅK); Organic solvents (methanol, ethanol, acetone, ÉíÅK) Others (CaCl2, KSCN, Na2CO3, KHCO3, EDTA, ÉíÅK) Destructive

incineration, dissolution into strong acids or alkalis, ÉíÅK

bed reactors have low mass transfer limitation relative to packed bed reactors. However, these reactors have been very rarely used for the purpose of biosorption using dead biomass. To achieve simple liquid-solid separation, some hybrid processes have been suggested in the literature. K. A. Matis and A. I. Zouboulis have studied the ‘biosorptive flotation’ process since 1993 [80,81]. Most recently, a biosorption process using bio-functional magnetic beads has been proposed by a few researchers [82]. Recovery and Regeneration

One of the important industrial applications of biosorption is recovery of loaded pollutants (especially valuable metals) from the biosorbent and simultaneous regeneration of the biosorbent for reuse. In fact, the usefulness of a specific biomass as a biosorbent depends not only on its biosorptive capacity, but also on the ease of its regeneration and reuse [45]. However, most researchers have tended to focus only on the biosorptive capacity of biosorbent tested, without consideration of the regeneration required for industrial applications [2]. The adsorbate bound onto the surface of a biosorbent through metabolism-independent biosorption may be easily desorbed by simple non-destructive physical/chemical methods using chemical eluants, but intracellularly bound adsorbate through metabolism-dependent bioaccumulation can be only released by destructive methods like incineration or dissolution into strong acids or alkalis [39,75]. If cheap biomass is used as a biosorbent for recovering rare and/or valuable metals, then destructive recovery would be economically feasible [50]. However, most attention to date has focused on non-destructive desorption from the loaded biosorbent [2,23]. For this reason, the choice between living or dead biomass systems is important because of the implication for later metal recovery [39]. As shown in Table 6, various chemical eluants have been tested for desorption of target materials from biosorbents. In many cases, dilute mineral acids or alkalis allow efficient desorption from the biosorbent, but they also cause serious structural damage to the biosorbent itself, resulting in a drop in the biosorptive capacity of the biosorbent following regeneration [2]. Organic solvents such as ethanol can be also used for desorbing organic pollutants such as dyes from the biosorbent [83]. Some-

Table 7. Published patents related to biosorption Title of the invention

Pub. Num.

Pub. Date

Apparatus for the biological treatment of waste water by the biosorption process

GB1324358 1973.07

Separation of uranium by biosorption

UP4320093 1982.03

Process for the separation of metals from aqueous media

UP4701261 1987.10

Removal of contaminants

UP4732681 1988.03

Biosorbent for gold

UP4769223 1988.09

Metal recovery

UP4898827 1990.02

Recovery of heavy and precious metals from aqueous solutions

WO9007468 1990.07

Removal of metal ions with immobilized metal ion-binding microorganisms

UP5055402 1991.10

Process and apparatus for removing heavy metals EP0475542 1992.03 from aqueous media by means of a bioadsorber Ionic binding of microbial biomass

WO9413782 1994.06

Polyaminosaccharide phosphate biosorbent

GB2306493 1997.05

Method for production of adsorption material

UP5648313 1997.07

Biosorption system

WO9826851 1998.06

Biosorbent for heavy metals prepared from biomass UP5789204 1998.08 Bacteria expressing metallothionein gene into the periplasmic space, and method of using such bacteria in environment cleanup

UP5824512 1998.10

Biosorption agents for metal ions and method for the production thereof

WO9848933 1998.11

Hydrophilic urethane binder immobilizing organisms having active sites for binding noxious materials

US5976847 1999.11

Process for producing chitosan-glucan complexes, US6333399 2001.12 compounds producible therefrom and their use Bioadsorption process for the removal of colour from textile effluent

WO0242228 2002.05

Heavy metal adsorbent composition

WO04022728 2004.03

A novel process for decolorization of colored effluents

WO06059348 2006.06

Process for the removal of metals by biosorption from mining or industrial effluents

US7326344 2008.02

times heating or microwaving can aid desorption with an eluant or mixture solution [84]. As well, as previously mentioned, the solution pH will have a strong influence on biosorption of a target pollutant; thus, simple manipulation of the pH of the desorbing solution should theoretically be a good method for regeneration of the biosorbent and recovery of the pollutant. Commercial Applications of Biosorption Technology

As many specialists in this area have frequently mentioned,

94

Table 8. Commercialized biosorbents Products

Remarks

TM

AlgaSORB

B.V. Sorbex Biosorbent

TM

Table 9. Guiding questions to be considered for commercial application of biosorption Category

Remarks

Biosorbent manufactured from a fresh water alga, `ÜäçêÉää~=îìäÖ~êáë, by being immobilized on silica

Effluent

Biosorbent manufactured from a variety of sources including the algae p~êÖ~ëëìã= å~í~åë, ^ëÅçéÜóäJ äìã= åçÇçëìã, e~äáãÉÇ~= çéìåíá~, m~äãóê~= é~ã~J Ç~, `ÜçåÇêìë=ÅêáëéìëI and `K=îìäÖ~êáë

Biosorbent Availability, overall manufacturing cost, regenerability and reusability, pollutant specificity, biosorptive capacity and rate, mechanical stability, ÉíÅK

Effluent volume, types of target pollutant and other contaminants, solution chemistry, pH, temperature, ÉíÅK

AMT-Bioclaim

Biosorbent manufactured from _~Åáääìë sp. by being immobilized with polyethyleneimine and glutaraldehyde

Process

Types of process, connection with other processes, operator’s skill, ÉíÅK

Bio-Fix

Biosorbent manufactured from a variety of sources including algae by being immobilized in porous polypropylene beads

Capital

Land space, construction cost, operating cost, ÉíÅK

Others

Disposal of exhausted biosorbent, recovery/reuse of metals in eluants, ÉíÅK

RAHCO Bio-Beads

Biosorbent prepared from a variety of sources including peat moss by being immobilized within an organic polymer

biosorption is a potent alternative technique for treating industrial wastewaters containing metals and/or dyes [2,7,16, 17]. The potential of biosorption is very great; for example, it may be used for the purification and recovery of rare proteins, steroids, pharmaceuticals, and drugs that are valued in thousands of dollars per gram [7]. For this reason, many biosorption processes are under development or have been developed and patented for commercial applications, as shown in Table 7. Pilot installations and a few commercialscale units have been constructed in the USA and Canada [38]. Through a pilot installation, M. Tsezos has confirmed the applicability of biosorption as the basis for sequestering or removing pollutants (especially uranium), but also found some limitations of this technique, i.e. difficulty in obtaining a reliable supply of inexpensive raw biomass, difficulty in regeneration and reuse of the biomass, and negative effects of co-existing ions on biosorptive capacity [38]. Although some biosorbents have been commercialized as adsorbents for removing/sequestering metals from aqueous solutions (Table 8), to the best of our knowledge, no industrial facility yet exists that uses these adsorbents at the present time. Thus, biosorption is not yet a proven technology, given its market history [2,38]. Recently, some researchers have highlighted questions that should be considered when evaluating the feasibility of a potential biosorbent for the removal of metals or dyes from industrial effluents [1,7,38,77]. These include the effluent characteristics, biosorbent characteristics, the biosorption process itself, and capital characteristics (Table 9). More information regarding the R&D work in the field of biosorption is available in a special volume published by B. Volesky, owner of BV Sorbex, Inc. [7,22].

BIOSORPTION MODELLING Appropriate models are useful for understanding process

mechanisms, analyzing experimental data, predicting answers to operational condition changes, and optimizing processes. In the field of biosorption, many researchers have developed/used various models for predicting/describing batch equilibria, batch kinetics and reactor operational data. Some useful review papers that focus on the modeling of biosorption are available in the literature [2,16,58,71,85-87]. Modeling of Batch Equilibrium Isotherms

The biosorption process involves a solid phase (sorbent) and a liquid phase (solvent, normally water) containing the dissolved species to be adsorbed (adsorbate). Quantification of adsorbate-adsorbent interactions is fundamental for the evaluation of potential implementation strategies. To compare pollutant uptake capacities of different types of biosorbents, adsorption phenomena can be expressed as batch equilibrium isotherm curves. These can be modeled by mechanistic or empirical equations; the former can explain, represent, and predict the experimental behavior, while the latter do not reflect the mechanism, but can reflect the experimental curves [2]. As shown in Table 10, empirical models involving 2, 3, or even 4 parameters have been used to fit batch equilibrium isotherm curves to biosorbents. Among these, the Langmuir and Freundlich models have been most commonly used, with a high rate of success. There are no critical reasons to use more complex models if the twoparameter models can fit the experimental data reasonably well [87]. Since many industrial wastewaters contain several components to be bound onto the biosorbent, a very judicious use is necessary for practical applications of effective multicomponent biosorption models [87]. Single component isotherm models have frequently been extended to the formation of multi-component ones (Table 10). Among these, in many cases, the extended Langmuir equation is found to fit the experimental data reasonably well. To characterize the competitive adsorption of biosorbents, a few researchers have successfully employed the Ideal Adsorbed Solution (IAS) theory using only single-component isotherm parameters [2].


Table 10. Equilibrium isotherm models System

Expression Langmuir [88]

Equation form

Remarks

q bC q= m e 1 + bCe

Monolayer sorption

Freundlich q = KCe1/ n [89] RT Temkin q= ln(aCe ) [90] b

Simple expression Considering temperature

⎡ Dubinnin⎛ 1 ⎞⎪⎫ ⎪⎧ Radush- q = qD exp ⎢−BD ⎨RT ln ⎜1+ ⎟⎬ ⎢ ⎪ ⎝ Ce ⎠⎪⎭ kevich [91] ⎩ ⎣

2

LangmuirqmbC Freundlich q = 1 + bC [92]

1/ n e 1/ n e

Single component

⎤ ⎥ Considering ⎥ temperature ⎦ Combination

RedlichPeterson [93]

q=

aCe 1 + bCen

Approaches Freundlich at high concentration

Sips [92]

q=

aCen 1 + bCen

Complicated

RadkearCen Prausnitz q = a + rCen −1 [94] Khan [95]

q=

Toth [96]

q=

Complicated

qmbCe (1 + bCe )n qm bCe

Complicated Complicated

{(1 + (bC ) } e

1/ n n

qmBCe Brunnauer q = (BET) [97] ( Cs −Ce ) 1+ ( B −1)( Ce / Cs )

{

Langmuir [88]

qi =

}

Multilayer sorption

qmi bi Ci N

Competitive

1 + ∑ ( bi Ci ) i =1

1/ ni

Multicomponent

Langmuir- q = qmi bi Ci N Freundlich i bi Ci1/ ni 1+ [92]

∑( i =1

RedlichPeterson [93]

qi =

)

Competitive

ai Ci

N

(

1 + ∑ bi Cini i =1

)

Competitive

Based on preliminary biomass characterization, with the formulation of a set of hypothesized reactions between the sorbent sites and solutes, some mechanistic models have been proposed and used to describe equilibrium data of metal biosorption in a single, binary, or multi-component system(s) [2]. These models revealed the complexity of biosorption phenomenon and also showed good agreement with experimental data. Although mechanical modeling requires titration or other biomass characterization data, in addition to the solution chemistry, this approach would be useful for the understanding and isolation of the operating binding mechanisms, as well as the proper and true representation of experimental sets [2]. Thermodynamics Study

An increase in temperature affects not only diffusion rate of adsorbate molecules from the solution to the adsorbent,

Table 11. Thermodynamic equations and their parameters (Crini and Badot, 2008) Expression

Equation form

E = − a + ln ka RT

Parameters Apparent activation energy

Arrhenius

ln kabs

Gibbs

⎛q ⎞ ΔG = − RT ln ⎜ e ⎟ ⎝ Ce ⎠

Free energy change

van’t Hoff

⎛q ⎞ ΔH ΔS + ln ⎜ e ⎟ = − C RT R ⎝ e⎠

Enthalpy change Entropy change

Clausiusclapeyron

ΔH =

− RT1T2 ( ln C2 − ln C1 ) T2 − T2

Enthalpy change

but also the solubility of the adsorbate molecules (especially in the case of dye biosoprtion) [71]. The adsorption characteristics of a material can be expressed in thermodynamic parameters such as ΔG (Gibbs free energy change), ΔH (enthalpy change), and ΔS (entropy change). These parameters can be calculated by using the thermodynamic equilibrium coefficient obtained at different temperatures and concentrations (Table 11), and their evaluation gives an insight into the possible mechanisms of adsorption [71]. At constant temperature and pressure, the ΔG value is the fundamental criterion of spontaneity. If this value is negative, then adsorption would take place, indicating the spontaneity of the reaction. By using the equilibrium constant obtained from the Langmuir model at each temperature, ΔG can be easily calculated according to the Gibbs expression, while ΔH and ΔS can be determined using the van’t Hoff plot (Table 11). It is important to note that the ΔG can be estimated from the equilibrium adsorption data under the assumption that the adsorption of a molecule is reversible and that an equilibrium condition is established in the batch system [71]. In addition, it should be also noted that, theoretically, the concentration of adsorbate used in the Langmuir isotherm equation must be expressed as its molar concentration [86,98]. However, in the literature of biosorption research, the volumetric concentration of adsorbate has been commonly used in the Langmuir isotherm equation without any theoretical consideration. This has eventually led to misapplication of the Langmuir isotherm equation in calculating the ΔG in thermodynamic studies [98,99]. Modeling of Batch Kinetics

Batch kinetic modeling is necessary to describe the response of the biosorption system to changes caused by variations in the experimental conditions and the properties of biosorbents, as well as, the parametric sensitivity of the model to process parameters [23,71,85,86]. The model results can be affected by biosorbent size, initial pollutant concentration, the maximum uptake capacity of biosorbent, mass transfer coefficients, and solute diffusivity. Thus, kinetics studies give detailed information on adsorbate uptake

96

Table 12. Adsorption kinetic models for biosorption Expression Second-order rate equation [85]

Equation form

1 1 = kt + Ct C0

Lagergren equation − kt [101] (Pseudo first- qt = qe 1 − e order model)

(

Remarks Early applied second-order rate equation in solid/liquid system

)

Based on adsorption capacity

Elovich equation [102]

⎛ 2.3 ⎞ ⎛ 2.3 ⎞ q = ⎜ ⎟ log ( t + t0 ) − ⎜ ⎟ log t0 Chemisorption ⎝α ⎠ ⎝α ⎠

Webber-Morris equation [100]

qt = kt1/ 2 + C

Intra-diffusion

Ho equation [85] (Pseudo secondorder model)

t 1 1 = + t qt k2 qe2 qe

Based on adsorption capacity

General rate raw equation [103]

−

dλt = k λtn dt

Non-fixed reaction order

rates and on rate-controlling steps such as external mass transfer, intraparticle mass transfer, and biosorptive reaction(s) [23]. Intraparticle diffusion has often been shown to be an important factor in determining the attainment of equilibrium in immobilized biosorbents [2]. To identify its involvement, batch kinetic data is fitted to an intraparticle diffusion plot, as suggested by Weber and Morris; i.e. qt = kt1/2 [100]. If this plot passes through the origin, then intraparticle diffusion is the rate-determining step. Various intra- or extramass transfer models in sorption studies have been well summarized in the literature [58]. However, it should be noted that the effects of transport phenomena and biosorptive reaction(s) are often experimentally inseparable [48]. Over 25 models have been introduced in attempts to quantitatively describe kinetic behavior during the adsorption process, but each model has its own limitations [2]. Table 12 shows representative kinetic models for a biosorptive reaction. Derivation of these equations as well as their physical meaning has been summarized in the literature [85,86]. In most cases, both pseudo-first- and second-order kinetic equations have been commonly employed in parallel, and one was often claimed to be better than the other, according to marginal differences in the correlation coefficient [85]. In general, the pseudo-second-order equation has been successfully applied to the biosorption of metal ions, dyes, herbicides, oils, and organic substances from aqueous solutions [86]. Due to the complexity of the biosorption mechanism, however, Y. Liu comments that, in theory, the order of a biosorption process must be determined by the general rate law equation, rather than preset-order kinetic equations [86,103]. He also comments that selection of a kinetic equation should be based on the mechanism since a good curve fitting cannot guarantee the physical meaning of the equation used. Fig. 3 shows model selection criteria in sorption studies, suggested by Gerente and his coworkers [58].

Fig. 3. Model selection criteria in sorption studies, suggested by Gerente Éí=~äK [58].

Modeling of a Continuous Biosorption Process

The model development of a continuous biosorption process would be helpful for evaluating the biosorptive performance of an industrial-scale process, based on data from laboratory-scale experiments. Good models cannot only help in analyzing and interpreting experimental data, but they also aid in predicting the response of the systems to changing conditions [41]. Due to its simple/reproducible method and the relative ease of scaling up the procedures, as mentioned before, an up-flow packed bed column reactor has been extensively used for laboratory study. Thus, almost all modeling of continuous biosorption process have been done with continuous operation of a column reactor [2]. The performance of continuous column operation is described through the concept of the breakthrough concentration curve of a target pollutant, which is typically S-shaped. Various parameters have been examined for its characterization, including the length of the sorption zone, uptake, removal efficiency, and slope of the breakthrough curve [2]. Flow rate, initial solute concentration, and the amount of biosorbent loaded also influence the biosorption performance of the column. Good biosorbents for the column reactor process are regarded as ones that show a delayed breakthrough, earlier exhaustion, a shorted mass transfer zone, high uptake, steep breakthrough curve, and high removal efficiency [2,7]. The breakthrough curves of a column reactor could be modeled using mathematical models or statistical approaches like neural networks, but the former have been preferred in this field. Table 13 shows typical models that have been tested for a packed-bed biosorption column; i.e. the BohartAdams, Thomas, Wolborska, Yoon-Nelson, Modified doseresponse, and Clark models. These models have primarily originated from research on activated carbon sorption, ion exchange, or chromatographic applications [2,7]. As a matter of course, reliable prediction of the concentration-time profile or effluent breakthrough curve is required for the successful design of a column biosorption process [7]. Among the column models, the Bohart-Adams and Thomas models have been found to fulfill this purpose and thus have


Table 13. Mathematical models for continuous biosorption processes Process CSTR

Expression

Equation form

dC j

dq Reversible mass V = v0C j 0 − v0C j − j Vxi transfer model [104] dt dt Bohart-Adams model [105]

⎛ C Z ⎞ = exp ⎜ kABC0t − kAB N 0 ⎟ C0 U0 ⎠ ⎝

Thomas model [106]

C0 ⎛k ⎞ = 1 + exp ⎜ TH ( Q0 M − C0Veff ) ⎟ C ⎝ F ⎠

Wolborska model [107]

⎛β C β Z⎞ C = exp ⎜ a 0 t − a ⎟ C0 U0 ⎠ ⎝ N0

PackedYoon-Nelson model bed R. [108]

exp ( kYN t − τ kYN ) C = C0 1 + exp ( kYN t − τ kYN )

Modified dose-response model [109]

C 1 = 1− a C0 1 + (Veff / bmdr ) mdr

Clark model [110]

⎛ ⎞ ⎜ ⎟ C ⎜ 1 ⎟ = n − 1 ⎟ C0 ⎜ ⎛ C0 ⎞ ⎜⎜ 1 + ⎜ n −1 − 1⎟ exp ( rtbreak − rt ) ⎟⎟ ⎠ ⎝ ⎝ Cbreak ⎠

1/ n −1

been widely applied to determine the characteristic parameters during the biosorption of a target pollutant [2,7]. Besides the typical models, mechanistic models that take mass transfer and/or diffusion into consideration have also been used to describe the column biosorption process [52,87]. In particular, B. Volesky and his coworkers have developed a good column model that can predict breakthrough curves of each element even in a mixture system [7,41,87]. However, many column modeling work needs to be done to allow industrial scale applications of biosorption.

COMMENTS AND SUGGESTIONS Many researchers have made valuable comments and/or suggestions on biosorption in their review papers and/or in supplemental publications such as notes or letters. We have summarized these comments and suggestions, and have added our own ideas regarding the current status of biosorption research. Selection of Potential Biomass

The application of untreated plant wastes as adsorbents can bring about a serious release of soluble organic compounds contained within the plant materials [54]. Thus, researchers have to consider this point when screening raw biomass for potential use in biosorption processes. Normally, biomass and biomass-driven biosorbents are biodegradable or decomposable. This property may be a

serious drawback for long-term applications in adsorption processes, in particular, in dynamic systems using fixed-bed columns [71]. The low thermal stability of biomass and its degradation resulting from desorbing agents are other important criteria that need to be taken into account. The cost of producing/cultivating microorganisms for the sole purpose of transformation into biosorbents has been shown to be too expensive. Furthermore, the continuous supply of biomass cannot be assured, which has a huge impact on its successful application in an actual industrial setting [2,38]. Quite a few researchers have been suggesting the use of their microbial biomass systems without adequately considering this point. Some researchers have reported useless case studies introducing new microbial or waste biomass systems that have very poor biosorptive capacity for heavy metals (even below 10 mg/g). Factors other than simply the availability and cheapness of biomass, especially the biosorptive capacity, need to be considered when selection of biomass is made. Batch Experiment

It is relatively simple and easy to obtain laboratory equilibrium biosorption data for a single adsorbate. Unfortunately, however, quite a few researchers err when obtaining data points for equilibrium isotherms. A general experimental procedure for this has been kindly described in a review paper [7], in which the importance of controlling environmental parameters (especially pH) at the given value over the entire period of contact time, until the sorption reaches its equilibrium state, was stressed. In studying biosorption behavior, we always have to avoid micro-precipitation phenomena and their contribution to the uptake of metals, by maintaining the pH of the sorption process [7]. Unfortunately, the effect of pH on the biosorption capacity of a given biosorbent is not always presented in the literature. It should not be forgotten that the neglect of a possible pH effect may lead to serious deviation in experimental results [16]. Although the solution pH changes during the course of an adsorption experiment, some researchers examine the pH effect only in terms of the initial pH of the aqueous solution before adding biosorbent [111,112]. Except in special cases, the solution pH should be constantly maintained at a given value during the course of a biosorption experiment by using acids/alkalis or buffer solutions. Modeling Work

G. McKay and his coworkers indicated common mistakes in equilibrium and kinetic modeling as follows [65]: many researchers failed to test experimental equilibrium data using several models and did not determine the best-fit model by error analysis or by postulating sorption mechanism(s). In addition, the application of more than one kinetic model is extremely rare. They also indicated little information on the characteristics of biosorbents tested, such as surface area,

98

pore size distribution, surface activity, particle size, hardness or attrition rates, and influence of pH. These are the key factors that need to be known in order to develop and design industrial biosorption systems. Due to the complexity of biosorption mechanism, Y. Liu commented that, in theory, the order of the biosorption process must be determined by the general rate law equation, rather than the preset-order kinetic equations [86,103]. He also commented that selection of kinetic equation should be based on the mechanism, since a good curve fitting cannot guarantee the physical meaning of the equation used. Although, theoretically, the concentration of adsorbate used in the Langmuir isotherm equation must be expressed as its molar concentration, the volumetric concentration of adsorbate has been commonly used in the biosorption research literature [86,98]. This has eventually led to misapplication of the Langmuir isotherm equation in calculating the ΔG in thermodynamic studies [98,99]. Modification Studies for Better Biosorbent

Although modification methods can cause mass loss of raw biomass, many researchers have evaluated these methods according to the biosorptive capacity of the modified biosorbent, without consideration of its overall mass yield. Together with the biosorptive capacities of raw biomass and the modified biosorbent, researchers also need to measure the weights of the biomass before and after the modification methods. In order for raw biomass to have enhanced sorption capacity, researchers may try to add the binding sites to and/or remove some interfering sites from the raw biomass or biomaterial. Once the chemically modified biosorbents are obtained, researchers should verify if the biomass are successfully modified. For this, instrumental analyses such as FTIR, XPS, and so on should be provided as evidences along with the experimental data indicating the enhanced uptake. Pretreatment of biomass increases the cost of biosorbents preparation. However, the enhanced sorption performance may compensate for the cost of modification steps. Therfore, cost aspects should be discussed with the effect of modification on the performace enhancement. Process Study

Many researchers have proposed the suitability of bacterial biomass for industrial applications, based on batch experimental results. However, a continuous mode of operation is preferred for most industrial applications. Thus, only careful and systematic investigation of biosorbent performance in a column mode will ensure its applicability to real situations [2]. Paper Publication

These days, a large number of manuscripts have been submitted to peer-reviewed international journals. As a result of the excessive work of editorial reviewers, as well as writing

skills of authors, duplicated or repeated work already performed by other researchers have been published, occasionally even in well-known journals. Some researchers have written “Salami slice” papers of low scientific quality, looking at experimental batch data combined with a fullyresearched adsorbate and a fully-researched biosorbent. Researchers should make an effort to publish more valuable and/or useful papers that make significant contributions to new knowledge in this area.

FUTURE DIRECTION Biosorption is in its developmental stages and further improvement in both performance and costs can be expected in future. We have summarized future directions of biosorption research, mentioned by other researchers in this area and also added our opinions. We must continue fundamental research to better understand the mechanisms of biosorption and on what drives the selectivity of biosorptive and bioaccumulatory processes [38]. Various high techniques like XAS will be helpful in this area. More comprehensive or specific models for equilibria or kinetic studies should be developed that can simulate more complex biosorption systems, such as hybrid biosorption system [68]. Unlike laboratory solutions, industrial effluents contain various pollutants including those of interest. Thus, there is a need to investigate the simultaneous removal of many coexisting pollutants. It is desirable to develop general-purpose biosorbents that can remove a variety of pollutants. One such possibility would be the use of ‘combo’ biosorbents consisting more than one type of biomass [23]. Although ‘combo’ biosorbents would tend to further complicate characterization of these biosorption systems, it may represent a more realistic approach to the design of biosorbent systems [50]. To date, there are no systematic or comparative studies taking into account the physicochemical properties of the different kinds of pollutant dyes. A more detailed study appears to be necessary to show how the chemical structure of a dye affects not only its adsorption capacitie, but also the understanding of the adsorption phenomena involved for that dye. Thus, more investigation should be focused on studying the influence of the chemical structure of dyes on their biosorption capacity [71]. Although chemical pretreatment methods significantly enhance biosorptive capacity and specificity of the biomass, these are not cost effective at large scale [5]. Further study is therefore required to drop the overall cost for pretreatments or to develop new methods that are both cheap and effective. The use of immobilized biomass, rather than native biomass, has been recommended for large-scale application of biosorption process. Immobilization techniques increase the overall cost of biosorbents, and decrease their biosorptive rates and capacities. Thus, more attention needs to be paid to this point. In addition, more work needs to be done to understand the effect of various immobilization techniques on the


rate and equilibrium uptake of pollutant by immobilized biomass. Biosorption processes are still at the stage of laboratoryscale study in spite of unquestionable progress. Thus, much work in this area is necessary to demonstrate its possibilities on an industrial scale [71]. So far, biosorption research has mainly aimed for the removal of pollutants such as heavy metals and organics. However, precious metal resources are getting paid attention because of their price increases and limited deposits. For the recovery of precious metals such as gold, platinum, palladium, ruthenium, etc. the performance-effectiveness would be more important property of sorbents than cost-effectiveness. With the purpose of their recovery, the recovery efficiency and purity of finally recovered products would be additional criteria for evaluating biosorbents and related processes. We expect that high-performance biosorbents will be used for the practical purpose in the near future. Biosorbents can be also used for the purification of ionic pharmaceuticals like proteins, antibodies, and peptides. For this, column chromatography would be more effective for the high-purity products than fixed or moving bed adsorption. Heat resistance of biosorbents and release of impurity during autoclave and purification must be considered for pharmaceutical applications. The difficulties that exist for biosorption application should be pushing researchers to consider applying hybrid technologies, which involve combining various processes for large-scale treatment of real wastewater [36,68]. This includes biosorption, bioreduction, bioprecipitation, flotation, membrane technology, and photochemical/electrochemical processes. Thus, the corresponding novel reactor systems should be designed and their operating conditions should be optimized for large scale use. When living cell systems are used to treat metal-containing wastewaters, the metal tolerances of the living cell is very important in its application in a real case. Genetic engineering may further enhance the potential of robust environmental strains [40]. However, the issue of living genetically modified organisms (LMO) should be addressed prior to field applications. The application of modern molecular biotechnology to microorganisms may greatly enhance the specificity of biosorbents, particularly if applied to synthesis of metal-specific peptides or cell wall polymer composition [50,68]. Protein engineering may also conceivably lead to enhanced metal specificity, stability, and other useful properties of peptides or other biopolymers [75]. In future, therefore, more attention should be given to these areas. Although biosorption is one of the main components of environmental biotechnology, to the best of our knowledge, there is neither an international conference nor a global network for researchers in this area. Needless to say, a weak relationship between researchers slows down development of biosorption technology and delays its commercialization. Acknowledgements

This work was supported by the

second phase of the Brain Korea 21 Program in 2009 at Kyungpook National University. This work was also supported by the KOSEF through the AEBRC at POSTECH and by the KOSEF NRL Program grant funded by the Korea government (MEST) (No. R0A-2008-000-20117-0). Received August 3, 2009; accepted September 12, 2009

REFERENCES 1. Krishnani, K. K. and S. Ayyappan (2006) Heavy metals remediation of water using plants and lignocellulosic agrowastes. Rev. Environ. Contam. Toxicol. 188: 59-84. 2. Vijayaraghavan, K. and Y. -S. Yun (2008) Bacterial biosorbents and biosorption. Biotechnol. Adv. 26: 266-291. 3. Hai, F. I., K. Yamamoto, and K. Fukushi (2007) Hybrid treatment systems for dye wastewater. Crit. Rev. Environ. Sci. Technol. 37: 315-377. 4. Crini, G. (2005) Recent developments in polysaccharide-based materials used as adsorbents in wastewater treatment. Prog. Polym. Sci. 30: 38-70. 5. Crini, G. (2006) Non-conventional low-cost adsorbents for dye removal: a review. Bioresour. Technol. 97: 1061-1085. 6. Vieira, R. H. S. F. and B. Volesky (2000) Biosorption: a solution to pollution? Int. Microbiol. 3: 17-24. 7. Volesky, B. (2007) Biosorption and me. Water Res. 41: 4017-4029. 8. Ahmaruzzaman, Md. (2008) Adsorption of phenolic compounds on low-cost adsorbents: a review. Adv. Colloid Interf. Sci. 143: 48-67. 9. Babel, S. and T. A. Kurniawan (2003) Low-cost adsorbents for heavy metals uptake from contaminated water: a review. J. Hazard. Mater. 97: 219-243. 10. Bailey, S. E., T. J. Olin, R. M. Bricka, and D. D. Adrian (1999) A review of potentially low-cost sorbents for heavy metals. Water Res. 33: 2469-2479. 11. Bhatnagar, A. and A. K. Minocha (2006) Conventional and non-conventional adsorbents for removal of pollutants from water - a review. Indian J. Chem. Technol. 13: 203-217. 12. Kurniawan, T. A., G. Y. S. Chan, W.-H. Lo, and S. Bebel (2006) Comparisons of low-cost adsorbents for treating wastewaters laden with heavy metals. Sci. Total Environ. 366: 409-426. 13. Lin, S.-H. and R.-S. Juang (2009) Adsorption of phenol and its derivatives from water using synthetic resins and low-cost natural adsorbents: a review. J. Environ. Manage. 90: 1336-1349. 14. Mohan, D. and C. U. Pittman, Jr. (2006) Activated carbon and low cost adsorbents for remediation of tri- and hexavalent chromium from water. J. Hazard. Mater. 137: 762-811. 15. Mohan, D. and C. U. Pittman, Jr. (2007) Arsenic removal from water/wastewater using adsorbents-a critical review. J. Hazard. Mater. 142: 1-53.

100

16. Aksu, Z. (2005) Application of biosorption for the removal of organic pollutants: a review. Process Biochem. 40: 997-1026. 17. Sağ, Y. and T. Kutsal (2001) Recent trends in the biosorption of heavy metals: a review. Biotechnol. Bioprocess Eng. 6: 376-385. 18. McCallan, S. E. A. and L. P. Miller (1956) Innate toxicity of fungicides. pp. 107-134. In: R. L. Metcalf (ed.). Advanced in Pest Control Research: Vol. II. Interscience, NY, USA. 19. Muraleedharan, T. R., L. Iyengar, and C. Venkobachar (1991) Biosorption: an attractive alternative for metal removal and recovery. Curr. Sci. 61: 379-385. 20. John Wase, D. A. and C. F. Forster (1997) Biosorbents for metal ions. CRC Press, Florida, USA. 21. Volesky, B. (1990) Biosorption of heavy metals. CRC Press, Florida, USA. 22. Volesky, B. (2004) Sorption and biosorption. BVSorbex Inc., Quebec, Canada. 23. Modak, J. M. and K. A. Natarajan (1995) Biosorption of metals using nonliving biomass-a review. Miner. Metall. Proc. 12: 189-196. 24. Ullrich, A. H. and M.W. Smith (1951) The biosorption process of sewage and waste treatment. Sewage Ind. Wastes 23: 1248-1253. 25. Stasiak, M. (1969) Application of biosorption process for renovation of waste waters at chemical industry, Przemysl Chemiczny 48: 426-428. 26. Ames Crosta Mills & Company Ltd. and J. R. Sanderson (1973) Apparatus for the biological treatment of waste water by the biosorption process. Great Britain Patent GB1324358. 27. Ruchoft, C. C. (1949) The possibilities of disposal of radio active wastes by biological treatment methods. Sewage Works J. 21: 877-883. 28. Volesky, B. and M. Tsezos (1982) Separation of uranium by biosorption. US Patent US04320093. 29. Goodman, G. T. and T. M. Roberts (1971) Plants and soils as indicators of metals in the air. Nature 231: 287292. 30. Neufeld, R. D. and E. R. Hermann (1975) Heavy metal removal by acclimated activated sludge. J. Water Pollut. Control Fed. 47: 310-329. 31. Friedman, B. A. and P. R. Dugan (1968) Concentration and accumulation of metallic ions by the bacterium Zoogloea. Dev. Ind. Microbiol. 9: 381-388. 32. Nakajima, A., T. Horikoshi, and T. Sakaguchi (1982) Studies on the accumulation of heavy metal elements in biological systems. J. Appl. Microbiol. 16: 88-91. 33. Sakaguchi, T., A. Nakajima, and T. Horikoshi (1978) Studies on the accumulation of heavy metal elements in biological systems: VI. Uptake of uranium from sea water by microalgae. J. Ferment. Technol. 56: 561-565. 34. Gould, M. S. and E. J. Genetelli (1984) Effects of competition on heavy metal binding by anaerobically digested sludges. Water Res. 18: 123-126. 35. Chiu, Y., M. Asce, and J. E. Zajic (1976) Biosorption isotherm for uranium recovery. J. Environ. Eng. ASCE

102: 1109-1111. 36. Tsezos, M. and B. Volesky (1981) Biosorption of uranium and thorium. Biotechnol. Bioeng. 23: 583-604. 37. Steen, W. C. and S. W. Karickhoff (1981) Biosorption of hydrophobic organic pollutants by mixed microbial populations. Chemosphere 10: 27-32. 38. Tsezos, M. (2001) Biosorption of metals: the experience accumulated and the outlook for technology development. Hydrometallurgy 59: 241-243. 39. Gadd, G. M. (1990) Heavy metal accumulation by bacteria and other microorganisms. Experientia 46: 834-840. 40. Malik, A. (2004) Metal bioremediation through growing cells. Environ. Int. 30: 261-278. 41. Kratochvil, D. and B. Volesky (1998) Advances in the biosorption of heavy metals. Trends Biotechnol. 16: 291-300. 42. Volesky, B. (1994) Advances in biosorption of metals: selection of biomass types. FEMS Microbiol. Rev. 14: 291-302. 43. Volesky, B. and Z. R. Holan (1995) Biosorption of heavy metals. Biotechnol. Progr. 11: 235-250. 44. Ahluwalia, S. S. and D. Goyal (2007) Microbial and plant derived biomass for removal of heavy metals from wastewater. Bioresour. Technol. 98: 2243-2257. 45. Bishnoi, N. R. and A. Garima (2005) Fungus-an alternative for bioremediation of heavy metal containing wastewater: a review. J. Sci. Ind. Res. 64: 93-100. 46. Gupta, R. and H. Mohapatra (2003) Microbial biomass: an economical alternative for removal of heavy metals from waste water. Indian J. Exp. Biol. 41: 945-966. 47. Kaushik, P. and A. Malik (2009) Fungal dye decolourization: recent advances and future potential. Environ. Int. 35: 127-141. 48. Lodeiro, P., R. Herrero, and M. E. Sastre de Vicente (2006) Thermodynamic and kinetic aspects on the biosorption of cadmium by low cost materials: a review. Environ. Chem. 3: 400-418. 49. Mack, C., B. Wilhelmi, J. R. Duncan, and J. E. Burgess (2007) Biosorption of precious metals. Biotechnol. Adv. 25: 264-271. 50. McHale, A. P. and S. McHale (1994) Microbial biosorption of metals: potential in the treatment of metal pollution. Biotechnol. Adv. 12: 647-652. 51. Mehta, S. K. and J. P. Gaur (2005) Use of algae for removing heavy metals ions from wastewater: progress and prospects. Crit. Rev. Biotechnol. 25: 113-152. 52. Sağ, Y. (2001) Biosorption of heavy metals by fungal biomass and modeling of fungal biosorption: a review. Separ. Purif. Method 30: 1-48. 53. Veglio, F. and F. Beolchini (1997) Removal of metals by biosorption: a review. Hydrometallurgy 44: 301-316. 54. Wan Ngah, W. S. and M. A. K. M. Hanafiah (2008) Removal of heavy metal ions from wastewater by chemically modified plant wastes as adsorbents: a review. Bioresource Technol. 99: 3935-3948. 55. Wilde, E. W. and J. R. Benemann (1993) Bioremoval of heavy metals by the use of microalgae. Biotechnol. Adv. 11: 781-812.


56. Romera, E., F. González, A. Ballester, M. L. Blázquez, and J. A. Muñoz (2006) Biosorption with algae: a statistical review. Cri. Rev. Biotechnol. 26: 223-235. 57. Varma, A. J., S. V. Deshpande, and J. F. Kennedy (2004) Metal complexation by chitosan and its derivatives: a review. Carbohyd. Polym. 55: 77-93. 58. Gerente, C., V. K. C. Lee, P. Le Cloirec, and G. MaKay (2007) Application of chitosan for the removal of metals from wastewaters by adsorption - mechanisms and models review. Crit. Rev. Environ. Sci. Technol. 37: 41-127. 59. Demirbas, A. (2008) Heavy metal adsorption onto agrobased waste materials: a review. J. Hazard. Mater. 157: 220-229. 60. Johnson, T. A., N. Jain, H. C. Joshi, and S. Prasad (2008) Agricultural and agro-processing wastes as low cost adsorbents for metal removal from wastewater: a review. J. Sci. Ind. Res. 67: 647-658. 61. Mahvi, A. H. (2008) Application of agricultural fibers in pollution removal from aqueous solution, Int. J. Environ. Sci. Tech. 5: 275-285. 62. Sud, D., G. Mahajan, and M. P. Kaur (2008) Agricultural waste material as potential adsorbent for sequestering heavy metal ions from aqueous solutions-a review. Bioresour. Technol. 99: 6017-6027. 63. Swami, D. and D. Buddhi (2006) Removal of contaminants from industrial wastewater through various nonconventional technologies: a review. Int. J. Environ. Pollut. 27: 324-346. 64. O’Connell, D. W., C. Birkinshaw, and T. F. O’Dwyer (2008) Heavy metal adsorbents prepared from the modification of cellulose: a review. Bioresour. Technol. 99: 6709-6724. 65. McKay, G., Y. S. Ho, and J. C. Y. Ng (1999) Biosorption of copper from waste waters: a review. Separ. Purif. Method 28: 87-125. 66. Popa, K. and A. Cecal (2003) A review on biosorption of uranyl ions. Environ. Eng. Manage. J. 2: 69-75. 67. Andrès, Y., A. C. Texier, and P. Le Cloirec (2003) Rare earth elements removal by microbial biosorption: a review. Environ. Technol. 24: 1367-1375. 68. Wang, J. and C. Chen (2006) Biosorption of heavy metals by Saccharomyces cerevisiae: a review. Biotechnol. Adv. 24: 427-451. 69. Pal, A. and A. K. Paul (2008) Microbial extracellular polymeric substances: central elements in heavy metal bioremediation. Indian J. Microbiol. 48: 49-64. 70. Gupta, R., P. Ahuja, S. Khan, R. K. Saxena, and H. Mohapatra (2000) Microbial biosorbents: meeting challenges of heavy metal pollution in aqueous solutions. Curr. Sci. 78: 967-973. 71. Crini, G. and P.-M. Badot (2008) Application of chitosan, a natural aminopolysaccharide, for dye removal by aqueous solutions by adsorption processes using batch studies: a review of recent literature. Prog. Polym. Sci. 33: 399-447. 72. Chandana Lakshmi, M. V. V., V. Sridevl, and S. K. Beebl (2007) A review on biosorption of heavy metals from industrial effluents. Indian J. Environ. Prot. 27:

545-553. 73. Ioannidou, O. and A. Zabaniotou (2007) Agricultural residues as precursors for activated carbon production-a review. Renew. Sust. Energ. Rev. 11: 1966-2005. 74. Suhas, P., J. M. Carrott, and M. M. L. Ribeiro Carrott (2007) Lignin - from natural adsorbent to activated carbon: a review. Bioresour. Technol. 98: 2301-2312. 75. Gadd, G. M. and C. White (1993) Microbial treatment of metal pollution - a working biotechnology? Trends Biotechnol. 11: 353-359. 76. Kapoor, A. and T. Viraraghavan (1995) Fungal biosorption - an alternative treatment option for heavy metal bearing wastewaters: a review. Bioresour. Technol. 53: 195-206. 77. Atkinson, B. W., F. Bux, and H. C. Kasan (1998) Considerations for application of biosorption technology to remediate metal-contaminated industrial effluents. Water SA 24: 129-135. 78. Gavrilescu, M. (2004) Removal of heavy metals from the environment by biosorption. Eng. Life Sci. 4: 219-232. 79. Volesky, B. (1987) Biosorbents for metal recovery. Trends Biotechnol. 5: 96-101. 80. Zouboulis, A. I., N. K. Lazaridis, and K. A. Matis (2008) The process of flotation: an efficient solid/liquid separation technique for biological materials. Int. J. Environ. Pollut. 32: 29-42. 81. Zouboulis, A. I. and K. A. Matis (1997) Removal of metal ions from dilute solutions by sorptive flotation. Crit. Rev. Environ. Sci. Technol. 27: 195-235. 82. Li, H., Z. Li, T. Liu, X. Xiao, Z. Peng, and L. Deng (2008) A novel technology for biosorption and recovery hexavalent chromium in wastewater by bio-functional magnetic beads. Bioresour. Technol. 99: 6271-6279. 83. Binupriya, A. R., M. Sathishkumar, D. Kavitha, K. Swaminathan, and S. E. Yun (2007) Aerated and rotated mode of decolorization of a textile dye solution by native and modified mycelial biomass of Trametes versiocolor. J. Chem. Technol. Biotechnol. 82: 350-359. 84. Kuyucak, N. and B. Volesky (1989) Desorption of cadmium from algal biosorbent. Biotechnol. Bioeng. 33: 815-822. 85. Ho, Y.-S. (2006) Review of second-order models for adsorption systems. J. Hazard. Mater. 136: 681-689. 86. Liu, Y. and Y.-J. Liu (2008) Biosorption isotherms, kinetics, and thermodynamics. Sep. Purif. Technol. 61: 229-242. 87. Volesky, B. (2003) Biosorption process simulation tools. Hydrometallurgy 71: 179-190. 88. Langmuir, I. (1918) The adsorption of gases on plane surfaces of glass, mica, and platinum. J. Am. Chem. Soc. 40: 1361-1403. 89. Freundlich, H. (1907) Ueber die adsorption in Loesungen. Z. Phy. Chem. 57: 385-470. 90. Temkin, D. (1934) Die gas adsorption under nernstsche wärmesatz. Acta. Physicochima URSS 1: 36-52. 91. Dubinin, M. M. (1960) The potential theory of adsorption of gases and vapors for adsorbents with energeticcally non-uniform surface. Chem. Rev. 60: 235-266.

102

92. Sips, R. (1948) On the structure of a catalyst surface. J. Chem. Phys. 16: 490-495. 93. Redlich, O. and D. L. Peterson (1959) A useful adsorption isotherm. J. Phys. Chem. 63: 1024-1024. 94. Radke, C. J. and J. M. Prausnitz (1972) Adsorption of organic solutions from dilute aqueous solution on activated carbon. Ind. Eng. Chem. Fund. 11: 445-451. 95. Khan, A. R., A. Ataullah, and A. Al-Haddad (1997) Equilibrium adsorption studies of some aromatic pollutants from dilute aqueous solutions on activated carbon at different temperatures. J. Colloid Interf. Sci. 194: 154-165. 96. Toth, J. (1971) State equations of the solid gas interface layer. Acta Chim. Acad. Sci. Hung. 69: 311-328. 97. Brunauer, S., P. H. Emmett, and E. Teller (1938) Adsorption of gases in multimolecular layers. J. Am. Chem. Soc. 60: 309-319. 98. Liu, Y. (2006) Some consideration on the Langmuir isotherm equation. Colloid Surf. A.: Physicochem. Eng. Aspects 274: 34-36. 99. Lu, X. (2008) Comment on “Thermodynamic and isotherm studies of the biosorption of Cu(II), Pb(II), and Zn(II) by leaves of saltbush (Atriplex canescens)”. J. Chem. Thermodyn. 40: 739-740. 100. Weber, W. J. and J. C. Morris (1963) Kinetics of adsorption on carbon solution. J. Sanit. Eng. Div. Am. Soc. Civ. Eng. 89: 31-59. 101. Lagergren, S. (1898) Zur theorie der sogenannten adsorption gelöster stoffe. K. Sven. Vetenskapsakad. Handl. 24: 1-39. 102. Zeldowitsch, J. (1934) Über den mechanismus der katalytischen oxidation von CO an MnO2. Acta Phys-

icochim. URSS 1: 364-449. 103. Liu, Y. and L. Shen (2008) A general rate law equation for biosorption. Biochem. Eng. J. 38: 390-394. 104. Sağ, Y., A. Yalçuk, and T. Kutsal (2000) Mono and multi-component biosorption of heavy metal ions on Rhizopus arrhizus in a CFST. Process Biochem. 35: 787-799. 105. Bohart, G. and E. Q. Adams (1920) Some aspects of the behavior of charcoal with respect to chlorine. J. Am. Chem. Soc. 42: 523-544. 106. Thomas, H. C. (1944) Heterogeneous ion exchange in a flowing system. J. Am. Chem. Soc. 66, 1664-1666. 107. Wolborska, A. (1989) Adsorption on activated carbon of p-nitrophenol from aqueous solution. Water Res. 23: 85-91. 108. Yoon, Y. H. and J. H. Nelson (1984) Application of gas adsorption kinetics. I. A theoretical model for respirator cartridge service time. Am. Ind. Hyg. Assoc. J. 45: 509516. 109. Yan, G., T. Viraraghavan, and M. Chen (1999) A new model for heavy metal removal in a biosorption column. Adsorpt. Sci. Technol. 19: 25-43. 110. Clark, R. M. (1987) Evaluating the cost and performance of field-scale granular activated carbon systems. Environ. Sci. Technol. 21: 573-580. 111. Tien, C. (2007) Remarks on adsorption manuscripts received and declined: an editorial. Sep. Purif. Technol. 54: 277-278. 112. Tien, C. (2008) Remarks on adsorption manuscripts revised and declined: an editorial. J. Hazard. Mater. 150: 2-3.