Application of Ion For The Removal of Organic Pollutants

Process Biochemistry 40 (2005) 9971026
Review
Application of biosorption for the removal of organic pollutants: a review

Zmriye Aksu
Department of Chemical Engineering, Hacettepe University, Beytepe, Ankara 06532, Turkey Received 30 September 2003; received in revised form 26 March 2004; accepted 4 April 2004
Abstract In modern society, an increasing number of hazardous organic compounds are being discharged into the environment. Most are degraded or detoxicated by physical, chemical and biological treatments before released into the environment. Although the biological treatments are a removal process for some organic compounds, their products of biodegradation may also be hazardous. Moreover, some nondegradable compounds discharged into the environment along with the treated compounds can cause problems because they usually come back to humanbeings through the several channels such as bioaccumulation. As a result, organic molecules that are not biodegradable, can still be removed from the wastewater by the microbial biomass via the process of biosorption. Biosorption is also becoming a promising alternative to replace or supplement the present removal processes of organic pollutants from wastewaters. Among these pollutants, dyes, phenolics and pesticides have recently been of great concern because of the extreme toxicity and/or persistency in the environment. Biosorption of these type of hazardous organics by selected live and dead microoganisms has been investigated by various workers. This review examines a wide variety of microorganisms (fungi, yeasts, bacteria, etc.), which are capable of uptake of organic pollutants, discusses various mechanisms involved in biosorption, discusses the effects of various parameters such as pH, temperature, concentrations of organic pollutant, other ions, and biomass in solution, pretreatment method, etc. on biosorption, reports some elution and regeneration methods for biomass; summarizes the equilibrium and kinetic models used in batch and continuous biosorption systems which are important to determine the biosorption capacity of microorganism and to design of treatment processes. 2004 Elsevier Ltd. All rights reserved.
Keywords: Biosorption; Organic pollutant; Microorganism; Batch system; Continuous system; Equilibrium; Kinetics
1. Introduction A great number of industry such as textile, paper and pulp, printing, iron-steel, coke, petroleum, pesticide, paint, solvent, pharmaceutics, wood preserving chemicals, consume large volumes of water, and organic based chemicals. These chemicals show a great difference in chemical composition, molecular weight, toxicity, etc. Efuents of these industries may also contain undesired quantities of these pollutants and need to be treated. Synthetic dyestuffs, one group of organic pollutants, are used extensively in textile, paper, printing industries and dyehouses. It is reported that there are over 100,000 commercially available dyes with a production of over 7 105 metric tonnes per year [1,2]. Dyeing industry efu
Tel.: +90-312-2977434; fax: +90-312-2992124. E-mail address: zaksu@hacettepe.edu.tr (Z. Aksu).
ents constitute one of the most problematic wastewaters to be treated not only for their high chemical and biological oxygen demands, suspended solids and content in toxic compounds but also for colour, which is the rst contaminant to be recognized by human eye. Dyes may signicantly affect photosynthetic activity in aquatic life due to reduced light penetration and may also be toxic to some aquatic life due to the presence of aromatics, metals, chlorides, etc., in them [16]. Dyes usually have a synthetic origin and complex aromatic molecular structures which make them more stable and more difcult to biodegrade. Dyes are classied as follows: anionicdirect, acid and reactive dyes; cationicbasic dyes; non-ionicdisperse dyes [3,5]. The chromophores in anionic and non-ionic dyes are mostly azo groups or anthraquinone types. The reductive cleavage of azo linkages is responsible for the formation of toxic amines in the efuent. Anthraquinone-based dyes are more resistant to degradation due to their fused aromatic
0032-9592/$ see front matter 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.procbio.2004.04.008
998
Z. Aksu / Process Biochemistry 40 (2005) 9971026
structures and thus remain coloured for a longer time in the wastewater. Reactive dyes are typically azo-based chromophores combined with different types of reactive groups e.g., vinyl sulfone, chlorotriazine, trichloropyrimidine, diuorochloropyrimidine. They differ from all other classes of dyes in that they bind to the textile bres such as cotton to through covalent bonds. They are used extensively in textile industries regarding favorable characteristics of bright colour, water-fast, simple application techniques with low energy consumption. Water-soluble reactive and acid dyes are the most problematic, as they tend to pass through conventional treatment systems unaffected. Hence, their removal is also of great importance [613]. Basic dyes have high brilliance and intensity of colours and are highly visible even in a very low concentration [1,4,5,1416]. Metal complex dyes are mostly based on chromium, which is carcinogenic [1,3,4,17]. Disperse dyes do not ionize in an aqueous medium and some disperse dyes have also been shown to have a tendency to bioaccumulate [4]. Due to the chemical stability and low biodegradability of these dyes, conventional biological wastewater treatment systems are inefcient in treating dye wastewater. Dye wastewater is usually treated by physical- or chemical-treatment processes. These include chemical coagulation/occulation, ozonation, oxidation, ion exchange, irradiation, precipitation and adsorption [36,8,1727]. Some of these techniques have been shown to be effective, although they have limitations. Among these are: excess amount of chemical usage, or accumulation of concentrated sludge with obvious disposal problems; expensive plant requirements or operational costs; lack of effective colour reduction; and sensitivity to a variable wastewater input. In recent years, a number of studies have focused on some microorganisms which are able to biodegrade or to bioaccumulate azo dyes in wastewaters. A wide variety of microorganisms including bacteria, fungi and algae are capable of decolourizing a wide range of dyes via anaerobic, aerobic, and sequential anaerobicaerobic treatment processes [46,28,29]. Cytoplasmic azo reductases play an important role in the anaerobic biodegradation of azo dyes to produce colourless aromatic amines although complete mineralization is difcult and the resulting aromatic amines may be toxic and carcinogenic. These amines are resistant to further anaerobic mineralization. Fortunately, once the xenobiotic azo component of the dye molecule has been removed, the resultant amino compounds are good substrates for aerobic biodegradation suggesting a choice of a sequential anaerobicaerobic system for wastewater treatment. Although a number of aerobic biological processes for the removal of dyes from textile efuents have been explored, such as decolourization through liquid fermentations by white-rot fungi (among these microorganisms Phanerochaete chrysosporium, Trametes versicolor, Coriolus versicolor biotransformed or mineralized several azo dyes through catalytic action of extracellular enzymes, such as lignin peroxidases and manganese dependent peroxidase) and bacterial cultures (such
as Pseudomonas strains, mixed bacterial cultures, Bacillus subtilis), yeasts (such as Klyveromyces marxianus, Candida zeylanoides), biochemical oxidation suffers from signicant limitations since more dyestuffs found in the commercial market have been intentionally designed to be resistant to aerobic microbial degradation. Reactive azo dyes are electron decient in nature and this property makes them less susceptible to oxidative catabolism. Research has shown that the efciency of biological treatment systems is greatly inuenced by the operational parameters, the composition of textile wastewater and the structure and substituents of dye molecule. The level of aeration, temperature, pH, and redox potential of the system are the variables that should be optimized to produce the maximum rate of dye reduction. To test the ability of microorganisms to reduce dyes from a range of dye classes (acidic, basic, direct, disperse, metal-complex, reactive) is also important to determine the types of wastewater that can be treated by the system. The composition of textile wastewater is varied and can include organics, nutrients, salts, sulfur compounds and toxicants as well as the colour, so the inhibitory effect of any of these compounds on the dye reduction process should be investigated [46,28,3035]. The other biological treatment method; bioaccumulation is dened as the accumulation of pollutants by actively growing cells by metabolism- and temperature-independent and metabolism-dependent mechanism steps. Although bioaccumulation of dyes by yeasts [36,37] were accomplished, however, there are signicant practical limitations regarding the inhibition of cell growth at high dye concentrations and requirement of metabolic energy externally provided. So there is a need to nd alternative treatment methods that are effective in removing dyes from large volumes of efuents and are low in cost, such as biosorption. Phenols, another group of organic pollutants are considered as priority pollutants since they are harmful to organisms at low concentrations and many of them have been classied as hazardous pollutants because of their potential to harm human health. It should be noted that the contamination of drinking water by phenolics at even a concentration of 0.005 mg l1 could bring about signicant taste and odor problems making it unt for use. Human consumption of phenol-contaminated water can cause severe pain leading to damage of the capillaries ultimately causing death. Phenol containing water, when chlorinated during disinfection of water also results in the formation of chlorophenols. The most important pollution sources containing phenols and phenolic compounds such as nitrophenols, chlorophenols, are the wastewaters from the iron-steel, coke, petroleum, pesticide, paint, solvent, pharmaceutics, wood preserving chemicals, and paper and pulp industries [3841]. Current methods for removing phenolics from wastewater include microbial degradation, adsorption on activated carbon, chemical oxidation (using agents such as ozone, hydrogen peroxide or chlorine dioxide), deep-well injection, incineration, solvent extraction and irradiation. Solvent extraction
999
methods are expensive, and deep-well injection may lead to contamination of ground water. Adsorption and oxidation treatments become exceedingly expensive when low efuent concentrations must be achieved. Wastewaters containing phenol in the range of 5500 mg l1 are considered suitable for treatment by biological processes. Although biological treatment has shown great promise, a wide variety of pure and mixed cultures of microorganisms are capable of degrading phenol and phenolics under both aerobic and anaerobic conditions and microbial degradation of these compounds is seen as a cost effective method, the biological treatment of phenolics is limited by the intrinsic properties of these compounds owing to their toxicity; they are slow to biodegrade, and the degrading microorganism must be exposed to only low concentrations of the substrates. Therefore, alternative technologies have to be explored [4255]. Advancing increase of production and application of pesticides for agriculture as well as for plant protection and animal health has caused the pollution of soil, ground and surface water which involves a serious risk to the environment and also to the human health due to direct exposure or through residues in food and drinking water. In the world, alarming levels of pesticides have been reported in air, water, soil as well as in foods and biological materials. Some of these pesticides have been reported to be persistent, toxic, mutagenic, carcinogenic, and tumorogenic. Pesticide contamination of water systems has been of major concern in recent years. Pesticide residues reach the aquatic environment through manufacturing plants, direct surface run-off, leaching, careless disposal of empty containers, equipment washings, etc. Pesticides are divided into many classes, of which the most important are organochlorine and organophosphorous compounds. The chemical stability of organochlorine compounds is reected in their resistance to microbial degradation. The lipophilic nature, hydrophobicity and low chemical and biological degradation rates of organochlorine pesticides have led to their accumulation in biological tissues and subsequent magnication of concentrations in organisms progressing up the food chain. Organophosphorous pesticides on the other hand are known to degrade rapidly depending on their formulation, method of application, climate and the growing stage of the plant. The most important and common pollutants among organochlorine pesticides are dichlorodiphenyltrichloroethane and its metabolites (DDTs), polychlorinated biphenyls (PCBs), hexachlorocyclohexane isomers (HCHs), chlordane related compounds (CHLs), hexachlorobenzene (HCB), cyclodienes, dieldrin, etc. The wide range of pesticides used makes it extremely difcult to produce a single method for pesticide disposal that applies universally. Photochemical or chemical treatments are frequently inefcient for the removal of synthetic organochlorine pesticides from waters and may also lead to hazardous nal products. On the other hand, advanced water treatment processes, and mainly the adsorption onto activated carbon, have proved to be the most efcient and reliable method for the removal of aqueous-dissolved organic pesticides. In
recent years the ability of microorganisms to metabolize some pesticides has also received much attention due to the environmental persistence and toxicity of these chemicals. Although in some cases, microbial metabolism of contaminants may produce toxic metabolites, a variety of microorganisms (many aerobic bacteria and fungi) are known to utilize organic pesticides as the sole carbon or energy source, such as Pseudomonas pickettii, Alcalilgenes eutrophus, Desulfomonile tiedjei, Phanerochaete chrysosporium, etc. However, conventional activated sludge systems often fail to achieve high efciency in removing pesticides from wastewater due to the low biodegradability and toxicity or inhibition of organic pesticides to microorganisms [5663]. Adsorption has been shown to be the most promising option for all these non-biodegradable organics for the removal from aqueous streams, activated carbons being the most common adsorbent for this process due to its effectiveness and versatility. Activated carbons are usually obtained from materials with a high carbon content and possess a great adsorption capacity, which is mainly determined by their porous structure. Although activated carbon, in granular or powdered form has a good capacity for the adsorption of organic molecules, it suffers from a number of disadvantages. Activated carbon is quite expensive and the higher the quality the greater the cost. Both chemical and thermal regeneration of spent carbon is expensive, impractical on a large scale and produces additional efuent and results in considerable loss of the adsorbent. This has led many workers to search for the use of cheap and efcient alternative materials such as bagasse pith, carbonized bark, peat, soil, tree, and eucalyptus barks, chitin, rice husk, wood, y ash, and carbonized sewage sludge. However, these low-cost adsorbents have generally low adsorption capacities so large amounts of adsorbents will be needed [5,6,8,9,1727,3850,5662]. Alternatively, the so-called biosorption, i.e. the passive uptake of pollutants from aqueous solutions by the use of non-growing or non-living microbial mass, thus allowing the recovery and/or environmentally acceptable disposal of the pollutants, could also be considered. The special surface properties of bacteria, yeasts, fungi and algae enable them to adsorb different kinds of pollutants from solutions. Biosorption term is used to indicate a number of metabolism-independent processes (physical and chemical adsorption, electrostatic interaction, ion exchange, complexation, chelation, and microprecipitation) taking place essentially in the cell wall rather than oxidation though anaerobic or aerobic metabolism (biodegradation). The main attractions of biosorption are high selectivity and efciency, cost effectiveness and good removal performance; raw materials which are either abundant (sea weeds) or wastes from other industrial operations (fermentation wastes, activated sludge process wastes) can be used as biosorbents presenting performances often comparable with those of ion exchange resins. Both living and dead (heat killed, dried, acid and/or otherwise chemically treated) biomass can be used to remove hazardous organics,
1000
but maintaining a viable biomass during adsorption is difcult, because it requires a continuous supply of nutrients and avoidance of organic toxicity to the microorganisms. The use of dead microbial cells in biosorption is more advantageous for water treatment in that dead organisms are not affected by toxic wastes, they do not require a continuous supply of nutrients and they can be regenerated and reused for many cycles. Dead cells may be stored or used for extended periods at room temperature without putrefaction occurring. Their operation is easy and their regeneration is simple. Moreover, dead cells have been shown to accumulate pollutants to the same or greater extent than growing or resting cells. The mechanism of binding by inactivated biomass may depend on the chemical nature of pollutant (species, size, ionic charge), type of biomass, its preparation and its specic surface properties and environmental conditions (pH, temperature, ionic strength, existence of competing organic or inorganic ligands in solution). As hydrophobic organic pollutants show a high tendency to accumulate onto microbial cells or sludge, the microbial biomass could be used as an adsorbent of biological origin for the removal of very low concentration hazardous organics from the wastewater [47,1012,1416,3942,64109]. Although biosorption is generally used for the treatment of heavy metal pollutants in wastewaters [6476], it can also be considered a promising technology for the removal of organics from industrial waste streams and polluted natural waters [47,1012,1416,3942,77113]. A great deal of the biosorption studies are performed in batch systems with single species of organics. These processes are conceptually simple. A suitable microbial biomass is contacted with aqueous solution containing organic pollutant molecules or ions. The contacting process is allowed to proceed for a sufcient time for the biomass to sequester these molecules and to reach equilibrium. Then the biomass is separated from the liquid phase and the pollutant-containing biomass is either regenerated or disposed in an environmentally acceptable manner. A major consideration with any biosorption scheme is the separation of liquid and solids after batch or counter current contacting. Centrifugation of ltration, as routinely used in the laboratory, are not generally practical in industrial processes; thus, continuous systems such as continuous stirred tank reactors, uidized bed, moving bed and packed bed columns must be used. For continuous operation, the most convenient conguration is that of a packed column, much like that used for ion exchange. This operating method ensures the highest possible concentration difference driving force. Continuous packed bed sorption has a number of process engineering advantages including high yield operations and relatively easy scaling up from a laboratory scale procedure. The stages in the separation protocol can also be automated and high degrees of purication can often be achieved in a single step process. A large volume of wastewater can be continuously treated using a dened quantity of biosorbent in the column. Reuse of microorgan-
ism is also possible. After pollutant loading the pollutant may be concentrated in a small volume of solid material or desorbed into a small volume of eluant for recovery, disposal or containment. However, the use of dead biomass in powdered form in the column has some problems, such as difculty in the separation of biomass after biosorption, mass loss after regeneration, low strength and density and small particle size, which make it difcult to use in column applications. To solve these problems, dead biomass can be immobilized in a supporting material. Researchers have recognized that immobilizing nonliving biomass in a biopolymeric or polymeric matrix may improve biomass performance, biosorption capacity, increase mechanical strength and facilitate separation of biomass from pollutant containing solution. Immobilization also allows higher biomass concentration, resistance to chemical environments and column operations and immobilized systems may be well suited for non-destructive recovery. Indeed, the use of immobilized biomass has a number of major disadvantages. In addition to increasing the cost of biomass pre-treatment, immobilization adversily affects the mass transfer kinetics of organics uptake. When biomass is immobilized the number of binding sites easily accessible to organic molecules or ions in solution is greatly reduced since the majority of sites will lie within the bead [64,71,108].
2. Modeling of biosorption in batch and continuous systems 2.1. Equilibrium modeling of biosorption in a batch system Equilibrium data, commonly known as adsorption isotherms, are basic requirements for the design of biosorption systems used for the removal of organic pollutants. The Langmuir, Freundlich, LangmuirFreundlich, Redlich Peterson, BrunauerEmmetTeller (BET), RadkePrausnitz are the most frequently used two- and thee-parameters models in the literature describing the non-linear equilibrium between adsorbed organic pollutant on the cells (qeq ) and organic pollutant in solution (Ceq ) at a constant temperature. The Langmuir equation which is valid for monolayer sorption onto a surface with a nite number of identical sites is given by Eq. (1). qeq = Q0 bCeq 1 + bCeq (1)
where parameters Q0 and b are Langmuir constants related to maximum adsorption capacity (monolayer capacity) and bonding energy of adsorption, respectively, which are functions of the characteristics of the system as well as time [114]. Q0 and b can be determined from the linear plot of Ceq /qeq versus Ceq . The Langmuir equation is used for homogeneous surfaces. The Freundlich isotherm model assumes neither ho-
1001
mogeneous site energies nor limited levels of sorption. The Freundlich equation has the general form: qeq = KF Ceq
1/n
(2)
where KF and n are the Freundlich constants related to adsorption capacity and adsorption intensity, respectively [115]. Eq. (2) can be linearized in logarithmic form and Freundlich constants can be determined. The LangmuirFreundlich model is essentially a Freundlich isotherm which approaches an adsorption maximum at high concentrations of adsorbate. An equation mathematically equivalent to the LangmuirFreundlich equation can also be obtained by assuming that the surface is homogeneous, but that the adsorption is a cooperative process due to adsorbateadsorbate interactions. The following relation represent this model: qeq = Q0 bCeq
1/n 1/n
When several components are present, interference and competition phenomena for adsorption sites occur and lead to a more complex mathematical formulation of the equilibrium. Several isotherms have been proposed to describe equilibrium and competitive adsorption for such a system. These isotherms range from simple models related to the individual isotherm parameters only (such as competitive RedlichPeterson isotherm model), to more complex models related to the individual isotherm parameters and to correction factors (such as modied competitive Langmuir and modied Freundlich isotherm models). The modied competitive Langmuir isotherm is written as: qeqi = Q0 bi (Ceqi /i ) i 1+
N j=1 bj (Ceqj /j )
(8)
1 + bCeq
(3)
For positive interactions (1/n > 1), the LangmuirFreundlich converts to Hill equation [39]. A further empirical model has been developed by RedlichPeterson to improve the t by the Langmuir or Freundlich equation [116] and is given by Eq. (4). qeq = KRP Ceq 1 + aRP Ceq
where Ceqi and qeqi are the unadsorbed concentration of each component at equilibrium and the adsorbed quantity of each component per g of dried biomass at equilibrium, respectively. bi and Q0 are derived from the corresponding i individual Langmuir isotherm equations.i is the Langmuir correction coefcient of the i component where estimated from competitive adsorption data [119]. The empirical extended form of the Freundlich model restricted to binary mixtures can be given by Eqs. (9) and (10) for each component of binary system: qeq1 = KF1 Ceq1 1
1 Ceq1
(4)
1/n +x1 z1 Ceq2
where KRP , aRP , and are the RedlichPeterson parameters. The exponent lies between 0 and 1. For = 1 Eq. (4) converts to the Langmuir form. The RadkePrausnitz isotherm model [117] is given as: qeq = arCeq a + rCeq
p1 p
x +y1
(9)
qeq2 =
KF2 Ceq2 2
2 Ceq2
1/n +x2 z2 Ceq1
x +y2
(10)
(5)
where a, r, and p are related model constants. The theoretical BET model for multilayer sorption [118] is: qeq = BQ0 Ceq (Cs Ceq )[1 + (B 1)(Ceq /Cs )] (6)
where KF1 , KF2 and n1 and n2 are derived from the corresponding individual Freundlich isotherm equations and the six other parameters are the competition coefcients for two species [119]. The competitive RedlichPeterson model related to the individual isotherm parameters only is given as follows: qeqi = 1+ KRPi Ceqi N j j=1 aRPj (Ceqj ) (11)
where Cs is the saturation concentration of the adsorbed component; B a constant indicating the energy of interaction between the solute and the adsorbent surface, and Q0 is a constant indicating the amount of solute adsorbed forming a complete monolayer. In some cases the relationship between equilibrium concentrations of organics in liquid and solid phases could be linear and dened by simple distribution coefcients. In this case the adsorption data are tted to linear adsorption isotherm as described in Eq. (7) [43,96,97]. qeq = Kd Ceq where Kd is distribution coefcient. (7)
where KRPi , aRPi , and j are the RedlichPeterson parameters derived from the corresponding individual RedlichPeterson isotherm equations [119]. 2.2. Kinetic modeling of biosorption in a batch system If the movement of organic pollutant molecule from the bulk liquid to the liquid lm or boundary layer surrounding the biosorbent is ignored, the following sequence of steps can take place in the biosorption process of porous biosorbent: transport of solute molecules from the boundary lm to the external surface of the biosorbent (lm diffusion), transfer of molecules from the surface to the intraparticular active
1002
sites and uptake of molecules by the active sites of sorbent. In the removal of organics from wastewater, it is important for design purposes to investigate the mechanisms of adsorption and potential rate controlling steps which control the adsorption rate. In order to nd the contribution of rate controlling steps such as external mass transfer, intraparticle diffusion, and adsorption process and also, mass transfer and kinetic models have been used to test the experimental data. In the rst step of adsorption, the lm diffusion is an important rate-controlling step and external mass transfer or boundary layer diffusion can be characterized by the initial rate of solute sorption. In this case, adsorption rate is expected to be proportional to the rst power of concentration; it means that this step is a rst-order process and can be dened as: dC (12) = k1,ad C dt where C is the pollutant concentration in the wastewater remaining at each contact time and k is the rst-order reaction-rate constant. After integration and applying boundary conditions, t = 0 to t = t and C = C0 to C = C; the integrated form of Eq. (12) becomes C0 1 log = k1,ad t C 2.303 (13)
boundary conditions, t = 0 to t = t and q = 0 to q = q; the integrated form of Eq. (15) becomes log(qeq q) = log qeq k1,ad t 2.303 (16)
A straight line of log(qeq q) versus t suggests the applicability of this kinetic model. In order to t Eq. (16) to experimental data, the equilibrium sorption capacity, qeq , must be known. In many cases qeq is unknown and as adsorption tends to become unmeasurably slow, the amount sorbed is still signicantly smaller than the equilibrium amount. For this reason it is necessary to obtain the real equilibrium sorption capacity, qeq , by extrapolating the experimental data to t = or by using a trial and error method. Furthermore, in most cases the rst-order equation of Lagergren does not t well for the whole range of contact time and is generally applicable over the initial 2030 min of the sorption process. The pseudo second-order equation is also based on the sorption capacity of the solid phase. Contrary to the other model it predicts the behaviour over the whole range of adsorption. The pseudo second-order kinetic rate equation is expressed as dq = k2,ad (qeq q)2 dt (17)
where C0 is the initial pollutant concentration [15]. If intraparticular diffusion is involved in the sorption process, the model developed by Weber and Morris [120] can be used to nd the region where intraparticle diffusion is rate-limited and to determine intraparticular diffusion rate. In this model, the rate of intraparticular diffusion is a function of t0.5 and can be dened as follows: q=f Dt 2 rp
0.5
where k2,ad is the rate constant of second-order biosorption. For the boundary conditions t = 0 t = t and q = 0 q = q; the integrated and linear form of Eq. (17) becomes t 1 1 + t = 2 q qeq k2,ad qeq (18)
= K t 0.5
(14)
If second-order kinetics are applicable, the plot of t/q against t of Eq. (18) should give a linear relationship, from which qeq and k2,ad can be determined from the slope and intercept of the plot and there is no need to know any parameter beforehand. 2.3. Kinetic modeling of biosorption in a continuous packed bed system When an organic pollutant containing solution passes through a packed bed column, at the beginning, most of organic pollutant get sorbed on biosorbent so organic pollutant concentration in the efuent remains either very low or in some cases is not detectable. As biosorption continues, organic pollutant concentration in the efuent rises, slowly at rst, and then abruptly. When this abrupt rise or breakthrough occurs, the ow is stopped. The performance of continuous packed bed is described through the concept of the breakthrough curve. The time for breakthrough appearance (breakthrough time) and the shape of the breakthrough curve are very important characteristics for determining the operation and the dynamic response of a biosorption column. The general position of the breakthrough curve along the time or volume axis depends on the capacity of the column with respect to the feed concentration and ow
where rp is particle radius, D is the effective diffusivity of solute within the particle, and K intraparticular diffusion rate. If intraparticle diffusion is rate-limited; then a plot of adsorbate uptake (q) versus the square root of time (t0.5 ) would result in a linear relationship and K value can be obtained from this plot. Moreover, the particle diffusion would be the rate-controlling step if the line passes through the origin. In many cases, the kinetics of biosorption based on overall adsorption rate by biosorbents are described by the rst-order Lagergren [121] and pseudo second-order [122] kinetic models. The rst-order rate expression of Lagergren based on the sorption capacity of adsorbent is generally expressed as follows: dq = k1,ad (qeq q) (15) dt where q is the amount of adsorbed pollutant on the biosorbent at time t, and k1,ad is the rate constant of Lagergren rst-order biosorption. After integration and applying
1003
rate. The breakthrough curves show the loading behaviour of pollutant to be removed from solution in a xed bed and is usually expressed in terms of normalized concentration dened as the ratio of efuent pollutant concentration to inlet pollutant concentration (C/C0 ) as a function of time or volume of efuent (Veff ) for a given bed height. Successful design of a column adsorption process requires prediction of the concentration-time prole or breakthrough curve for the efuent under given specic operating conditions. Developing a model to accurately describe the dynamic behaviour of adsorption in a xed bed system is inherently difcult. Since the concentration of the adsorbate as the feed moves through the bed, the process does not operate at steady state. The fundamental transport equations derived to model the xed bed with theoretical rigor are differential in nature and usually require complex numerical methods to solve. Such a numerical solution is not usually difcult, but often does not t experimental results especially well. Some solutions for very limiting cases have been reported, but in general, complete time-dependent analytical solutions to differential equation based models of the proposed rate mechanisms are not available. Because of this, various simple mathematical models have been developed to predict the dynamic behaviour of the column and the following models used in the literature to characterize the xed bed performance for the removal of organics are presented here [41,64,71,108,123]. The AdamsBohart model is used for the description of the initial part of the breakthrough curve and the linear form of model is given by Eq. (19): ln C Z = kAB C0 t kAB N0 C0 U0 (19)
Clark [126] dened a new simulation of breakthrough curves. This model combines the Freundlich equation and the mass transfer concept and has the following form: C = C0 with A= and R(n 1) = r and R = kCl U0 (24)
n1 Cbreak n1 C0
1 1 + A ert
1/n1
(22)
1 ertbreak
(23)
Eq. (24) is the generalized logistic function where n; Cbreak , tbreak , kCl , and are the Freundlich constant, the outlet concentration at breakthrough (or limit efuent concentration), the time at breakthrough, the Clark rate constant and migration rate, respectively. For a particular adsorption process on a xed bed and a chosen treatment objective, values of A and r can be determined by using Eq. (24) by non-linear regression analysis, enabling the prediction of the breakthrough curve according to the relationship between C/C0 and t in Eq. (24) [126]. Yoon and Nelson [127] have developed a relatively simple model which not only is less complicated than other models, but also requires no detailed data concerning the characteristics of adsorbate, the type of adsorbent, and the physical properties of adsorption bed. The Yoon and Nelson equation regarding to a single-component system is expressed as: ln C = kYN t kYN C0 C (25)
where kAB is the AdamsBohart kinetic constant, N0 is the saturation concentration and Z is the column height. From this equation, values describing the characteristic operational parameters of the column can be determined from a plot of ln C/C0 against t at a given bed height and ow rate [124]. Besides the prediction of the concentrationtime prole or breakthrough curve for the efuent, the maximum adsorption capacity of an adsorbent is also needed in design. Traditionally, the Thomas model is used to full the purpose. The model has the following form: C 1 = C0 1 + exp(kTh /Q(q0 X C0 Veff )) (20)
where kYN is the Yoon and Nelson rate constant, t is the time required for 50% adsorbate breakthrough and is the breakthrough (sampling) time. The calculation of theoretical breakthrough curves for a single-component system requires the determination of the parameters kYN and for the adsorbate of interest. These values may be determined from available experimental data. The approach involves a plot of ln C/(C0 C) versus sampling time (t) according to Eq. (25). If the theoretical model accurately characterizes the experimental data, this plot will result in a straight line with slope of kYN and intercept kYN [127].
where kTh is the Thomas rate constant, q0 is the maximum solid-phase concentration of the solute, Q is the ow rate and X is the amount of sorbent in the column. The linearized form of the Thomas model is as follows: C0 kTh q0 X kTh C0 ln (21) 1 = Veff C Q Q The kinetic coefcient kTh and the adsorption capacity of the bed q0 can be determined from a plot of ln[(C0 /C] 1] against t at a given ow rate [125].
3. Biosorption of dyes A wide variety of microorganisms including bacteria, fungi and yeasts are used for the biosorption of a broad range of dyes. Textile dyes vary greatly in their chemistries, and therefore their interactions with microorganisms depend on the chemical structure of a particular dye, the specic chemistry of the microbial biomass and characteristics of the dye solution or wastewater. Depending on the dye
1004
Table 1 Data on the biosorption of dyes by various microorganisms Biosorbent Dye Operation conditions pH Activated sludge Basic Basic Basic Basic Basic Basic Basic Red 29 Yellow 24 Blue 54 Red 18 Violet 3 Blue 4 Blue 3 7 5 3 3 3 3 6 4 6 4 2 2 2 2 2 2 3 3 3 3 T ( C) C0 (mg l1 ) teq 6h 6h 6h 6h 6h 6h 6h 1h 1h 2h 1h 1h 1h 1h 48 h 30 h 42 h 48 h 2 weeks 24 h 24 h 24 h 24 h 24 h 4h 1h 1h 1h 1h 20 h 20 h 20 h 12 h 12 h 12 h 12 h 12 h Biosorption capacity qeq (mg g1 ) [15] Ref.
20 20 20 20 20 20 20 25 25 20 28 28 28 28 25 25 25 25 25 25 28 28 28 28 RT RT RT RT RT RT RT RT
500 500 500 500 500 500 500 200 200 200 200 200 200 200 50 50 50 50 250 400 400 300 300 400 300 200 200 200 200 100 100 100 100a 100a 100a 100a 100a
113.2 105.6 86.6 133.9 113.6 157.5 36.5 102.0 119.4 (123.2) 124.8 116.5 114.5 124.3 18.5 (1.2) 13.8 (6.6) 14.7 5.6 14.2 42 (13.0) 360 (49.7) 169 230 149 152 180 113 8 (8) 31 (31) 407 (308) 23 (22) 76 (60) 407 (360) 19 (36) 36 (38) 589 (527) 44 307 89.4 76.6 65.5 52.4 503.1 545.2 643.9 17 (60) 45 (7) 37 (60) 37 98 68 33 8.5
Activated sludge Activated sludge Aeromonas sp.
Reactive Blue 2 Reactive Yellow 2 Maxilon Red BL-N Reactive Reactive Reactive Reactive Blue 5 Red 22 Violet 2 Yellow 2
[91] [94] [83]
Aspergillus niger
Basic Blue 9 Acid Blue 29 Congo Red Disperse Red 1 Reactive Brilliant Red Reactive Blue 19 Sulfur Black 1 Remazol Remazol Remazol Remazol Remazol Remazol Blue Blue Blue Blue Blue Blue
[88] [89] [16] [16] [85] [84] [93]
Aspergillus niger Botrytis cinerea Candida Candida Candida Candida Candida Candida sp. lipolytica membranaefaciens quilliermendii tropicalis utilis
Candida rugosa
Reactive Blue 19 Reactive Black 5 Sulfur Black 1 Reactive Blue 19 Reactive Black 5 Sulfur Black 1 Reactive Blue 19 Reactive Black 5 Sulfur Black 1 Reactive Black 5 Sulfur Black 1 Reactive Reactive Reactive Reactive Blue 5 Red 22 Violet 2 Yellow 2
[84]
Cryptococcuss heveanensis
[84]
Dekkera bruxellensis
[84]
Endothiella aggregata Escherichia coli
[84] [83]
Fomitopsis carnea
Orlamar Red BG Orlamar Blue G Orlamar Red GTL Reactive Blue 19 Reactive Black 5 Sulfur Black 1 Remazol Black B Rem. Turquoise Blue Remazol Red Rem. Golden Yellow Cibacron Orange
[14]
Geotrichum ci
[84]
Kluyveromyces marxianus
[87]
Z. Aksu / Process Biochemistry 40 (2005) 9971026 Table 1 (Continued) Biosorbent Dye Operation conditions pH Kluyveromyces marxianus Kluyveromyces waltii Remazol Blue Reactive Blue 19 Reactive Black 5 Sulfur Black 1 Reactive Brilliant Red Orange II 10B (Blue) RS (Red) Congo red Reactive Blue 19 Reactive Black 5 Sulfur Black 1 Reactive Reactive Reactive Reactive Blue 5 Red 22 Violet 2 Yellow 2 2 3 3 3 3 2 2 2 2 2 2 T ( C) 25 28 28 28 28 RT RT RT 35 25 25 C0 (mg l1 ) 300 250 200 200 200 500 200 200 200 200 500 400 250 350 800 250 250 300 300 280 180 150 80 200 teq 4h 4 weeks 5h 5h 5h 2 days 1h 1h 1h 1h 20 h 20 h 20 h 1h 4 weeks 4 weeks 4h 4h 14 days 14 days 14 days 14 days 14 days Biosorption capacity qeq (mg g1 ) 161 14 (20) 72 (60) 549 (445) 20.5 70% 86% 95% 90% 5 (3) 32 (25) 549 (499) 102.5 105.3 96.4 102.6 91.9 190 90 150 500.7 102.6 37.2 452 (99) 3008 (1107) 162 69 (52) 152 27.0% 73.0% 29.0% 70.0% 39.0% 35 (41) 79 (92) 892 (934) 60 (0) 1 (11) 60 (63)
1005
Ref.
[93] [84]
Laminaria digitata Myrothecum verrucaria
[85] [80]
Phanerochaete chrysosporium Pichia carsonii
[86] [84]
Pseudomonas luteola
[83]
Rhizopus arrhizus Rhizopus arrhizus
Humic acid Reactive Orange 16 Reactive Blue 19 Reactive Red 4 Remazol Black B Reactive Brilliant Red Reactive Brilliant Red Reactive Black 5 Sulfur Black 1 Remazol Blue Reactive Blue 19 Remazol Blue Anthraquinone Blue 114 Azo-copper Red 171 147 209 116 Reactive Blue 19 Reactive Black 5 Sulfur Black 1 Reactive Blue 19 Reactive Black 5 Sulfur Black 1
[82] [12]
Rhizopus arrhizus Rhizopus oryzae (26668) Rhizopus oryzae (57412) Rhizopus oryzae Saccharomyces cerevisiae Saccharomyces cerevisiae Saccharomyces pombe Streptomycetes BW130
[11] [85] [84] [93] [84] [93] [81]
Azo-reactive Red Formazan Blue Phytalocyanine Blue Tremella fuciformis
[84]
Xeromyces bisporus
[84]
Values in parentheses represent biosorption capacity of live biomass; %: percent removal. a Equilibrium concentration.
and the species of microorganism used different binding capacities have been observed (Table 1). 3.1. Microorganisms and dyes used in biosorption: biosorption mechanisms Zhou and Banks [77] rstly reported the adsorption of humic acid caused organic colour in raw water by dead Rhizopus arrhizus and they concluded that adsorption was
a biphasic process; the rst was fast and independent of metabolic energy while the second was slow and dependent on metabolic energy. Based on the examinations by infrared spectra, they concluded that no chemical reaction occurred between cell wall and humic acid; just a physical adsorption [77]. Hu [7] demonstrated the ability of bacterial cells isolated from activated sludge process of a textile industry and soil to adsorb 11 reactive dyes including Reactive Blue, Reactive
1006
Red, Reactive Violet, Reactive Yellow and Procion Red G. The author suggested that the cell wall portion of Aeromonas sp. had a higher specic adsorption capacity than the intact cells due to the larger surface area in the cell walls. At 100 mg l1 dye concentration the colour removal efciencies ranged from 12.9 to 94.3% and the maximum specic adsorption capacity of Aeromonas sp. was 27.4 mg dye g1 dried cells for Procion Red G at pH 3.0 [7]. Brahimi-Horn et al. [80] studied with the intact and disrupted (sonicated) Myrothecum verrucaria cells for the removal of three acid dyes in order to investigate the possible role of intracellular compartmentation of dye in decolourization. They found that both external and internal uptake were important for the binding capacity. On the other hand they observed that the divalent dye (Acid Red) was bound to a greater extent than the monovalent dye (Acid Orange II) [80]. Zhou and Zimmerman [81] used the actinomycete Streptomycetes BW130 as an adsorbent for the decolourization of efuents containing anthroquinone, phtlocyanine, and azo dyes [81]. In another study of Zhou and Banks [82], they reported that chitin/chitosan was the major active component of R. arrhizus for humic acid adsorption [82]. In another study of Hu [83], three Gram-negative bacteria (Aeromonas sp., Pseudomonas luteola and Escherichia coli), two Gram-positive bacteria (Bacillus subtilis and S. aureus) and activated sludge (consisting of both Gram-negative and Gram-positive bacteria) were used as biosorbents for the removal of reactive dyes of Reactive Blue, Reactive Red, Reactive Violet and Reactive Yellow. Dead cells of test genera showed a higher uptake than the living cells due to increased surface area and Gram-negative bacteria had a higher adsorption capacity than Gram-positive bacteria due to higher lipid contents in the cell wall portion. Among these microorganisms, the specic adsorption capacity of Aeromonas sp. for these dyes was the maximum in the range of 114146 mg g1 at 200 mg l1 initial dye concentration [83]. Polman and Breckenridge [84] tested 30 species of lamentous fungi, yeast and bacteria to remove reactive (Reactive Black 5, Reactive Blue 19) and sulfur (Sulfur Black 1) dyes from simulated plant waste efuents. They used both dead and live forms of each of the species and observed that among 28 microbial species, 64% of the dead forms had a higher adsorption capacity for the Reactive Black 5 dye waste; among the 21 species capable of binding Reactive Blue 19 dye waste, 71% were more efcient dye binders in the dead form than in the live form. They suggested that this might be due to an increase in the surface area for adsorption because of cell rupture upon death. But among the 26 species capable of binding Sulfur Black 1 dye waste, 54% were more efcient in the live state. They proposed that this might be due to the chemistry of different dyes [84]. Mittal and Gupta [14] examined dead macrofungus, Fomitopsis carnea for the sorption of three cationic dyes, Orla-
mar Red BG (ORBG), Orlamar Blue G (OBG), and Orlamar Red GTL (ORGTL) [14]. Gallagher et al. [85] investigated three types of fungi, including Laminaria digitata, Rhizopus oryzae, and Aspergillus niger, to remove Reactive Brilliant Red, a reactive dye suggesting that adsorption was occurred by combined mechanisms onto a heterogeneous surface [85]. Tatarko and Bumpus [86] studied the biosorption of Congo Red, a cationic azo dye on autoclaved P. chrysosporium, a wood rotting basidiomycete in a agitated batch system and observed a higher colour removal (90%) [86]. Bustard et al. [87] used the biomass derived from the thermotolerant ethanol-producing yeast strain Kluyveromyces marxianus IMB3 for the removal of commonly used textile dyes including Remazol Black B, Remazol Turquoise Blue, Remazol Red, Remazol Golden Yellow and Cibacron Orange. They proposed that Cu atom in the Remazol Turquoise Blue plays a role in the interaction between that dye and the biosorbent regarding the maximum uptake of this dye by the yeast [87]. Aksu and Tezer [11] studied with dried R. arrhizus for the removal of Remazol Black B, a reactive anionic dye from aqueous solution. They proposed that the biosorption is a result of interaction between the active groups on the cell surface of the fungus such as chitin, acidic polysaccharides, lipids, amino acids, and other cellular components of the microorganism and dye anions which are typically azo-based chromophores combined with vinyl sulfone reactive groups [11]. Fu and Virarahavan [5,16,8890] investigated the removal of Basic Blue 9 (cationic), Acid Blue 29 (anionic), Congo Red (anionic), and Disperse Red 1 (nonionic) dyes from aqueous solutions by biosorption on dead and pretreated Aspergillus niger fungus. They found that A. niger is capable of removing dyes from an aqueous solution. They explored that three major functional groups: carboxyl, amino and phosphate, and the lipid fraction in the biomass of A. niger played an important role in the biosorption of these dyes [5,16,8890]. Aksu [91] investigated the biosorption of two reactive dyes (Reactive Blue 2 and Reactive Yellow 2) onto dried activated sludge consisting of mainly both bacteria and protozoa. They suggested that activated sludge has an extensive uptake capacity for organic pollutants due to acidic polysaccharides, lipids, amino acids and other cellular components available on the cell wall of bacteria [91]. OMahony et al. [12] indicated that the ability of oven-dried R. arrhizus biomass for the biosorption of three commonly used reactive dyes, Cibacron Brilliant Red 3B-A (Reactive Red), Remazol Brilliant Blue R (Reactive Blue 19), Remazol Brilliant Orange3WR (Reactive Orange 16) from aqueous solutions in a batch system [12]. Chu and Chen [15,92] studied with the oven-dried activated sludge biomass in the particle size range of 105297 m as an biosorbent for the removal of selected
1007
anionic dyes such as Direct Orange 39 and Direct Red 83, or for selected non-ionic dyes, such as Disperse Violet 8 and Disperse Yellow 54 or for cationic (basic) dyes such as Basic Blue 3 (B-3), Basic Violet 3 (V-3), Basic Yellow 24 (Y-24), Basic Red 18 (R-18), Basic Red 29 (R-29), Basic Blue 47 (B-47), Basic Blue 54 (B-54) from wastewater. They observed that the biomass had no afnity for anionic and non-ionic dyes. However, the biomass could integrate with the cationic dyes. Maximum adsorption capacity of these basic dyes occurred in the order B-47 > R-18 > V-3 > R-29 > Y-24 > B-54 B-3, They concluded that the chemical structure (e.g. molecular structure of colouring groups, such as anthraquinone, monoazo, oxazine, thiazole azo, or triarylmethane and the type and number of the position of the substituents in the dye molecule), basicity (e.g. element of chromophore group, insulated or conjugated type), and molecular weight of basic dye molecules have an inuence on the adsorption capacity of activated sludge biomass [15,92]. Aksu and Dnmez [93] reported the biosorption capacities and rates of nine yeast species (Saccharomyces cerevisiae, Schizosaccharomyces pombe, K. marxianus, Candida sp., Candida tropicalis, Candida lipolytica, Candida utilis, Candida quilliermendii, and Candida membranaefaciens) for Remazol Blue reactive dye from aqueous solutions. The yeasts studied were found to be more effective for concentrating Remazol Blue dye at different capacities according to the dye concentration. They explained the differences between yeast species for dye binding capacity in terms of the properties of the yeast (e.g., structure, functional groups, surface area and morphological differences depending on the yeast division, genera and species). They proposed that cell walls of yeasts contain polysaccharides as basic building blocks which have ion exchange properties, and also proteins and lipids and therefore offer a host of functional groups capable of binding dye molecules. These functional groups such as amino, carboxylic, sulfydryl, phosphate and thiol groups, differ in their afnity and specicity for dye binding [93]. Basibuyuk and Forster [94] studied the biosorption of one acid dye (Acid Yellow 17) and one basic dye (Maxilon Red BL-N) onto live activated sludge. They chose live activated sludge in order to understand the adsorption properties of dye-activated sludge systems since sorption is the primary mechanism leading to biodegradation in activated sludge processes commonly used for the treatment of textile wastewaters. The results showed that binding of Acid Yellow 17 where the colouring group is anionic onto activated sludge was not promising while Maxilon Red BL-N where the colouring group is cationic was adsorbed well by activated sludge. They explained the main reasons for the poor adsorption capacity of acid dye as the negative electrical charge of activated sludge under normal pH conditions so repulsion between negatively charged sorbate ions and negatively charged sorbent surface, and the number of sulpho groups in acid dye reducing dye adsorption [94].
3.2. Pretreatment of microorganism Researches have shown that some physical or chemical pretreatment processes can increase the adsorption capacity of biomass. These pretreatment methods mainly included drying, autoclaving, contacting with organic chemicals, such as formaldehyde, or inorganic chemicals, such as NaOH, H2 SO4 , NaHCO3 , and CaCl2 . Zhou and Banks [77] reported that R. arrhizus pretreated with 10% formaldehyde or autoclaving signicantly increased the humic acid adsorption capacity compared with living cells, due to the exposure of latent binding sites [77]. In another study of Zhou and Banks [82], they used R. arrhizus biomass pretreated with 2 M NaOH for 1 h and they found an increased biosorptive capacity. They also observed that the longer duration of treatment caused further enhancement of the biosorption capacity. They suggested that NaOH treatment could remove proteins and glucans from the cell wall thereby increasing the percentage of chitin/chitosan in the whole cell fraction. Some chitin may also be transformed to chitosan with concentrated alkaline solution over a long period. They suggested chitosan could be the most efcient sequester of humic acid molecules [82]. Hu [83] used live and autoclaved Gram-negative bacteria for the removal of reactive dyes and indicated that the autoclaved cells had a higher uptake capacity than living cells due to increasing in surface area caused by cell rupture during autoclaving [83]. Gallagher et al. [85] observed that all methods; including autoclaving, calcium saturation, NaOH and chitin/chitosan enrichment, they used for the pretreatment of R. oryzae increased the biosorption capacity from 7 to 15%. After measuring the porosity and surface area of the biomass of R. oryza, they explained the increase in biosorption capacity by autoclaving process due to the disruption of the particle structure. The disruption may cause an increase of surface area and monolayer volume and an increase in porosity of the particles and thus expose latent sites, consequently increasing the dye adsorption. An increase of adsorption capacity by Ca2+ saturation was demonstrated as a fact that R. oryzae had a low afnity for Ca2+ ions, which made calcium a good activating counter ion which was easy to be replaced by dyes that formed more stable complexes. According to authors, pretreatment by NaOH could generate anionic sites without signicant modication of the cell wall structure and also expose the chitin/chitosan complex of the cell by dissolving certain biopolymers from the surface of biomass particles, since chitin/chitosan was suggested as the predominant biosorbent of the dye [85]. Tatarko and Bumpus [86] used both living and autoclaved cultures of P. chrysosporium to decolourize Congo Red and observed that the autoclaved cells had a higher colour removal (90%) than the living cells (70%) [85]. Fu and Viraraghavan [88,89] used some pretreatment methods such as autoclaving and contacting with normal chemicals, including 0.1 M NaOH, 0.1 M HCl, 0.1 M
1008
H2 SO4 , 0.1 M CaCl2 , 0.1 M NaHCO3 , 0.1 M Na2 CO3 and 0.1 M NaCl to pretreat the living fungal biomass A. niger. They reported that the effective pretreatment was different with each of the dyes, Basic Blue 9 and Acid Blue 29. Autoclaving increased the biosorption capacity from 1.2 mg of Basic Blue 9 per gram of living fungal biomass to 18.5 mg g1 of autoclaved biomass, while 0.1 M H2 SO4 pretreatment enhanced the biosorption capacity from 6.6 mg of Acid Blue 29 per gram of living biomass to 13.8 mg g1 of dead biomass. They suggested that autoclaving could disrupt the fungal structure and expose the potential binding sites for Basic Blue 9, a cationic dye, biosorption, while H2 SO4 pretreatment could change the negatively charged surface of the fungal biomass to positively charged and thus increase the attraction between fungal biomass and Acid Blue 29, an anionic dye [88,89]. Fu and Viraraghavan [90] also studied the removal of Congo Red, an anionic dye by pretreated fungus A. niger. They classied the chemicals used for pretreatment as acids, alkalis and salts. They used autoclaved (for 30 min at 121 C and 18 p.s.i.), 0.1 M NaOH, 0.1 M HCl, 0.1 M H2 SO4 , 0.1 M CaCl2 , 0.1 M NaHCO3 , 0.1 M Na2 CO3 , and 0.1 M NaCl treated A. niger biomass. They observed that while HCl, H2 SO4 , CaCl2 , NaHCO3 , and NaCl pretreatments all increased biosorption capacity, NaOH and Na2 CO3 pretreatments decreased biosorption capacity. They proposed that fungal biomass is usually charged negatively on its surface. Congo Red ionizes to give a coloured anion in solution. Therefore the coloured anions of Congo Red will be repulsed by the anionic groups on the surface of fungal biomass. As autoclaving could cause the disruption o the fungal structure resulting in an increase in porosity [85], more Congo Red ions could enter the expanded pores in autoclaved fungal biomass leading to increased biosorption capacity. They explained the reason why CaCl2 pretreatment increased biosorption capacity could be that Ca2+ is divalent and thus could neutralize the negative charge on the surface of fungal biomass and change part of the negatively charged surface to positively charged. NaOH pretreatment decreased biosorption capacity of Congo Red. This is because pretreatment by NaOH could generate anionic sites on the surface of fungal biomass [85] and thus increase repulsion between the negatively charged surface of the fungal biomass and the coloured anions of Congo Red. Pretreatment with NaHCO3 was found to be the most effective with a biosorption capacity of 14.7 mg g1 compared with 12.1 mg g1 of living biomass for Congo Red. This could be because bicarbonate ion, HCO3 can either provide protons or accept protons in water. The protons could neutralize negative charges on the surface of fungal biomass and change the part of the negatively charged surface to positively charged. Meanwhile, they explored that changes in charge density could also affect adsorption afnity for particular dyes. For Acid Blue 29 they found the extent of increase in biosorption capacity by NaHCO3 pretreatment was lower than that by HCl and
H2 SO4 pretreatment. They attributed the difference to the different molecular structures of the two dyes. Therefore, they suggested that the effective pretreatment is related to dye molecules, which is specic for each dye [90]. 3.3. Effect of pH on dye biosorption Since pH is the most important parameter affecting not only the biosorption capacity, but also the colour of the dye solution and the solubility of some dyes, various researchers have investigated the effect of pH on colour removal. Hu [7] demonstrated that the optimal pH for biosorption of 11 reactive dyes by Aeromonas sp. cells was at acidic range. He found that the removal decreased as the pH of the dye solution increased from 3.0 to 11.0. He suggested that at a lower pH, the association of dye anions with positively charged bacterial cell surfaces at acidic pH takes place [7]. Zhou and Banks [82] reported that the biosorption of humic acid by R. arrhizus increased with decreasing pH. They suggested that at lower pH, more of humic acid functional groups were uncharged and humic acid had a lower solubility and was thus more adsorbable. On the other hand, the lower pH results in high concentrations of protons which neutralize the negative charge on both R. arrhizus and humic acid, leading to increased adsorption [82]. On the other hand Mittal and Gupta [14] studied the effect of pH on the biosorption of three cationic dyes, Orlamar Red BG, Orlamar Blue G and Orlamar Red GTL by dead fungus of F. carnea and their results showed that colour removal decreased with decreasing pH due to repulsive forces between coloured dye cations in solution and biosorbent surface charged positively at pH values lower than 3.0 [14]. Hu [83] investigated the effect of pH on the removal of six reactive dyes by three Gram-negative bacteria (P. luteola, E. coli, and Aeromonas sp.) and reported that the biosorption of all dyes by all cells increased signicantly with decreasing pH. They explained this situation as a fact that dye anions are electrostatically bonded to positively charged bacterial cell surfaces at low pH [83]. Fu and Viraraghavan [88,89] reported that initial pH of dye solution signicantly inuenced the chemistry of both Acid Blue 29 and Basic Blue 9 molecules and dead A. niger fungus in an aqueous solution. The effective initial pH of dye solution was 6.0 and 4.0, respectively, for Basic Blue 9 and Acid Blue 29. At pH of 2.0, no biosorption occurred for Basic Blue 9 due to the high concentration of protons, while at pH of 12, no biosorption occurred for Acid Blue 29 [88,89]. The same authors [16] also investigated the effect of pH on Congo Red biosorption by NaHCO3 pretreated A. niger biomass in an aqueous solution and they determined the effective pH as 6.0. They explained the biosorption mechanism due to pH as follows: the surface of NaHCO3 pretreated fungal biomass could be partially positively charged, so it might have some negatively charged adsorption sites. So the presence of high concentrations of protons at a lower pH could neutralize the negative charge on the surface of
1009
NaHCO3 pretreated biomass, leading to increased biosorption capacity. Therefore, a pH of 6.0 was the effective pH for biosorption of Congo Red. At a high pH, a high concentration of OH could neutralize the positively charged surface of NaHCO3 pretreated biomass and might form a negatively charged surface again. Thus, it would increase the repulsion between the coloured anions of Congo Red and the negatively charged fungal biomass and cause a decrease in biosorption capacity. Meanwhile, there would be competition between OH (at high pH) and the coloured anions of Congo Red for the positively charged adsorption sites, which could also decrease biosorption capacity [16]. Aksu and Tezer [11] also examined the effect of initial pH on fungal (dried R. arrhizus) binding of reactive dye Remazol Black B and they found maximum uptake at pH 2.0. They explained the higher uptakes at lower pH values by electrostatic attractions between negatively charged dye anions and positively charged cell surface [11]. The results obtained by OMahony et al. [12] also showed that the maximum biosorption of three commonly used reactive dyes, Reactive Red, Reactive Blue 19, and Reactive Orange 16 from aqueous solutions by oven-dried R. arrhizus biomass was performed at pH 2.0. They explained the variation in uptake capacity of the Rhizopus biomass across the pH range in terms of its effective isoelectric point. At pH values below the isoelectric point (<4.0), the biomass will have a net positive charge. It is expected that nitrogen-containing functional groups such as amines or imadazoles in the biomass will also be protonated at acidic pH values. These charged sites become available for electrostatic binding of anionic reactive dyes [12]. In a study performed by Aksu and Dnmez [93], optimum biosorption pH was also determined as 2.0 for the removal of Remazol Blue reactive dye by nine yeast species. C. lipolytica showed the maximum biosorption capacity at pH 2.0 binding 173.1 mg dye g1 dry biomass. They explained the enhancement of uptake of reactive dyes at acidic pH in terms of electrostatic interactions between the biomass and the dye particles. Upon dissolution, ionic dyes release coloured dye ions into solution. The adsorption of these charged dye groups onto the adsorbent surface is primarily inuenced by the surface charge that in turn is inuenced by the solution pH. With diminishing pH increasing numbers of weak base groups in the biomass become protonated and acquire a net positive charge. These charged sites become available for binding anionic groups such as the reactive dye used in this study [93]. 3.4. Effect of temperature on dye biosorption As various textile dye efuents are discharged at relatively high temperatures (5060 C), so temperature will be an important design parameter affecting the biosorption capacity in the real application of biosorption by biomass in future [4,5].
Zhou and Banks [82] investigated the effect of temperature on humic acid biosorption by R. arrhizus. They observed that low temperature (from 36 to 16 C) caused a high biosorption. They suggested that biosorption between R. arrhizus and humic acid was an exothermic process and the mechanism was mainly physical adsorption, dominant at lower temperatures [82]. Hu [83] studied the effect of temperature on the removal of six reactive dyes by three Gram-negative bacteria (P. luteola, E. coli, and Aeromonas sp.) and reported that temperature had slight or no effect on the equilibrium uptake suggesting the feasibility of directly using dead biomass in the dyeing wastewater to absorb dyes without decreasing the temperature of wastewater [83]. Gallagher et al. [85] also decided that biosorption of Reactive Brilliant Red by R. oryzae was a physical adsorption due to increase of biosorption capacity with decreasing temperature [85]. Aksu and Tezer [11] also investigated the effect of temperature on the biosorption of Remazol Black B reactive dye by R. arrhizus and their results indicated that optimum adsorption temperature was 35 C and adsorption decreased with further increasing temperature due to the decreased surface activity [11]. Chu and Chen [15,92] studied the effect of temperature on biosorption of Basic Violet 3 and Basic Yellow 24 dyes using dried activated sludge biomass and they observed that adsorption capacity decreased from 113.6 to 109.8 mg g1 for Basic Violet 3 and decreased from 57.0 to 51.3 mg g1 for Basic Yellow 24 with increasing temperature from 20 to 40 C. These results indicated that both biosorption processes are exothermic in nature. They determined the activation energy as 3.27 kcal mol1 for Basic Violet 3 (colorant triarylmethane) biosorption and 1.45 kcal mol1 for Basic Yellow 24 (colorant triarylmethane) biosorption showing fast and intraparticular diffusion limited adsorptions [15,92]. 3.5. Effect of initial dye concentration on dye biosorption Dye concentration also affects the efciency of colour removal. Initial concentration provides an important driving force to overcome all mass transfer resistances of the dye between the aqueous and solid phases. Hence a higher initial concentration of dye may enhance the adsorption process. Bustard et al. [87] observed that although the uptake of Remazol Golden Yellow dye by K. marxianus IMB3 was lower at lower dye concentrations, the biosorptive capacity increased signicantly at higher concentrations of dye. These results suggested some form of cooperativity with respect to interactions between the dye and the biomass. On the other hand for Cibacron Orange dye biosorption by the same biomass, they found that the biosorptive capacity increased to a maximum of 8.5 mg g1 at a residual dye concentration of 100 mg l1 and then decreased rapidly as the equilibrium concentration increased. They suggested one possible reason for this observation that, as the concentration of dye
1010
increases above 100 mg l1 , dyedye interactions become prevalent and these interactions may result in decreased afnity of the dye binding sites on the biomass [87]. The results obtained by Aksu and Tezer [11] showed that the equilibrium sorption capacity of dried R. arrhizus increased with increasing initial Remazol Black B concentration up to 800 mg l1 while the adsorption yield of dye indicated the opposite trend. At 35 C, they found that when the initial Remazol Black B dye concentration increased from 20.5 to 802.4 mg l1 , the loading capacity of biomass increased from 19.3 to 500.7 mg g1 and the adsorption yield of biomass decreased from 94.0 to 62.4% [11]. Aksu [89] reported that the equilibrium sorption capacity of dried activated sludge increased with increasing initial dye concentration up to 200 mg l1 for both Reactive Blue and Reactive Yellow dyes [89]. OMahony et al. [12] reported that uptake of each of the Reactive Red, Rective Blue 19 and Reactive Orange 16 dyes by oven-dried R. arrhizus increased with increasing dye concentration [12]. Chu and Chen [92] investigated the effect of dye concentration on adsorption of Basic Yellow 24 using dried activated sludge biomass. Uptake of the dye increased from 18 to 90 mg g1 with increasing dye concentration from 50 to 300 mg l1 [92]. Dnmez and Aksu [93] also investigated the effect of initial Remazol Blue concentration on the dye sorption capacity and yield of each of nine yeast species between 100 and 400 mg l1 at the initial pH value of 2.0. They found different binding capacities and yields depending on the species and initial dye concentration. However, all the yeast species were capable of removing more than 90% of the colouring material at 100 mg l1 of initial dye concentration [93]. 3.6. Effect of salts on dye biosorption Dyeing processes consume large amounts of salts. So salt concentration in dye wastewater (or the ionic strength of solution) is one of the important factors which inuence the biosorption capacity. Zhou and Banks [77,82] reported that high ionic strength (high concentration of NaCl) led to high biosorption of humic acid by R. arrhizus. They proposed that the effect of ionic strength was similar to that of a colloid. At higher ionic strength, the electrical double layers of both R. arrhizus biomass and humic acid would be compressed thinner. Therefore, biomass and humic acid could approach closer and thus this would increase van der Waals bonding and hence increase biosorption [77,82]. 3.7. Effect of heavy metal ions on dye biosorption Textile wastewaters may include metal ions beside dyes and salts due to metal-containing dyes used in textile industry. Metal ions would be a factor inuencing biosorption rate and capacity. They might compete with dye molecules
for the binding sites or stimulate the biosorption of dye onto biomass. Zhou and Banks [77,82] studied the effect of Cd2+ , Cu2+ , and Al3+ ions on humic acid adsorption by R. arrhizus. They observed that high concentrations of Cd2+ , Cu2+ , and Al3+ resulted in high biosorption. They suggested that metal ion could be a bridge between R. arrhizus and humic acid, which were both negatively charged. So the addition of metal ions would neutralize their surface charge and thus reduce the repulsive forces between them, leading to their closer contact and increase bonding. Metal ions with di- and tri-valent cations could interact with humic acid to form precipitates or aggregates and thus reduce humic acid solubility and increase its biosorption potential [77,82]. OMahony et al. [12] investigated the effect of Cd2+ ions on the uptake of each of the Reactive Red, Reactive Blue 19, and Reactive Orange 16 dyes by oven-dried R. arrhizus. They observed uptake of each of the dye was diminished by the presence of 100 mg l1 Cd2+ ions due to competition between Cd2+ and dye molecules. For Cibacron Red, the maximum reduction was of the order of 20 mg g1 biosorbent which represents 12.5% of maximum dye adsorption levels. They also found similar reductions in uptake of Remazol Blue and Remazol Orange dyes. They explored that the presence of high levels of Cd2+ did not signicantly decrease the adsorption capacity of the biomass [12]. 3.8. Effect of other dyes on dye biosorption (multicomponent dye biosorption) To study the biosorption of a dye or dyes from a multicomponent dye solution which simulate dyehouse or textile mill efuents is important for design. While the knowledge of general uptake of single species of dyes by microorganisms is increasing, relatively little is known about the combined effects of two or more dyes and simultaneous removal of dyes from a mixture of dye solution. OMahony et al. [12] studied with multicomponent dye solutions containing equal concentrations of the Reactive Red, Reactive Blue 19, and Reactive Orange 16 dyes to a maximum total dye concentration of 450 mg l1 . They observed that uptake of each of the dyes from multicomponent solution at pH 2.0 by Rhizopus biomass increased with increasing solution concentration suggesting a direct competition mechanism and no preferentially dye binding [12]. 3.9. Effect of surfactants on dye biosorption In the dyeing process, surfactants are occasionally used and thus may be present in dye wastewaters. Brahimi-Horn et al. [80] observed that the presence of detergent in wastewaters may reduce the binding efciency of the cells and reported that high concentration of Tween, a nonionic surfactant, results in a low adsorption and different dyes show different effects with the same concentration of Tween. The effect of Tween diminished with time [80].
1011
3.10. Regeneration of biosorbent One of the important characteristics of a biosorbent is whether it can be regenerated. Research has shown that biomass can be eluted and regenerated by some organic solvents such as methanol, ethanol, and some surfactants such as nonionic Tween, as well as NaOH solution. Brahimi-Horn et al. [80] used methanol to desorb dyes from bound M. verrucaria cells and recovered 39, 35, and 53% of Orange II, 10B (blue) and RS (red) dye, respectively. They observed that methanol-treated cells still possessed to a large extent the capacity to absorb dyes. They suggested that methanol might inuence the hydrophobic/hydrophilic interaction between the dyes and biomass [80]. Zhou and Banks [82] used 0.1 M NaOH to desorb the humic acid from R. arrhizus biomass because humic acid solubility increased in water at higher pH and thus humic acid was eluted from fungal biomass. The average desorption efciency was above 90%. The results showed that R. arrhizus biosorbents could be used for several sorptiondesorption cycles with similar efciency [82]. Polman and Breckenridge [84] studied the recovery of Reactive Black 5 from R. oryzae using ethanol and Tween 80 and the recoveries were 38.4 and 6.5% at the concentrations of ethanol 60% (v/v in water) and Tween 80 two percent, respectively [84]. 3.11. Effect of shaking rate on dye biosorption 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. Chu and Chen [92] investigated the effect of shaking rate on the biosorption of Basic Yellow 24 using dried activated sludge biomass with 300600 m selected range of particle size. They observed that uptake capacity of biomass increased from 18 to 53 mg g1 with increasing shaking rate from 40 to160 rpm. The results showed that there is a boundary layer surrounding the biomass particles and a decrease in its effect with increasing shaking rate [92]. 3.12. Effect of particle size on dye biosorption 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. Chu and Chen [92] studied the effect of biomass particle size on the biosorption of Basic Yellow 24 using dried activated sludge biomass with 75150, 150300, 300600, 6001180 m selected ranges of particle size. They observed that biosorption capacity of biomass increased with decreasing particle size. This situation was explained by larger total surface area of smaller particles for the same amount of biomass [92].
3.13. Equilibrium modeling of biosorption Hu [7] observed that the adsorption isotherm BG13 blue reactive dye by Aeromonas sp. followed the Freundlich model (Eq. (2)) with the values of KF and 1/n of 0.3769 and 1.255, respectively [7]. Zhou and Banks [82] reported that humic acid adsorption on R. arrhizus obeyed the Freundlich isotherm model which suggested that biosorption occurred on the heterogeneous surface [82]. Hu [83] reported that the biosorption equilibrium of six reactive dyes by dead cells of Aeromonas sp., P. luteola and E. coli tted to Freundlich model [83]. Gallagher et al. [85] used R. oryzae biomass to adsorb Reactive Brilliant Red in solution and observed that both Freundlich and Langmuir (Eq. (1)) isotherm models tted biosorption well, which indicated adsorption by combined mechanisms onto a heterogeneous surface [85]. Bustard et al. [87] reported that the biosorption of Remazol Black B, Remazol Turquoise Blue, Remazol Red onto K. marxianus IMB3 tted to Langmuir model while Remazol Golden Yellow and Cibacron Orange failed to adhere this model [87]. Aksu and Tezer [11] used the Freundlich and Langmuir adsorption models for the mathematical description of the biosorption equilibrium of Remazol Black B on dried R. arrhizus and evaluated the isotherm constants at different temperatures. Equilibrium data tted very well to the Freundlich model in the studied concentration (20800 mg l1 ) and temperature (2555 C) ranges [11]. The Freundlich and Langmuir models were also applied to the biosorption equilibrium data of Reactive Blue 2 and Reactive Yellow 2 dyes onto dried activated sludge by Aksu [91] and both the models were found suitable for describing equilibrium data of both the dyes. The Langmuir and Freundlich constants were used to compare the biosorptive capacity of the dried biomass for both the dyes [91]. Fu and Virarahavan [88] reported that at initial pH 4, biosorption of Basic Blue 9 by A. niger tted the Langmuir equation well; at initial pH 10, the Langmuir and Freundlich isotherm models both tted biosorption well [88]. The isotherm studies for Acid Blue 29 biosorption by A. niger fungus conducted by Fu and Virarahavan [89] showed that the Langmuir, Freundlich, and BET (Eq. (6)) isotherm models all tted well with the experimental data [89]. Isotherm studies performed by Fu and Virarahavan [16,90] indicated that among the Langmuir, Freundlich and BET isotherm models, none was found suitable, but the Radke-Prausnitz model (Eq. (5)) was able to describe the biosorption equilibrium of Congo Red on NaHCO3 pretreated A niger [16,90]. Aksu and Dnmez [93] reported that both the Freundlich and Langmuir adsorption models were found suitable for describing the biosorption of the Remazol Blue reactive dye by all the Candida yeasts (except C. membranaefaciens). According to Langmuir constants, C. lipolytica exhibited
1012
the highest dye uptake capacity (Q0 = 250 mg g1 ) among these species [93]. Basibuyuk and Forster [94] applied the Langmuir model to the biosorption data of basic dye Maxilon Red BL-N by live acivated sludge and they noted that Langmuir equation tted the data very well [94]. 3.14. Biosorption kinetics Hu [83] reported that the time required to reach equilibrium for the biosorption of reactive dyes to dead cells of Aeromonas sp., P. luteola, and E. coli appeared to be very short and was roughly within 1 h [83]. Mittal and Gupta [14] described the biosorption of cationic dyes by F. carnea in the batch adsorber by rst-order reaction kinetics dened in Eq. (16) [14]. Aksu and Tezer [11] applied the pseudo rst- and second-order kinetic models (Eqs. (16) and (18)) to the experimental kinetic data of Remazol Black B biosorption on dried R. arrhizusassuming that the external mass transfer limitations in the system can be neglected. The results indicated that the dye uptake process followed the pseudo second-order rate expression and adsorption rate constants increased with increasing temperature up to 35 C and decreased with increasing concentration [11]. The kinetic studies performed by Fu and Virarahavan [16,8890] for the biosorption of Acid Blue 29, Basic Blue 9 and Congo red by treated A. niger, indicated that equilibrium was reached in 30, 48, and 42 h, respectively, dependent on initial pH of the dye solution. These equilibrium times were shorter than the time observed by Zhou and Banks [82] (3 days) and Gallagher et al. [85] (4 weeks). They also reported that the Lagergren rst-order and pseudo second-order rate equations were able to provide a realistic description of biosorption kinetics for the biosorption of all dyes by treated A. niger [16,8890]. Aksu [91] reported that the initial sorption of Reactive Yellow 2 occurred more rapidly by dried activated sludge than that of Reactive Blue 2. Equilibrium was established in 1530 min for Reactive Yellow 2 and in 3060 min for Reactive Blue 2 at all dye concentrations studied. The results showed that the uptake process of each of the dye is not Lagergren rst-order reaction and that the second-order model, based on the assumption that the rate limiting step may be chemical biosorption [91]. Work carried out by Chu and Chen [15] indicated that equilibrium was established in 6 h for the biosorption of basic dyes by dead activated sludge. They observed that the kinetics of initial adsorption stage of basic dyes by biomass is a rst-order process and is controlled by lm diffusion according to Eq. (13) [15]. Chu and Chen [15] also studied the rate processes for the adsorption of Basic Yellow 24 dye on dried activated sludge as a function of shaking rate, initial dye concentration, biomass particle size, and dye solution temperature. The experimental results indicated that there is a boundary layer surrounding the biomass parti-
cles, the kinetics of the adsorption process is mainly controlled by intraparticle diffusion due to Weber-Morris theory (Eq. (14)). Aksu and Dnmez [93] studied the biosorption kinetics of nine yeasts for Remazol Blue reactive dye removal at 200 mg l1 initial dye concentration for the rst 240 min of biosorption. The results showed that the biosorption behaviour and biosorption capacities of all the yeasts were different from each other. Initial sorption of Remazol Blue dye by S. cerevisiae, S. pombe, K. marxianus, and C. utilis yeast cells occurred more rapidly than by other Candida yeasts. A larger amount of dye was removed by these dried cells in the rst 15 min of contact (69, 68, 58 and 57%, respectively). An equilibrium was established in 240 min for these biosorbents for all the initial dye concentrations studied and equilibrium did not change subsequently up to 72 h. They suggested that for these yeast cells the uptake of dye occurs predominantly by surface binding and that available sites on the biosorbent are the limiting factor for the biosorption. In contrast with the Candida yeasts, they proposed that the intracellular uptake by these cells appears to be insignicant [93]. The data obtained by Basibuyuk and Forster [94] showed that a contact time of 2 h was sufcient to achieve equilibrium for the Maxilon Red adsorption by live activated sludge. The results indicated that the initial part of the Maxilon Red adsorption followed a rst-order process dened by Eq. (13) controlled by lm diffusion. Although intraparticle diffusion played a signicant role, it was not the main rate determining step throughout the adsorption. A comparison of the kinetic models on the overall adsorption rate showed that the Maxilon Red and live activated sludge system was best described by the pseudo second order kinetic model [94]. 3.15. Column studies Banks and Parkinson [79] packed the autoclaved R. arrhizus mycelia in a sorption column to remove the organic colour in raw water attributed to humic acid. They reported that active sites for humic acid adsorption on fungal biomass in R. arrhizus were on the fungal cell wall and were most probably the chitin/chitosan components [79].
4. Biosorption of phenols and phenolic compounds In recent years, a number of studies have focused on some microorganisms including bacteria and fungi which are able to biosorb phenols and chloro- and nitro-phenols. Depending on the phenolic compound and the species of microorganism used also different binding capacities have been determined (Table 2). The researchers have selected the pH, initial pollutant and biomass concentrations and pretreatment method as important parameters affecting the removal efciency of phenolics.
Z. Aksu / Process Biochemistry 40 (2005) 9971026 Table 2 Data on the biosorption of phenol and phenolic compounds by various microorganisms Biosorbent Phenolic compound Operation conditions pH Activated sludge Activated sludge PCP Phenol o-Chlorophenol p-Chlorophenol PCP Phenol Phenol 2-CP 3-CP 4-CP 2,3-DCP 2,4-DCP 2,5-DCP 2,6-DCP 3,4-DCP 3,5-DCP 2,3,4-TCP 2,3,5-TCP 2,3,6-TCP 2,4,5-TCP 2,4,6-TCP PCP 2-NP 4-NP 2,4-DNP Phenol 2,4-DCP 4-CP 4-CP PCP PCP Phenol 2-CP 3-CP 4-CP 2-NP 4-NP 2,4-DCP 3,4-DCP 3,5-DCP 2,4,5-TCP 1.0 1.0 1.0 7.0 1.0 1.0 7.5 7.5 7.5 7.5 7.5 7.5 7.5 7.5 7.5 7.5 7.5 7.5 7.5 7.5 7.5 7.5 7.5 7.5 5.1 6 6 6.1 7 6 6 6 6 6 6 6 6 6 6 T ( C) C0 (mg l1 ) teq 3 days 50 min 350 min 350 min 2h 2h 2h 2h 2h 2h 2h 2h 2h 2h 2h 2h 2h 2h 2h 2h 4h 4h 4h 24 h 3h 3h 2h 1.5 min 3 days 260 h 3h 3h 3h 3h 3h 3h 3h 3h 3h Biosorption capacity qeq (mg g1 )
1013
Ref.
20 25 25 25 25 25 25 35 35 35 35 35 35 35 35 35 35 35 35 35 35 35 29 29 29 21 20 20 25 30 20 20 20 20 20 20 20 20 20 20 20
1a 100 100 100 0.5 500 500 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 90 90 90 1 163 128.6 50 1a 800 800 800 800 800 800 800 800 800 800
3.3 86.1 102.4 116.3 2.56 166.6 245.0 0.0016 0.0203 0.0219 0.0216 0.0638 0.0291 0.0066 0.0595 0.0726 0.0489 0.0271 0.0132 0.0324 0.0189 0.2704 1.43 1.51 1.87 0.5 9.1 3.0 72.3 23.0 14.9 0.4 0.34 1.0 1.0 0.12 0.31 2.7 5.0 3.0 2.7
[95] [101]
Activated sludge Activated sludge Anaerobic sludge Anaerobic granular sludge
[103] [104] [105] [43]
Anaerobic granular sludge
[107]
Aspergillus niger Emericella nidulans Kluvera cryocrescens Mycobacterium chlorophenolicum PCP-1 Rhizopus arrhizus Papermill sludge
[41] [102] [106] [99] [95] [40]
Equilibrium concentration.
4.1. Microorganisms and phenolics used in biosorption: biosorption mechanisms Bell and Tsezos [95] reported on the biosorption of pentachlorophenol (PCP) onto two types of inactive microbial biomass; a mixed culture of aerobic activated sludge and a pure culture of R. arrhizus. Based on the examination of the uptake by cell walls, they concluded that biosorption process involves uptake by both the cell walls and other cellular components of the microorganisms [95]. They obtained that dead cells of R. arrhizus had a higher biosorption capacity
for PCP than that of dead activated sludge. Tsezos and Bell [96] also studied the biosorption of PCP by live cells of activated sludge and R. arrhizus. They found the biosorption of PCP to be nonlinear and correlated with the octane/water partition coefcient (Kow , dened as the ratio of concentrations in water immiscible n-octanol phase to one in aqueous phase) on both type of biosorbents within the concentration range (about 10 mg l1 ) studied. They related the uptake of PCP to the hydrophobicity of the target pollutant according to the hydrophobic partitioning model giving the correlation between octanolwater partition coefcient and
1014
the solid phase concentration (qeq ) within the concentration range studied [96]. Kennedy et al. [43] studied live anaerobic granular sludge for the sorption of a number of chlorophenols (phenol, most isomers of tri-, di-, and monochlorophenols and pentachlorophenol), observing that the component and content of cellular lipids would inuence the adsorption capacity. They found no obvious relationship between sorption and numbers or positions of chlorine substituents. The results showed that PCP was more strongly sorbed than the lesser-chlorinated phenols. Although the correlation coefcent (<0.6) indicated that Kow only partly described the sorption of chlorophenols to granular sludge, in general, the uptake capacity of live anaerobic biomass tended to increase with increasing octanolwater partition coefcient which is an indicator of hydrophobicity. They found that the PCP uptake capacity of live anaerobic sludge was much less (20- and 10-fold) than that of live or dead aerobic sludge obtained by Bell and Tsezos [95] and Tsezos and Bell [96]. They attributed these differences in biosorption capacity for anaerobic and aerobic biomass to the varying lipid composition and content of different biomasses. Another factor inuencing the sorptive capacity of anaerobic biomass was given as the test temperature (35 C) which is higher than that of Tsezos and Bells study (20 C) assuming adsorption is exothermic [43]. Logan et al. [97] studied the biosorption of PCP by 12 species of white rot fungi. In general PCP adsorption to mycelia was very low, ranging from 1 to 5 mg PCP g mycelium (dry weight basis)1 at 40 mg l1 PCP. Several species of fungi, including P. chrysosporium, T. versicolor and all Ganoderma sp. removed >50% of the PCP within 24 h [97]. Jacobsen et al. [98] also studied the adsorption and desorption of PCP to activated sludge biomass [98]. Brandt et al. [99] investigated the biosorption of PCP on the cells of Mycobacterium chlorophenolicium PCP-1, a Gram-positive bacterium. They proposed that adsorption mechanisms were a combination of reversible and irreversible adsorption processes. They suggested that the reversible adsorption was due to a physical adsorption (ion exchange) of the ionic PCP on the cell wall, while the irreversible adsorption was due to interaction between very hydrophobic PCP and hydrophobic cell membrane. In contrast to the results of Tsezos and Bell [96], they found that PCP is only adsorbed on the cell wall and sorption equilibrium was normally reached in less than 1.5 min [99]. Daughney and Fein [100] observed that 2,4,6-trichlorophenol (2,4,6-TCP) displayed a strong afnity for the cell walls of B. subtilis. They described 2,4,6-TCP-B. subtilis sorption by a surface complexation model in which both the negative and the neutral forms of TCP form 1:1 surface complexes with the neutral hydroxyl functional groups of the bacteria [100]. Aksu and Yener [39,101] investigated the biosorption of phenol and monochlorinated phenols (o-chlorophenol and
p-chlorophenol) on the dried activated sludge. They suggested that the cell wall of bacteria essentially consisting of various organic compounds such as chitin, acidic polysaccharides, lipids, amino acids and other cellular components is responsible for the uptake of organic pollutants. They determined the maximum saturation capacity of biosorbent as 236.8, 281.1, and 287.2 mg g1 for phenol, o-CP and p-CP, respectively. They found a higher adsorption capacity for o- and p-CP than that of phenol. They explained this behaviour due to the activation of the aromatic ring of monochlorophenol by the chlorine. This favored the formation of donoracceptor interactions between the phenolic compound and the groups of the biosorbent surface. They also suggested that biosorption capacity is affected by the position of Cl group on the ring. Biosorption of p-CP having a chlorine in the para position tended to be higher than o-chlorophenol containing chlorine in only ortho position. This may be a result of steric hindrance between the Cl and OH group in the case of o-chlorophenol [39,101]. Benoit et al. [102] studied the biosorption of 2,4-dichlorophenol (2,4-DCP) and 4-chlorophenol (4-CP) on the freeze-dried mycelium of Emericella nidulans and Penicillium miczynskii, isolated from composted wheat straw and a soil, respectively. Results obtained with inactivated fungal cells showed that P. miczynskii had a higher biosorption capacity for 2,4-DCP than that of E. nidulans due to different biochemical compositions and physicochemical properties of both fungi, and the biosorptive uptake of 2,4-DCP was higher than that of 4-CP. Higher sorption of 2,4-DCP was explained with increase in the polarity, decrease in the pKa of the phenol and enhance in the hydrophobicity of the substituted benzene ring due to the increase in chlorosubstitution. The rapid adsorption on fungal cell walls surfaces was the main sorption phenomenon for the more hydrophobic molecules [102]. Jianlong et al. [103] characterized the adsorption behaviour of pentachlorophenol from aqueous solution to activated sludge biomass collected from a local biological wastewater treatment plant [103]. The ability of dried activated sludge and dried anaerobic sludge to adsorb phenol was investigated by Aksu and Akpinar [104,105] in the absence and in the presence of heavy metal ions. They found that dried anaerobic sludge had a higher adsorption capacity than that of dried activated sludge [104,105]. Calace et al. [40] studied the sorption capacity of paper mill sludge produced from primary (sedimentation) and secondary (biological) treatments of a pulp and paper industry wastewater, for phenol, 2-chlorophenol (2-CP), 3-chlorophenol (3-CP), 4-chlorophenol (4-CP), 2-nitrophenol (2-NP), 4-nitrophenol (4-NP), 2,4-dichlorophenol (2,4-DCP), 3,4-dichlorophenol (3,4-DCP) 3,5-dichlorophenol (3,5-DCP) and 2,4,5-trichlorophenol (2,4,5-TCP) under batch conditions. The phenols selected were phenol and mono-, di- and trichlorophenols and mono-nitrophenols characterized by different pKa and solubility values. The
1015
order of sorption capacity on papermill sludge was: 2-NP = 4-NP 2-CP < phenol < 4-CP = 3-CP < 2, 4-DCP < 3, 4-DCP = 2, 4, 5-TCP < 3, 5-DCP. On the basis of the order of retention selectivity obtained, they hypothesized that hydrophobic interactions drive the phenol sorption on the sludge surface and that the main chemical features of phenols playing an important role in sorption mechanisms are solubility and pKa [40]. Rao and Viraraghavan [41] examined the phenol removal capacity of pretreated non-viable A. niger biomass from an aqueous solution containing phenol at a concentration of 1 mg l1 . They observed that sulphuric acid-treated biomass powder was the most effective for the removal of phenol [41]. A biolm represents a stable ecosystem. The main compositions of biolms are bacterial cells, extracellular polymers produced by the bacteria (exopolymers), lysis and hydrolysis products, attached organic matter and some inorganic compounds. Exopolymers consist mainly of polysaccharides, proteins, uronic acids, humic acids, nucleic acids, lipids, and cell fragments. In biolms, possible sorption sites are extracelluar polymeric substances, cell wall, cell membranes, and cytoplasm. These sites contribute to the sorption properties of biolms to organic and inorganic substances. Wang et al. [106] investigated the p-chlorophenol (4-CP) biosorption to biolm components under the conditions of temperature 25 C, pH values of 2.7, 5.3, and 6.1 in a batch system. They chose biolm coated kaolin, bacteria and bacterial exopolysaccharide (EPS) as biolm components for the adsorption of 4-CP. The bacteria used in this study was identied as Kluvera cryocrescens. They explained that the interaction between 4-CP and biomass is poorly understood. There could be the protonation of carboxyl, phosphate, and hydroxyl functional groups on K. cryocrescens bacteria. The bacterial surface develops a negative electric potential due to deprotonation of its surface functional groups. This potential affects the hydrophobicity of the surface, and it inuences interactions between the surface sites and charged species in solution [106]. Karim and Gupta [107] investigated the biosorption of 2-nitrophenol (2-NP), 4-nitrophenol (4-NP) and 2,4-dinitrophenol (2,4-DNP) on live anaerobic granular sludge in order to understand their fate in an upow anaerobic sludge blanket reactor. They demonstrated that the uptake of each nitrophenol was only weakly correlated to their respective octanolwater partition coefcients [107]. 4.2. Pretreatment of microorganism Tsezos and Bell [96] compared the biosorption of pentachlorophenol by live activated sludge and R. arrhizus with the results obtained by treated (autoclaved) activated sludge and R. arrhizus. They observed that the PCP uptake capacity of dead R. arrhizus was six times higher than that of live R. arrhizus. In the case of activated sludge, however, they found that live sludge had higher biosorption capacity. They
attributed this situation to the biodegradation of a portion of the PCP [96]. Rao and Viraraghavan [41] examined the phenol removal capacity of pretreated non-viable A. niger biomass from an aqueous solution. They pretreated live fungal pellicles in ve different ways: autoclaving, treatment with 0.1 M HNO3 , treatment with 0.1 M H2 SO4 , treatment with 0.1 M NaOH, treatment with a laboratory detergent (5 g l1 ). They found that the removal trend was as follows: sulfuric acid pretreated (50%) > laboratory detergent (42%) > sodium hydroxide (39.9%) > autoclaved biomass (26.8% > nitric acid (20.6%). They proposed that the difference in the percentage removal between H2 SO4 and HNO3 pretreated biomass could be due to the difference in the numbers of H+ ions contributed by them at the same molarity during pretreatment. Sodium hydroxide pretreated and laboratory detergent pretreated biomasses gave very close removals. Alkali pretreatment has also been shown to be a probable cause for destroying autolytic enzymes that cause putrefaction of the biomass and for removing lipids and proteins that mask reactive sites [41]. Gallagher et al. [85] have also suggested that NaOH pretreatment may also increase the percentage of chitin/chitosan in the whole cell wall fraction by dissolving certain biopolymers from the cell wall. Chitin/chitosan units may then be responsible for the uptake of phenol in the case of NaOH pretreated biomass [85]. Benoit et al. [102] pretreated E. nidulans and P. miczynskii by freeze drying, autoclaving (121 C, 103.4 kPa for 20 min) and autoclaving in the presence of formaldehyde at 30 g l1 and they observed that for both fungi, autoclaving increased the 2,4-DCP biosorption capacity 10% higher than that of freeze-dried and autoclaved with formaldehyde cells due to the solubilization of carbohydrates and peptidic compounds resulted in modications of chemical compositions on the fungal cell walls during heat sterilization [102]. 4.3. Effect of pH on phenolics biosorption Brandt et al. [99] observed that the adsorption capacity of M. chlorophenolicium PCP-1 for PCP increased with decreasing pH. The overall adsorption capacity at pH 5.4 was about eight-fold higher than that at pH 7.0. The effect of pH on the sorption behaviour was found to be related to the ionization of PCP. They demonstrated that the irreversibly adsorbed PCP is a function of undissociated PCP, while the reversibly adsorbed PCP correlates well with the concentration of ionic PCP [99]. Aksu and Yener [39,101] dened the pH of the sorption medium as the most critic parameter in the treatment of phenol and monochlorinated phenols by the dried activated sludge that affects biosorption capacity. They obtained that phenol and monochlorinated phenols were more effectively adsorbed to the biomass at very low values of pH and they determined the optimum initial pH as 1.0. They explained the change in biosorption due to pH with the ionization of phenols and chlorinated phenols, alterations in the sorbent
1016
surface and the interaction of phenols and chlorinated phenols with the cells with primarily electrostatic forces or complex formation or electron share in nature or membrane transport [39,101]. Jianlong et al. [103] demonstrated that the initial pH value was an important parameter affecting the pentachlorophenol adsorption capacity of activated sludge biomass that increased with decreasing pH (between 6.0 and 8.0). The equilibrium adsorption capacity dropped from 3.0 to 2.0 mg g1 when the initial pH was increased from 6.0 to 8.0. They explained the decrease in adsorption capacity of biomass with an increase in pH value due to the fact that as the pH increased, the overall surface charge on the cells became negative and this led to a lower electrostatic attraction between negatively charged PCP and binding sites of the biomass surface [103]. Aksu and Akpinar [104,105] studied the uptake of phenol by both the dried activated sludge and dried anaerobic sludge as a function of initial pH. The results obtained showed that the uptake of phenol increased with decreasing initial pH and was the greatest at pH 1.0 for both biosorbents [104,105]. Rao and Viraraghavan [41] also studied the effect of initial pH on the phenol removal capacity of sulfuric acid pretreated A. niger biomass. They obtained the maximum removal of phenol at an initial pH of 5.1 and they reported that an increase or decrease in the pH from this optimum pH resulted in a reduction in the biosorption of phenol. They explained the biosorption mechanism due to pH as a fact that phenol could be expected to become negatively charged phenoxide ion above a pH of 9.0 because of pKa value of phenol (=9.99 at 25 C). The surface charge on fungal biomass is predominantly negative over the pH range of 3.010.0. Below a pH of 3.0, the overall surface charge on fungal cells becomes positive. Pretreating it with sulfuric acid could generate positively charged sites on its surface due to the sorption of an excess of H+ ions. Phenol being weakly acidic will be partially ionized in solution. These ions will be negatively charged and will be directly attracted due to electrostatic forces by the positively charged fungal biomass surface. Unionized phenol molecules will also be attracted, possibly by physical forces. At a high basic pH range, OH ions would compete with the phenol molecules for biosorption sites. Sorption of an excess of OH ions could convert an initial positively charged surface into a negatively charged surface. This surface would then repel the negatively charged phenoxide ions. This was probably the reason why there was a decrease in biosorption at the basic range with ultimately no biosorption taking place at an initial pH of 10.0. At a low acidic pH of 2.0, phenol molecules get protonated and subsequently positively charged. This causes repulsion between the positively charged fungal surface and phenol molecules leading to a decreased uptake of phenol [41]. Calace et al. [40] studied the sorption capacity of paper mill sludge for phenol, and mono, di- and trichlorophenols solutions at pH 2.0 and 11.0. They found that the amount adsorbed increased with decreasing pH due to increase the
number of hydrophobic adsorptive domains on the surface and the undissociated fraction of chlorophenols that are able to interact at low pH value [40]. Wang et al. [106] investigated the impact of pH value on the p-chlorophenol (4-CP) biosorption to biolm components over the pH range 2.06.0 for an initial adsorbate concentration 20 mg l1 . They observed that the amount adsorbed slightly increased with increasing pH from 2.7 to 6.1 for the adsorption system of bacterial exopolysaccharide but it slightly decreased in the systems of biolm coated kaolin and K. cryocrescens biomass. They proposed that 4-CP was in the dissociated and undissociated forms in solutions within the pH range in these experiments. When pH decreased, H+ ion concentration increased and the undissociated forms of 4-CP increased in proportion. The undissociated 4-CP was highly hydrophobic, it was easier to be adsorbed than its dissociated form. The decrease of pH was useful for 4-CP adsorption on bacteria and kaolin with biolm coating. When pH increases, bacterial exopolysaccharide adsorbed more 4-CP [106]. 4.4. Effect of initial phenol concentration on phenolics biosorption Aksu and Yener [39,101] observed that the equilibrium sorption capacity of the dried activated sludge for phenol, o-chlorophenol and p-chlorophenol increased with the initial pollutant concentration up to 500 mg l1 . They suggested that the increase of loading capacity of biosorbent with the increase of pollutant concentration may be due to higher probability of collision between pollutants and biosorbent and sufcient active sites [39,101]. Jianlong et al. [103] also observed that the equilibrium sorption capacity of the activated sludge increased with increasing initial PCP concentration up to 0.5 mg l1 [103]. The results obtained by Aksu and Akpinar [104,105] showed that the equilibrium uptake of phenol by dried aerobic and anaerobic sludges increased with increasing initial phenol concentrations up to 500 mg l1 for both biosorbents. The curvilinear relationship between the amount of phenol adsorbed per unit weight of each microorganism and the residual phenol concentration at equilibrium suggested that saturation of cell-binding sites occurred at higher concentrations of this component [104,105]. Karim and Gupta [107] studied the sorption 2-NP, 4-NP and 2,4-DNP on live anaerobic granular sludge at different sorbate (nitrophenols) concentrations changing between 10 and 90 mg 11 and they found that equilibrium sorption capacity of biomass increased with increasing each initial nitrophenol concentration [107]. 4.5. Effect of biosorbent concentration on phenolics biosorption Brandt et al. [99] demonstrated that the adsorption capacity of M. chlorophenolicium PCP-1 for PCP increased sig-
1017
nicantly with decreasing biomass concentration in the low concentration range (below 0.5 g l1 ). They explained this situation by a smaller accessible sorbent surface resulting from cells that are closer to each other at high cell density [99]. Jianlong et al. [103] investigated the effect of activated sludge concentration on the adsorption of PCP. The biomass concentration varied from 0.5 to 5.0 g l1 . They observed that on one hand, as expected, the percentage of the PCP removal increased with increasing activated sludge concentration. But conversely, the absorbed amount of PCP per biomass quantity decreased with the increasing biomass concentration. The adsorption capacity dropped from 2.6 to 1.1 mg g1 when the biomass concentration increased from 0.5 to 5.0 g l1 . The drop in adsorption capacity was explained due to binding sites of the biomass remaining unsaturated during the adsorption reaction [103]. 4.6. Effect of heavy metal ions on phenolics biosorption Wastewaters of steel, metal plating, dye, textile, and painting industries frequently encounter organics along with heavy metal ions. The examining the combined effects of metal ions and organics in various combinations is more representative, of the actual environmental problems faced by organisms, than are single organic studies. In mixtures of two or more components in a solution, the synergistic or antagonistic interaction occurring between the components may affect the individual component uptake by the microorganism. The phenol uptake by dried activated sludge in the presence nickel(II) ions and the biosorption of phenol by dried anaerobic sludge in the presence chromium(VI) ions were investigated by Aksu and Akpinar [104,105] with respect to initial pH and initial concentration of each component in the adsorption medium. They observed that the equilibrium uptake of phenol was diminished by the addition of metal ions in the concentration range of 25500 mg l1 due to antagonistic interaction between the components for both sorbents. The most logical reason for this behaviour was claimed to be the competition for similar binding sites on the surface of cells and/or the screening effect by the second component [104,105]. 4.7. Regeneration of biosorbent Tsezos and Bell [96] used distilled deionized water for the desorption of PCP from live cells of activated sludge and R. arrhizus, and demonstrated that the biosorption of PCP by both live cells was partially irreversible [96]. Kennedy et al. [43] used a method based on contacting the loaded biomass with the adsorbate solution for the desorption of 3-chlorophenol, 3,4-dichlorophenol and 2,4,6-trichlorophenol from anaerobic granular sludge. They found that the adsorption of 3,4-DCP and 2,4,6-TCP was
almost completely reversible while 3-CP exhibited a greater degree of irreversibility [43]. Brandt et al. [99] found that the desorption of PCP from M. chlorophenolicium PCP-1 from was strongly affected by pH. At pH 5.4 the adsorption was almost completely irreversible, while a nearly complete desorption was obtained at pH 7.0 [99]. Benoit et al. [102] used 0.01 M CaCl2 to desorb 2,4-DCP and 4-CP from bound freeze-dried E. nidulans cells and found that biosorption was only partially reversible and the decrease of irreversibility of biosorption was related to an increase in chlorosubstitution [102]. This was consistent with results of Kennedy et al. [43] who also observed that the irreversibility of sorption on bacterial biomass was stronger for 3-chlorophenol than for 3,4-dichlorophenol [43]. Rao and Viraraghavan [41] found that the desorption of phenol from A. niger with distilled deionized water gave the maximum desorption of only about 5% which suggested strong biosorption by the biomass [41]. Karim and Gupta [107] used a dilution media (0.01 M NaOH solution adjusted to pH 7.5) to desorb 2-NP, 4-NP, and 2,4-DNP from bound anaerobic granular sludge and demonstrated that the sorption nitrophenols was partially reversible. About 2089%, 3690%, and 2980% desorption was observed for 1090 mg 11 sorbate concentrations of 2-NP, 4-NP, and 2,4-DNP, respectively [107]. 4.8. Equilibrium modeling of biosorption Tsezos and Bell [96] reported that the biosorption of PCP to living and dead activated sludge and R. arrhizus biomasses was non-linear and could be described by the Freundlich equation [96]. Kennedy et al. [43] investigated the tting of sorption data of phenol and a number of chlorophenols by anaerobic granular sludge to the Freundlich equation. The authors reported that most chlorophenols had linear sorption isotherms (1/n close to 1), which were dened by simple distribution coefcients (Eq. (7)). A linear adsorption isotherm commonly occurs when relatively pure, porous sorbents are used and is being carried out over a relatively small concentration range. The availability of sorption sites remains constant at all concentrations up to saturation, typical of the partitioning of a solute between two immiscible solvents. They proposed that the granules which consist of a consortium of anaerobic bacteria and are known to be very porous allowing penetration of sorbate to sorption sites in the inner portion of the granules, behaved mainly as a homogeneous and pure sorbent. However, these distribution coefcients were found only weakly correlated to octanolwater partition coefcients [43]. Jacobsen et al. [98] also observed linear sorption isotherms in the biosorption of PCP by activated sludge up to 0.08 mg l1 of dissolved PCP at pH 6, and up to 0.16 mg l1 at pH 8. They concluded that linear sorption coefcients were primarily inuenced by pH, although ionic
1018
strength (owing to pH-buffering) and the concentration of dissolved organic matter also had an impact [98]. Brandt et al. [99] observed that the sorption equilibrium data of PCP on M. chlorophenolicium PCP-1 was adequately described by the Freundlich equation, indicating no clear adsorption saturation. They also investigated the effect of biomass concentration on KF and n and found that KF was signicantly affected by lower biomass concentration while n was independent of the biomass concentration [99]. The sorption phenomena of phenol, o-chlorophenol and p-chlorophenol to dried activated sludge were expressed by the Langmuir and Freundlich adsorption models by Aksu and Yener [39,101]. The adsorption isotherms showed that the equilibrium data for all the pollutants tted well to both the Langmuir and Freundlich models in the studied concentration range studied for all the pollutants [39,101]. Benoit et al. [102] applied the Freundlich model to describe the biosorption equilibrium of 2,4-DCP and 4-CP from aqueous solution to freeze-dried and autoclaved with formaldehyde E. nidulans biomasses. These authors obtained that in both conditions, sorption isotherms were close to linearity (1/n close to 1) and autoclaved with formaldehyde E. nidulans had lower KF values for 2,4-DCP and 4-CP which could be due to a competitive effect of formaldehyde for the sorption sides [102]. Jianlong et al. [103] applied the Freundlich model to describe the biosorption equilibrium of pentachlorophenol from aqueous solution to activated sludge biomass by changing the initial PCP concentrations from 0.025 to 0.5 mg l1 . Both the biomass concentration and pH value only affected the capacity constant KF of the Freundlich equation while the intensity constant n remained constant. Attempts to use the Langmuir equation to t the adsorption isotherm failed to provide a satisfactory correlation [103]. Aksu and Akpinar [104] dened the equilibrium uptake of phenol in the presence of nickel(II) ions by dried activated sludge by competitive multi-component Langmuir, Freundlich and RedlichPeterson adsorption models (Eqs. (8)(11)) and estimated model parameters by the non-linear regression method at two optimum biosorption pH values determined as 4.5 for nickel(II) and as 1.0 for phenol. The results showed that all the multi-component adsorption models adequately predicted the multi-component adsorption equilibrium data at moderate ranges of concentration [104]. Aksu and Akpinar [105] also expressed the equilibrium uptake of phenol by dried anaerobic sludge in the presence of chromium(VI) ions by multi-component Langmuir, Freundlich and RedlichPeterson adsorption models and they found that modied Freundlich model adequately predicted the multi-component adsorption equilibrium data at moderate ranges of concentration [105]. Calace et al. [40] attempted to t the three equations (Langmuir, Freundlich and Langmuir-Freundlich) to their experimental data. The results showed that the biosorption equilibrium of phenol, mono-, di-, and tri-chlorophenols and
mono-nitrophenols tted the Hill equation very well, which is mathematically equivalent to the LangmuirFreundlich model (Eq. (3)) obtained by assuming that the surface is homogeneous, and that the adsorption is a cooperative process inuenced by adsorbateadsorbate interactions [40]. Rao and Viraraghavan [41] tted the Langmuir, Freundlich and the BrunauerEmmetTeller isotherm models to the isotherm data of phenol biosorption by H2 SO4 treated A. niger biomass. They found that the adsorption of phenol by treated biomass was best described by the BET model [41]. The adsorption data of p-chlorophenol by biolm components (biolm coated kaolin, bacterial exopolysaccharide and K. cryocrescens) was analyzed with Langmuir and Freundlich models to evaluate the parameters in the adsorption process by Wang et al. [106] at 25 C. All the adsorptions tted to these two equations. The maximum adsorption capacity was 72.3 mg 4-CP g1 dry bacteria and 6.6 mg 4-CP g1 biolm coated kaolin [106]. Karim and Gupta [107] tted the Freundlich equation to the equilibrium data of three nitrophenols (2-NP, 4-NP and 2,4-DNP). Since they found 1/n, the Freundlich constant, as 1.0 for all nitrophenols, they concluded that there is a linear relationship between nitrophenol concentration in the liquid and solid phases and equilibrium can be shown by linear adsorption isotherms suggesting a constant-partitioning sorption mechanism [107]. 4.9. Biosorption kinetics The detailed investigation on sorption of 15 chlorinated phenols onto anaerobic granular sludge conducted by Kennedy et al. [43] indicated that a rapid biosorption occurred and equilibrium was reached in less than 2 h for the sorption of all chlorophenols by anaerobic granular sludge [43]. Jacobsen et al. [98] observed that equilibrium conditions for sorption and desorption of pentachlorophenol to microbial biomass were established within 5 min [98]. Daughney and Fein [100] observed that the sorption and desorption reactions of 2,4,6-trichlorophenol by the cell walls of B. subtilis were reversible and rapid. The adsorption equilibration occurred in approximately 30 min [100]. Aksu and Yener [39,101] observed that initial sorption of phenol occurred very rapidly by the dried activated sludge; sorption reached equilibrium in 4560 min at 100 mg l1 initial phenol concentration. Adsorption proceeded at a slower rate in the case of o- and p-chlorophenol. They noted that although the initial phenol biosorption rate by dried activated sludge was higher than that of o-and p-chlorophenol, the equilibrium uptakes of phenol by biomass were lower than that of o- and p-chlorophenol [39,101]. Benoit et al. [102] indicated that the biosorption of 2,4-DCP by treated E. nidulans and P. miczynskii cells was fast and the equilibrium was reached within the rst 3 h of contact [102].
1019
Jianlong et al. [103] indicated that the pentachlorophenol biosorption equilibrium was reached in less than 2 h under experimental conditions. No changes in PCP concentrations were observed during prolonged shaking [103]. Rao and Viraraghavan [41] reported that biosorption of phenol by treated A. niger biomass reached equilibrium within 24 h. [41]. Kinetic experiments performed by Calace et al. [40] showed that substituted chlorophenol sorption on papermill sludge was rapid (equilibrium was reached after 3 h); conversely, the time taken by the phenol to reach equilibrium conditions was 260 h. Evaluating the experimental data by using Eq. (17) they found that intraparticle diffusion was involved in the sorption process but was not the only rate-limiting mechanism; several other mechanisms were involved [40]. Wang et al. [106] investigated the kinetic characteristics of 4-CP adsorption by biolm components. They observed different times to reach equilibrium in each system. The 4-CP adsorption by kaolin with biolm coating and EPS reached near equilibrium at 60 and 180 min at pH 6.1, respectively. But the 4-CP adsorption by bacteria K. cryocrescens showed no evident near equilibrium during 3 h in the experiment, the adsorption reached equilibrium slowly [106]. 4.10. Column studies Rao and Viraraghavan [40] studied phenol biosorption by immobilized H2 SO4 treated A. niger biomass in polysulphone in a packed bed column. They obtained phenol removal as 66% from breakthrough curves for up to 2 h at 1 mg l1 phenol concentration in the inuent with an adjusted pH of 5.1 at 7.0 ml min1 ow rate. The breakthrough data were tted to the Thomas model (Eq. (21)). Biosorption
Table 3 Data on the biosorption of pesticides by various microorganisms Biosorbent Pesticide Operation conditions pH Activated sludge Lindane Diazinon Malathion Lindane Lindane 2,4-D Lindane PCNB PCNB Lindane Diazinon Malathion 2-Chlorobiphenyl PCNB Lindane 6.0 T ( C)
capacity of the beads for phenol was found to be 0.2 mg g1 with a correlation coefcient of 0.93 [40]. Aksu and Gonen [108] used Mowital B30H resin immobilized dried activated sludge for the biosorption of phenol in a continuous xed bed. They applied four kinetic models; Adams-Bohart (Eq. (19)), Thomas, Clark (Eq. (22)) and Yoon-Nelson (Eq. (25)) models to experimental data to predict the breakthrough curves and to determine the characteristic parameters of the column useful for process design. All models were found suitable for describing the whole or a denite part of dynamic behaviour of the column with respect to ow rate and inlet phenol concentration. They determined the biosorption capacity of immobilized sludge for phenol as 6.4 mg g1 at 52.3 mg l1 initial phenol concentration with an adjusted pH of 1.0 at a ow rate of 0.8 ml min1 from the Thomas model [108].
5. Biosorption of pesticides Application of biosorption for pesticides is also possible and several microorganisms including bacteria and fungi have been studied for the removal of some pesticides. Table 3 presents a comparison of biosorption capacities of some microorganisms for some pesticides at their working conditions. 5.1. Microorganisms used in pesticide biosorption and biosorption mechanisms Bell and Tsezos [95] and Tsezos and Bell [96] studied the biosorption of lindane, diazinon, malathion and 2-chlorobiphenyl which are widely used organochlorine and organophosphorus insecticides, onto live and dead cells of activated sludge and R. arrhizus. They proposed that a part
Biosorption capacity C0 (mg l1 ) teq 3 days 3 days 3 days 4h 4h 3h 4h 6h 6h 3 3 3 3 days days days days qeq (mg g1 )
Ref.
20 20 20 20 20 20 20 21 21 20 20 20 20 21 20
1a 1a 1a 4 4 221 4 250 250 1a 1a 1a 1a 250 4
1.6 0.5 16.9 0.6 0.7 2.1 0.5 5.1 4.6 2.7 0.5 13.2 11.1 2.6 2.8
[95]
Bacillus subtilis Bacillus megaterium Emericella nidulans Escherichia coli Mucor racemosus Rhizopus arrhizus Rhizopus arrhizus
[110] [102] [102] [112] [112] [95]
Sporothrix cyanescens Zooglea ramigera

a
6h 4h
[112] [110]
Equilibrium concentration.
1020
of the observed biosorptive uptake can be attributed to the cell walls of the microbial biomass. Moreover the biosorption process in the case of diazinon and lindane, involved an exothermic physical, rather than chemical, mechanism. They found that the octanol/water partition coefcient was directly related to the biosorptive uptake of these organics onto live and dead biomasses [95,96]. Ju et al. [110] investigated the biosorption of lindane, an organochlorine pesticide onto dried Gram-negative bacteria (E. coli, Zooglea ramigera) and Gram-positive bacteria (Bacillus megaterium, B. subtilis). They proposed that hydrophobic interaction and van der Waals forces are involved in the biosorption of lindane. They found that among the four bacteria, Z. ramigera showed the maximum uptake capacity [110]. Young and Banks [111] used a heat treated non viable cell suspension of the fungus R. oryzae for the removal of low concentrations of lindane from aqueous solution in a batch system. The results indicated that the mechanism of adsorption was by physical bonding of the negatively charged lindane molecule to the negatively charged fungal cell wall with hydrogen ions acting as the bridging ligand [111]. Lievremont et al. [112] reported on the removal of pentachloronitrobenzene (PCNB), a fungicide, from aqueous solution by dead fungal mycelia of Mucor racemosus, R. arrhizus, and Sporothrix cyanescens and compared with sorption on isolated cell walls of these three strains. They proposed that biosorption involved both uptake by the cell walls and by other cellular components. Size of cells, morphology and chemical composition as well as the number of the active adsorption sites and their distribution may play a signicant role in determining uptake capacity. Sorption of the adsorbate is also dependent on its molecular size and reactivity as well as mobility in the solution phase [112]. Benoit et al. [102] investigated the biosorption characteristics of herbicide, 2,4-dichlorophenoyacetic acid (2,4-D) on the freeze-dried fungal mycelium of E. nidulans, isolated from composted wheat straw. They observed a lower adsorption of 2,4-D (2.1 mg g1 at 221 mg l1 initial 2,4-D concentration) due to the negative charge due to dissociation of the carboxylic group and due to electrostatic repulsion effects at pH 6.0 [102]. Hong et al. [113] studied the biosorption of 1,2,3,4-tetrachlorodibenzo-p-dioxin (1,2,3,4-TCDD) and some polychlorinated dibenzofurans (PCDFs) pesticides by Bacillus pumilus. The results showed that dead biomass of microorganism could remove these molecules from the medium more effectively than live cells. They suggested that in addition to the attachment to microorganisms itself, extracellular polymeric substances might also be involved in the biosorption process [113]. 5.2. Pretreatment of microorganism Bell and Tsezos [95] and Tsezos and Bell [96] used the live and dead activated sludge and R. arrhizus biomasses.
They prepared both types of pretreated biomass by rstly autoclaving and then, washing and drying. They found that uptake of lindane by both live biomass types was less than the respective uptake by the same dead cells. Diazinon was biosorbed by live R. arrhizus to approximately the same level as the dead biomass. Uptake of diazinon by live activated sludge was observed to be similar to the uptake by dead sludge. For 2-chlorobiphenyl, the uptake by both live R. arrhizus and activated sludge was found higher than the uptake by the same dead cells so they concluded that it was impossible to generalize on the relative magnitude of biosorption uptake between live and nonviable biomass [95,96]. Ju et al. [110] indicated that the treatment of 1 g of wet cell of E. coli or Z. ramigera or B. megaterium or B. subtilis with 15 mM EDTA for 5 min increased the biosorption capacity of each cellthe most signicant 156% increase in biosorption of EDTA treated E. coli was observedas a result of increased permeability toward lindane [110]. Benoit et al. [102] pretreated the biomass of E. nidulans by freeze drying and autoclaving at 121 C, 103.4 kPa for 20 min by adding formaldehyde at 30 g l1 for the biosorption of 2,4-D. They found that chemical sterilization by addition of formaldehyde at 30 g l1 decreased the biosorption capacity of fungus which could be due to a competitive effect of formaldehyde for the sorption sites [102]. 5.3. Effect of pH on pesticide biosorption Ju et al. [110] investigated the effect of pH between 2.93 and 6.88 on the biosorption of lindane by E. coli, Z. ramigera, B. megaterium, and B. subtilis. They observed higher biosorption under lower pH. They found the isoelectric points of all bacteria at pH 2.0, except for E. coli whose isoelectric point is at 3.0 so all cells are negatively charged above these pH values. They proposed that the repulsive electrostatic force for the adsorption of organic halide on the cell surface decreases when a lower pH generates less negative charge on cell surfaces. As the cell and lindane molecules move closer to each other, owing to the decrease in electrostatic force, the van der Waals force is intensied and biosorption is enhanced consequently [110]. Young and Banks [111] studied at different pH values changing from 2.0 to 10.0 in order to investigate the effect of pH on the biosorption of lindane by heat treated R. oryzae and they found that biosorption was most effective at low pH [111]. 5.4. Effect of temperature on pesticide biosorption Bell and Tsezos [95] studied lindane, diazinon and malathion biosorption by both dead and live cells of activated sludge and R. arrhizus at two different temperatures (5 and 20 C) and they found that the biosorption of lindane on both type of microorganisms was exothermic and the negative value of heat of biosorption was in the range where physical adsorption rather than chemisorption was
1021
the dominant mechanism. They also found low adsorption energies for diazinon biosorption suggesting that a physical adsorption process was dominant. Diazinon biosorption by activated sludge was endothermic. Based on the large positive value of H it was probable that a chemical reaction is involved in the biosorption of malathion by both biosorbents [95]. Ju et al. [110] investigated the biosorption of lindane by E. coli, Z. ramigera, B. megaterium, and B. subtilis as a function of temperature. They found that except for E. coli, increasing temperature tended to decrease the biosorption capacity of lindane for the other three bacteria [110]. Young and Banks [111] investigated the effect of temperature on the biosorption of lindane by dried R. oryza in the range of 545 C and they found that adsorption was most effective at low temperature [111]. 5.5. Effect of initial pesticide concentration on pesticide biosorption The results obtained by Ju et al. [110] indicated that the increase in initial lindane concentration from 1 to 4 mg l1 at a constant cell concentration of 8 g l1 , increased the biosorption capacity of lindane by dried bacteria of Z. ramigera, E. coli, B. subtilis, and B. megaterium from 370 to 2800 g g1 , from 98 to 500 g g1 , from 100 to 600 g g1 , and 100 to 700 g g1 , respectively [110]. 5.6. Effect of ionic strength on pesticide biosorption Ju et al. [110] investigated the effect of initial cell concentration on the biosorption of lindane by B. megaterium at an initial lindane concentration of 4 mg l1 . The results obtained showed that lindane biosorption capacity increased from 340 to 700 mg g1 with increasing cell concentration from 2 to 16 g l1 [110]. Young and Banks [111] observed that the biosorption capacity of R. oryzae for lindane increased with increasing biomass density from 1 to 12 g l1 [111]. 5.7. Effect of ionic strength on dye biosorption Ju et al. [110] investigated the effect of ionic strength on the biosorption of lindane by B. megaterium by adding 0.1 M of NaNO3 to the aqueous lindane solution. The results obtained showed that lindane biosorption increased by increasing ionic strength. Ionic strength inuenced the biosorption by affecting the surface charge and the double-layer properties of the cells [110]. 5.8. Regeneration of biosorbent
live and dead cells of activated sludge and R. arrhizus and the adsorption of diazinon on both species of dead biomasses were completely reversible, indicating a low binding energy characteristics of physical adsorption while diazinon appeared to desorb well from live R. arrhizus but not so well from live activated sludge. In the biosorption of malathion they observed reversibility at 5 C, irreversibility at 20 C, suggesting additional uptake at higher temperature [95]. Benoit et al. [102] used 0.01 M CaCl2 to desorb 2,4-D from bound freeze-dried E. nidulans and observed an irreversible biosorption between 2,4-D and biosorbent [102]. 5.9. Equilibrium modeling Bell and Tsezos [95] applied the Freundlich model to the biosorption data of lindane, diazinon, malathion and 2-chlorobiphenyl on both activated sludge and R. arrhizus and they found that the isotherms for lindane were linear (1/n = 1). A large ultimate adsorption capacity and low energy of adsorption could account for the linear isotherm. For diazinon biosorption by R. arrhizus equilibrium data tted the Freundlich model while the isotherm for activated sludge was essentially linear [95]. Ju et al. [110] dened the lindane biosorption equilibrium by E. coli, Z. ramigera, B. megaterium and B. subtilis in terms of the Freundlich model [110]. Young and Banks [111] also applied the Freundlich model successfully to the biosorption data of lindane on R. oryzae[111]. Lievremont et al. [112] also described the biosorption of PCNB on to dead fungal mycelia of M. racemosus, R. arrhizus, and S. cyanescens by the Freundlich model [112]. Benoit et al. [102] described the equilibrium data of 2,4-D by the pretreated E. nidulans by Freundlich model [102]. 5.10. Biosorption kinetics Ju et al. [110] observed that biosorption of lindane by E. coli, Z. ramigera, B. megaterium and B. subtilis at rst was relatively rapid and slowed down later, reaching equilibrium within 4 h [110]. Lievremont et al. [112] found a contact time of 6 h was sufcient enough to attain equilibrium for the biosorption of PCNB on to dead fungal mycelia of M. racemosus, R. arrhizus, and S. cyanescens [112]. The results obtained by Benoit et al. [102] indicated that a fast equilibrium between 2,4-D in solution and 2,4-D sorbed on pretreated E. nidulans was occurred within the rst three hours of contact [102].
6. Discussion Bell and Tsezos [95] studied the desorption of lindane, diazinon and malathion from bound live and dead cells of activated sludge and R. arrhizus using distilled deionized water. They demonstrated that the adsorption of lindane on both The usage of inactive microorganisms for the removal of organics including dyes, phenolics and pesticides from wastewaters and the parameters affecting the biosorption
1022
rate and capacity has been reviewed in detail in this paper. Use of untreated (live) or treated (chemical or heat treated) microorganisms as biological adsorbents has attracted attention during recent years because of fastness, low cost, easy availability, easy operating conditions, high efciency in detoxifying very dilute or concentrated efuents and no nutrient requirements and thus have been proposed to clean a variety of industrial efuents containing organic pollutants. Bacterial, fungal, and yeast strains are shown to be the main microorganism types capable of removing organics from wastewater. But the literature survey indicated that biosorption studies of organics are very limited and only sorption of selected toxic organics onto a few types of bacterial, fungal and yeast biomass have been investigated. There is a need to study with other organic pollutants and to develop new strains which can be provided easily as waste and/or abundant biomass or can grow in simple, inexpensive medium and have high production rate and possess high biosorption capacity. The research indicated that there are various factors inuencing biosorption rate and capacity related to structure of organic molecule, microorganism type, and wastewater characteristics. Dye, phenolic, and pesticide molecules have many different and complicated structures and biosorption is affected considerably by the molecular size, charge, solubility, hydrophobicity, and reactivity of organic molecule. Another factor affecting the biosorption is the mobility of sorbate molecule in the solution phase and the hydrodynamics of contact between the solution and particle phase. Further research is needed to establish the relationships between the structure of organic molecule and microbial biosorption. The type of biomass has also a signicant effect on the observed biosorptive uptake. Biosorption of organic pollutants is found strain specic, and the behaviour and mechanisms of biosorption of different sorbate/biomass systems are not well understood. It was proposed that the size of cells, morphology as well as the number of the active adsorption sites and their distribution related to surface chemistry may play a signicant role in determining uptake capacity. The lack of understanding of the mechanism of organic sorption process hinders the satisfactory estimation of process performance and limitations, and thus the widespread application of biosorption. Further investigation is needed to identify the mechanism of organic uptake by biomass. The feasibility and efciency of a biosorption process depends not only on the properties of the sorbate and biosorbent, but also on the composition of wastewater and environmental conditions. pH, temperature, concentrations of biomass and organic pollutant, ionic strength, other components in wastewater such as metal ions, are one or more selected parameters investigated in each study presented in the literature as the characteristics of wastewater affecting biosorption capacity. Further study is needed to determine the effects of parameters which are not investigated before and other parameters such as particle size, stirring rate on the biosorption capacity. Despite the fact that industrial efuents contain several
pollutants simultaneously, little attention has been given to sorption of organics from mixture. More information on biosorption is required to determine the best combination of organics, biomass types and environmental conditions. Some investigators observed that the uptake of organic pollutants by dead microbial biomass is greater than or equal to the uptake by the same living microorganisms due to the absence of metabolic protection against transport of pollutants into the cell, increased permeability of the dead cell membrane and the change of the surface adsorptive properties of the microbial cell following its death. However a generalization concerning the relative magnitude of biosorptive uptake between live and dead biomass could not be made. For molecules which are not readily biodegradable, the overall uptake by live biomass appears to be less than that of the same dead biomass. For more readily degradable molecules or for strongly adsorbing molecules, the reverse appears to be true. Additional work on this subject is needed. Research indicated that some pretreatment methods including heat-killing, contacting with organic chemicals, such as formaldehyde, detergent, or inorganic chemicals, such as NaOH, HCl, HNO3 , H2 SO4 , NaHCO3 , and CaCl2 for killing cells before nal drying and granulation effectively increased the biosorption capacity of biomass for organic pollutants in many cases. Additional research is required to improve the biosorptive capacity of many of these sorbents. To make the biosorption process more economical it is necessary to regenerate the spent adsorbent for reusing in multiple sorption cycles. Numerous methods are reported in the literature for the elution and regeneration of organic pollutant loaded biomass by some organic solvents, surfactants and NaOH solution. Adsorptiondesorption studies indicated that yield was changed due to reversibility of biosorption. A more detailed study on regeneration methods of spent biosorbents, desorption equilibrium and kinetics is needed. Biosorption is also a well known equilibrium separation process for wastewater treatment containing organics. Equilibrium data, commonly known as adsorption isotherms, are basic requirements for the design of adsorption systems and provide information on the capacity of the biosorbent or the amount required to remove a unit mass of pollutant under the system conditions. Langmuir, Freundlich, LangmuirFreundlich, RedlichPeterson, BrunauerEmmetTeller, RadkePrausnitz models are commonly used for describing the biosorption equilibrium of organics at a constant temperature. Measured values of model constants indicated signicant differences in the curve shapes and sorption capacities regarding microorganism and organic pollutant. Frequently there is more than one pollutant in wastewaters and, in this case, the equilibrium modelling of multi-component biosorption have to be considered for the real design of biosorption processes. Only a few studies regarding binary biosorption and equilibrium modeling of binary biosorption of organics are available in the literature. Further work should be carried out to better
1023
characterize the performance of the biosorbents, studying not only organics but also removal of other pollutants from solution and, moreover, carrying out multi-component adsorption tests in order to study adsorption under competition. Further study is also needed to develop equilibrium models to predict the behaviour of each component in a mixture. Kinetics studies give detailed information on sorbate uptake rates and rate controlling steps such as external mass transfer, intraparticle mass transfer, biosorption process. So the structure and particle size of biosorbent are the most important parameters affecting biosorption rate. Although biosorption equilibrium has been dened extensively, however, only limited information is available regarding the adsorption rate and kinetics of organic removal processes. The literature on kinetic modelling is also rather limited and only a few studies applying the rst and second order kinetic models to their biosorption data were reported. Moreover, no information is provided on the effect that diffusion of organics into sorbent may have on the rate or nature of sorption. Further investigation is needed to develop predictive models for the biosorption process kinetics playing an important role in transferring technologies from the laboratory to a full-scale application. For the industrial application of biosorption, immobilization of biosorbent is necessary for solid/liquid separation. Immobilized biomass beads can then be packed in sorption column, which is perhaps the most effective device for continuous operations. For the optimization of a biosorption process in a packed bed column, the effect of different operating conditions such as ow rate, initial pollutant concentration, particle size, etc. on the biosorption capacity should be studied and cheap and feasible immobilizing agents should be investigated. Mathematical models which are the functions of sorption equilibrium, mass transfer and uid-ow parameters are helpful to determine the overall sorption performance and the shape of the column breakthrough curve. The literature indicated that only limited information is available on packed bed applications and modeling of biosorption of organic pollutants and only a few studies were reported. Further study is needed to nd out parameters for describing and predicting performance of dynamic sorption systems and reactor design. For the removal of organics, fungi, yeast and bacteria are represented the efcient classes of biosorbents relative to other biomass types. Although the biosorptive capacity and the time needed to reach the equilibrium have differed from one to another combination of microorganism-organic pollutant, the studies indicated that biomass had a much more higher biosorption capacity for dyes than that of phenolics and pesticides. Research indicated that pH of biosorption medium is the most important parameter inuencing the biosorption capacity. Biosorption of anionic (reactive and acidic) dyes by bacterial and fungal cells was signicant particularly under acidic conditions while cationic (basic) dye biosorption was accomplished at pH values higher than 3.0. For the biosorption of phenolics and pesticides the pH
value for the highest biosorption was varied between acidic pH values. Unfortunately, the effect of pH on the biosorption capacity is not always given in the literature. It should not be forgotten that the neglect of a possible pH effect may lead to serious deviation of experimental results. In general the absorbed amount of organics per biomass quantity increased with increasing initial sorbate concentration and decreased with increasing biomass concentration. The investigators found that the uptake capacity is less than that of activated carbon, but it is high enough to provide signicant removal of trace quantities of toxic compounds combined with domestic and industrial pollutants. Microbial adsorption is a promising alternative to replace or supplement present treatment processes for the removal of very high concentrations of dyes and very low concentrations of phenolics and pesticides from the wastewater. The use of equilibrium and kinetic biosorptive data in association with plant operating parameters is useful in improving the understanding of the concentration proles of hazardous pollutants in the nal efuent and should be included in modeling attempts. However, using fungal, yeast and bacterial biomass to remove organic pollutants in a wastewater is still in the research stage. More studies are needed to develop a practical application.
References
[1] Clarke EA, Anliker R. Organic dyes and pigments. In: Handbook of environmental chemistry, anthropogenic compounds, vol. 3, part A. New York: Springer-Verlag, 1980. p. 181215. [2] Zollinger H. Azo dyes and pigments. Colour chemistry-synthesis, properties and applications of organic dyes and pigments. New York: VCH, 1987. p. 92100. [3] Mishra G, Tripathy M. A critical review of the treatment for decolourization of textile efuent. Colourage 1993;40:358. [4] Banat IM, Nigam P, Singh D, Marchant R. Microbial decolourization of textile-dye containing efuents: a review. Bioresour Technol 1996;58:21727. [5] Fu Y, Viraraghavan T. Fungal decolourization of wastewaters: a review. Bioresour Technol 2001;79:25162. [6] Robinson T, Mcmullan G, Marchant R, Nigam P. Remediation of dyes in textile efuent: a critical review on current treatment technologies with a proposed alternative. Bioresour Technol 2001;77:24755. [7] Hu TL. Sorption of reactive dyes by Aeromonas biomass. Water Sci Technol 1992;26:35766. [8] Juang R-S, Tseng R-L, Wu F-C, Lee S-H. Adsorption behaviour of reactive dyes from aqueous solutions on chitosan. J Chem Technol Biotechnol 1997;70:3919. [9] Karcher S, Kornmuller A, Jekel M. Removal of reactive dyes by sorption/complexation with cucurbituril. Water Sci Technol 1999;40:42533. [10] Sumathi S, Manju BS. Uptake of reactive textile dyes by Aspergillus foetidus. Enzyme Microbial Technol 2000;27:34752. [11] Aksu Z, Tezer S. Equilibrium and kinetic modelling of biosorption of Remazol Black B by R. arrhizus in a batch system: effect of temperature. Process Biochem 2000;36:4319. [12] OMahony T, Guibal E, Tobin JM. Reactive dye biosorption by Rhizopus arrhizus biomass. Enzyme Microbial Technol 2002;31:456 63.
1024
Z. Aksu / Process Biochemistry 40 (2005) 9971026 [36] Dnmez G. Bioaccumulation of the reactive textile dyes by Candida tropicalis growing in molasses medium. Enzyme Microbial Technol 2002;30:3636. [37] Aksu Z. Reactive dye bioaccumulation by Saccharomyces cerevisiae. Process Biochem 2003;38:143744. [38] Patterson JW. Wastewater treatment technology. USA: Ann Arbor Science Pub. Inc.; 1977. [39] Aksu Z, Yener J. A comparative adsorption/biosorption study of mono-chlorinated phenols onto various sorbents. Waste Manage 2001;21:695702. [40] Calace N, Nardi E, Petronio BM, Pietroletti M. Adsorption of phenols by papermill sludges. Environ Pollut 2002;118:3159. [41] Rao JR, Viraraghavan T. Biosorption of phenol from an aqueous solution by Aspergillus niger biomass. Bioresour Technol 2002;85:16571. [42] Perrich JR. Activated carbon adsorption for waste water treatment. USA, Florida: CRS Press; 1981. [43] Kennedy KJ, Lu J, Mohn WW. Biosorption of chlorophenols to anaerobic granular sludge. Water Res 1992;26:108592. [44] Callega G, Serna J, Thirumaleswara SGB. Kinetics of adsorption of phenolic compounds from wastewater onto activated carbon. Carbon 1993;31:6917. [45] Abdo MSE, Nosier SA, El-Tawil YA, Fadi SM, El-Khairy MI. Removal of phenol from aqueous solutions by mixed adsorbents: Maghara coal and activated carbon. J Environ Sci Health 1997;A32:115969. [46] Streat M, Patrick JW, Camporro-Perez MJ. Sorption of phenol and p-chlorophenol from water using conventional and novel activated carbons. Water Sci Res 1995;29:46772. [47] Edgehill RU, Lu GQ. Adsorption characteristics of carbonized bark for phenol and pentachlorophenol. J Chem Technol Biotechnol 1998;71:2734. [48] Brasquet C, Roussy J, Subrenat E, Le Cloirec P. Adsorption and selectivity of activated carbon bers application to organics. Environ Technol 1996;17:124552. [49] Daifullah AAM, Girgis BS. Removal of some substituted phenols by activated carbon obtained from agricultural waste. Water Res 1998;32:116977. [50] Gupta VK, Sharma S, Yadav IS, Mohan D. Utilization of bagasse y ash generated in the sugar industry for the removal of phenol and p-nitrophenol from wastewater. J Chem Technol Biotechnol 1998;71:1806. [51] Chitra S, Chandrakasan G. Response of phenol degrading Pseudomonos pictorum to changing loads of phenolic compounds. J Environ Sci Health 1996;A31:599619. [52] Garcia IG, Pena PRJ, Venceslada JLB, Martin AM, Santos MAM, Gomez ER. Removal of phenol from olive mill wastewater using Phanerochaete chrysosporium, Aspergillus niger, Aspergillus terreus and Geotrichum candidum. Process Biochem 2000;35:751 8. [53] Aksu Z, Blbl G. Investigation of the combined effects of external mass transfer and biodegradation rates on phenol removal using immobilized P. putida in a packed bed column reactor. Enzyme Microbial Technol 1998;22:397403. [54] Dapaah SY, Hill GA. Biodegradation of chlorophenol mixtures by Pseudomonas putida. Biotechnol Bioeng 1992;40:13538. [55] Perez RR, Benito GG, Miranda MP. Chlorophenol degradation by Phanerochaete chrysosporium. Bioresour Technol 1997;60:207 13. [56] Schwartz HG. Adsorption of selected pesticides on activated carbon and mineral surfaces. Environ Sci Technol 1967;1:3327. [57] Thacker NP, Vaidya MV, Sipani M, Kalra A. Removal technology for pesticide contaminants in potable water. J Environ Sci Health 1997;B32:48396. [58] Gonzalez-Pradas E, Villafranca-Sanchez M, Gallege-Campo A, Urena-Amate D, Fernandez-Perez M. Removal of atrazine from
[13] Moran C, Hall ME, Howell RC. Effects of sewage treatment on textile efuent. J Soc Dyers Colour 1997;113:2724. [14] Mittal AK, Gupta SK. Biosorption of cationic dyes by dead macro fungus Fomitopsis carnea: batch studies. Water Sci Technol 1996;34:15781. [15] Chu HC, Chen KM. Reuse of activated sludge biomass: I. Removal of basic dyes from wastewater by biomass. Process Biochem 2002;37:595600. [16] Fu Y, Viraraghavan T. Removal of Congo Red from an aqueous solution by fungus Aspergillus niger. Advances Environ Res 2002;7:23947. [17] Gupta GS, Prasad G, Singh VH. Removal of chrome dye from aqueous solutions by mixed adsorbents: y ash and coal. Water Res 1990;24:4550. [18] Slokar YM, Le Marechal AM. Methods of decolouration of textile wastewaters. Dyes Pigments 1997;37:33556. [19] El-Geundi MS. Colour removal from textile efuents by adsorption techniques. Water Res 1991;25:2713. [20] McKay G, Poots JP. Kinetics and diffusion processes in colour removal from efuent using wood as an adsorbent. J Chem Technol Biotechnol 1980;30:27992. [21] Lambert SD, Graham NJD, Sollars CJ, Fowler GD. Evaluation of inorganic adsorbents for the removal of problematic textile dyes and pesticides. Water Sci Technol 1997;36:17380. [22] Low KS, Lee CK. Quaternized rice husk as sorbent for reactive dyes. Bioresour Technol 1997;61:1215. [23] Ramakrishna KR, Viraraghavan T. Dye removal using low cost adsorbents. Water Sci Technol 1997;36:18996. [24] Lee CK, Low KS, Gan PY. Removal of some organic dyes by acid-treated spent bleaching earth. Process Biochem 1999;34:451 65. [25] Morais LC, Freitas OM, Gonalves EP, Vasconcelos LT, Gonzalez Bea CG. Reactive dyes removal from wastewaters by adsorption on eucalyptus bark: variables that dene the process. Water Res 1999;33:97988. [26] Ho YS, McKay G. Comparative sorption kinetic studies of dye and aromatic compounds onto y ash. J Environ Sci Health 1999;A34:1179204. [27] Otero M, Rozada F, Calvo LF, Garcia AI, Moran A. Kinetic and equilibrium modelling of the methylene blue removal from solution by adsorbent materials produced from sewage sludge. Biochem Eng J 2003;15:5968. [28] Razo-Flores E, Luijten M, Donlon B, Lettinga G, Field J. Biodegredation of selected azo dyes under methanogenic conditions. Water Sci Technol 1997;36:6572. [29] Manu B, Chaudhari S. Anaerobic decolourization of simulated textile wastewater containing azo dyes. Bioresour Technol 2001;82:22531. [30] Glenn JK, Gold MH. Decolourization of several polymeric dyes by the lignin degrading basidiomycete, Phanerochaete chrysosporium. Appl Environ Microbiol 1983;45:17417. [31] Knapp JS, Newby PS. The decolourization of a chemical industry efuent by white rot fungi. Water Res 1999;33:5757. [32] Kapdan IK, Kargi F, McMullan G, Marchant R. Effect of environmental conditions on biological decolourization of textile dyestuff by C. versicolor. Enzyme Microbial Technol 2000;26:381 7. [33] Meehan C, Banat IM, McMullan G, Nigam P, Smyth F, Marchant R. Decolourization of Remazol Black-using a thermotolerant yeast, Kluyveromyces marxianus IMB3. Environ Int 2000;26:759. [34] Ramalho PA, Scholze H, Cardoso MH, Ramalho MT, OliveiraCampos AM. Improved conditions for the aerobic reductive decolourisation of azo dyes by Candida zeylanoides. Enzyme Microbial Technol 2002;31:84854. [35] Pearce CI, Lloyd JR, Guthrie JT. The removal of colour from textile wastewater using whole bacterial cells: a review. Dyes Pigments 2003;58:17996.
Z. Aksu / Process Biochemistry 40 (2005) 9971026 aqueous solution by natural and activated bentonite. J Environ Qual 1997;26:128891. Kouras A, Zouboulis A, Samara C, Kouimtzis T. Removal of pesticides from aqueous solutions by combined physicochemical processesthe behaviour of lindane. Environ Pollut 1998;103:193 202. Gupta VK, Jain CK, Ali I, Chandra S, Agarwal S. Removal of lindane and malathion from wastewater using bagasse y asha sugar industry waste. Water Res 2002;36:248390. Sotelo JL, Ovejero G, Delgado JA, Mart`nez I. Adsorption of lindane from water onto GAC: effect of carbon loading on kinetic behaviour. Chem Eng J 2002;87:11120. Aksu Z, Kabasakal E. Batch adsorption of 2,4-dichlorophenoxyacetic acid (2,4-D) from aqueous solution by granular activated carbon. Sep Purif Technol 2004;35:22340. Shelton DR, Khader S, Karns JS, Pogell BM. Metabolism of twelve herbicides by Streptomyces. Biodegradation 1996;7:12936. Volesky B. Detoxication of metal-bearing efuents: biosorption for the next century. Hydrometallurgy 2001;59:20316. Huang C-P, Huang C-P, Morehart AL. The removal of Cu(II) from dilute aqueous solutions by Saccharomyces cerevisiae. Water Res 1990;24:4339. Nourbakhsh M, Sag Y, Ozer D, Aksu Z, Kutsal T, aglar A. A comparative study of various biosorbents for removal of chromium(VI) ions from industrial waste waters. Process Biochem 1994;29:15. Brady JM, Tobin JM. Adsorption of metal ions by Rhizopus arrhizus biomass: characterization studies. Enzyme Microbial Technol 1994;16:6715. Kapoor A, Viraraghavan T. Fungal biosorptionan alternative treatment option for heavy metal bearing wastewaters: a review. Bioresour Technol 1995;53:195206. Veglio F, Beolchini F. Removal of metals by biosorption: a review. Hydrometallurgy 1997;44:30116. Puranik PR, Paknikar KM. Biosorption of lead and zinc from solutions using Streptoverticillium cinnamoneum waste biomass. J Biotechnol 1997;55:11324. Aksu Z. Biosorption of heavy metals by microalgae in batch and continuous systems. In: Tam NFY, Wong Y-S (Eds.). Algae for waste water treatment. Germany: Springer Verlag and Landes Bioscience; 1998. p. 3753. Yetis U, Ozcengiz G, Dilek FB, Ergen N, Erbay A, Dilek A. Heavy metal biosorption by white-rot fungi. Water Sci Technol 1998;38:32330. Dnmez G, Aksu Z, Oztrk A, Kutsal T. A comparative study on heavy metal biosorption characteristics of some algae. Process Biochem 1999;34:88592. Yu Q, Matheickal JT, Yin P, Kaewsarn P. Heavy metal uptake capacities of common marine macro algal biomass. Water Res 1999;33:15347. Wong JPK, Wong YS, Tam NFY. Nickel biosorption by two chlorella species, C. vulgaris (a commercial species) and C. miniata (a local isolate). Bioresour Technol 2000;73:1337. Say R, Denizli A, Arica MY. Biosorption of cadmium(II), lead(II) and copper(II) with the lamentous fungus Phanerochaete chrysosporium. Bioresour Technol 2001;76:6770. Zhou JL, Banks CJ. Removal of humic acid fraction by Rhizopus arrhizus: uptake and kinetic studies. Environ Technol 1991;12:859 69. Mou DG, Lim KK, Shen HP. Microbial agents for decolourization of dye wastewater. Biotechnol Adv 1991;9:61322. Banks CJ, Parkinson ME. The mechanism and application of fungal biosorption to colour removal from raw water. J Chem Technol Biotechnol 1992;54:1926. Brahimi-Horn MC, Lim KK, Liany SL, Mou DG. Binding of textile azo dyes by Mirothecium verrucaria Orange II, 10B (blue) and RS (red) azo dye uptake for textile wastewater decolourization. J Ind Microbiol 1992;10:24561.
1025
[59]
[60]
[61]
[62]
[63] [64] [65]
[66]
[67]
[68]
[69] [70]
[71]
[72]
[73]
[74]
[75]
[76]
[77]
[78] [79]
[80]
[81] Zhou W, Zimmermann W. Decolourization of industrial efuents containing reactive dyes by actinomycetes. FEMS Microbiol Lett 1993;107:15762. [82] Zhou JL, Banks CJ. Mechanism of humic acid colour removal from natural waters by fungal biomass biosorption. Chemosphere 1993;27:60720. [83] Hu T-L. Removal of reactive dyes from aqueous solution by different bacterial genera. Water Sci Technol 1996;34:8995. [84] Polman JK, Breckenridge CR. Biomass-mediated binding and recovery of textile dyes from waste efuents. Text Chem Colour 1996;28:315. [85] Gallagher KA, Healy MG, Allen SJ. Biosorption of synthetic dye and metal ions from aqueous efuents using fungal biomass. In: Wise DL. (Ed.). Global Environmental Biotechnology. UK: Elsevier; 1997. p. 2750. [86] Tatarko M, Bumpus JA. Biodegradation of Congo Red by Phanerochaete chrysosporium. Water Res 1998;32:17137. [87] Bustard M, McMullan G, McHale AP. Biosorption of textile dyes by biomass derived from Kluveromyces marxianus IMB3. Bioprocess Eng 1998;19:42730. [88] Fu Y, Virarahavan T. Removal of a dye from an aqueous solution by the fungus Aspergillus niger. Water Quality Res J Can 2000;35:95 111. [89] Fu Y, Virarahavan T. Removal of C.I. Acid Blue 29 from an aqueous solution by Aspergillus niger. AATCC Mag 2001;1:3640. [90] Fu Y, Viraraghavan T. Dye biosorption sites in Aspergillus niger. Bioresour Technol 2002;82:13945. [91] Aksu Z. Biosorption of reactive dyes by dried activated sludge: equilibrium and kinetic modelling. Biochem Eng J 2001;7:7984. [92] Chu HC, Chen KM. Reuse of activated sludge biomass: II. The rate processes for the adsorption of basic dyes on biomass. Process Biochem 2002;37:112934. [93] Aksu Z, Dnmez G. A comparative study on the biosorption characteristics of some yeasts for Remazol Blue reactive dye. Chemosphere 2003;50:107583. [94] Basibuyuk M, Forster CF. An examination of the adsorption characteristics of a basic dye (Maxilon Red BL-N) on to live activated sludge system. Process Biochem 2003;38:13116. [95] Bell JP, Tsezos M. Removal of hazardous organic pollutants by adsorption on microbial biomass. Water Sci Technol 1987;19:409 16. [96] Tsezos M, Bell JP. Comparison of the biosorption and desorption of hazardous organic pollutants by live and dead biomass. Water Res 1989;23:5618. [97] Logan BE, Alleman BC, Amy GL, Gilbertson RL. Adsorption and removal of pentachlorophenol by white rot fungi in batch culture. Water Res 1994;28:15338. [98] Jacobsen BN, Arvin E, Reinders M. Factors affecting sorption of pentachlorophenol to suspended microbial biomass. Water Res 1996;30:1320. [99] Brandt S, Zeng A-P, Deckwer W-D. Adsorption and desorption of pentachlorophenol on cells of Mycobacterium chlorophenolicum PCP-1. Biotechnol Bioeng 1997;55:4809. [100] Daughney CJ, Fein JB. Sorption of 2,4,6-trichlorophenol by Bacillus subtilis. Environ Sci Technol 1998;32:74952. [101] Aksu Z, Yener J. Investigation of the biosorption of phenol and monochlorinated phenols on the dried activated sludge. Process Biochem 1998;33:49655. [102] Benoit P, Barriuso E, Calvet R. Biosorption characterization of herbicides, 2,4-D and atrazine, and two chlorophenols on fungal mycelium. Chemosphere 1998;37:127182. [103] Jianlong W, Yi Q, Horan N, Stentiford E. Bioadsorption of pentachlorophenol (PCP) from aqueous solution by activated sludge biomass. Bioresour Technol 2000;75:15761. [104] Aksu Z, Akpinar D. Modelling of simultaneous biosorption of phenol and nickel(II) onto dried aerobic activated sludge. Sep Purif Technol 2000;21:8799.
1026
Z. Aksu / Process Biochemistry 40 (2005) 9971026 [116] Redlich OJ, Peterson DL. A useful adsorption isotherm. J Phys Chem 1959;63:1024. [117] Radke CJ, Prausnitz JM. Adsorption of organic solutions from dilute aqueous solution on activated carbon. Ind Eng Chem 1972;11:445 51. [118] Weber Jr WJ. Adsorption. In: Physicochemical processes for water quality control, New York: Wiley 1972. p. 20611. [119] Bellot JC, Condoret JS. Modelling of liquid chromatography equilibria. Process Biochem 1993;28:36576. [120] Weber WJ, Morris JC. Kinetics of adsorption on carbon from solution. J Sanit Eng Div Am Soc Civ Eng 1963;89SA2:319. [121] Lagergren S. Zur theorie der sogenannten adsorption gelster stoffe. Kungliga Svenska Vetenskapsakademiens. Handlingar 1898;24:1 39. [122] McKay G, Ho YS. Pseudo-second order model for sorption processes. Process Biochem 1999;34:45165. [123] Guibal E, Lorenzelli R, Vincent T, Le Cloirec P. Application of silica gel to metal ion sorption: Static and dynamic removal of uranyl ions. Environ Technol 1995;16:10114. [124] Bohart G, Adams EQ. Some aspects of the behaviour of charcoal with respect to chlorine. J Am Chem Soc 1920;42:52344. [125] Thomas HC. Heterogeneous ion exchange in a owing system. J Am Chem Soc 1944;66:16646. [126] Clark RM. Evaluating the cost and performance of eld-scale granular activated carbon systems. Environ Sci Technol 1987;21:57380. [127] Yoon YH, Nelson JH. Aplication of gas adsorption kinetics. I. A theoretical model for respirator cartridge service time. Am Ind Hyg Assoc J 1984;45:50916.
[105] Aksu Z, Akpinar D. Competitive biosorption of phenol and chromium(VI) from binary mixtures onto dried anaerobic activated sludge. Biochem Eng J 2001;7:18393. [106] Wang W, Zhang X, Wang D. Adsorption of p-chlorophenol by biolm components. Water Res 2002;36:55160. [107] Karim K, Gupta SK. Biosorption of nitrophenols on anaerobic granular sludge. Environ Technol 2002;23:137984. [108] Aksu Z, Gnen F. Biosorption of phenol by immobilized activated sludge in a continuous packed bed: prediction of breakthrough curves. Process Biochem 2004;39:599613. [109] Voerman S, Tammes PML. Adsorption and desorption of lindane and dieldrin by yeast. Bull Environ Contam Toxicol 1969;45:2717. [110] Ju Y-H, Chen T-C, Liu JC. A study on the biosorption of lindane. Colloids Surf B 1997;9:18796. [111] Young E, Banks CJ. The removal of lindane from aqueous solution using a fungal biosorbent: the inuence of pH, temperature, biomass concentration and culture age. Environ Technol 1998;19:619 25. [112] Livremont D, Seigle-murandi F, Benoit-guyod J-L. Removal of PCNB from aqueous solution by a fungal adsorption process. Water Res 1998;32:36016. [113] Hong H-B, Hwang S-H, Chang Y-S. Biosorption of 1,2,3,4tetrachlorodibenzo-p-dioxin and polychlorinated dibenzofurans by Bacillus pumilus. Water Res 2000;34:34953. [114] Langmuir I. The adsorption of gases on plane surfaces of glass, mica, and platinum. J Am Chem Soc 1918;40:13618. [115] Freundlich H. Adsorption in solution. Phys Chem Soc 1906;40: 13618.

Application of Ion For The Removal of Organic Pollutants

Caricato da

Informazioni sul documento

Descrizione originale:

Titolo originale

Copyright

Formati disponibili

Condividi questo documento

Condividi o incorpora il documento

Opzioni di condivisione

Hai trovato utile questo documento?

Questo contenuto è inappropriato?

Copyright:

Formati disponibili

Application of Ion For The Removal of Organic Pollutants

Caricato da

Copyright:

Formati disponibili

Process Biochemistry 40 (2005) 9971026

Application of biosorption for the removal of organic pollutants: a review

Tel.: +90-312-2977434; fax: +90-312-2992124. E-mail address: zaksu@hacettepe.edu.tr (Z. Aksu).

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

1/n +x1 z1 Ceq2

1/n +x2 z2 Ceq1

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Activated sludge Activated sludge Aeromonas sp.

[91] [94] [83]

[88] [89] [16] [16] [85] [84] [93]

Endothiella aggregata Escherichia coli

Laminaria digitata Myrothecum verrucaria

Phanerochaete chrysosporium Pichia carsonii

Rhizopus arrhizus Rhizopus arrhizus

[11] [85] [84] [93] [84] [93] [81]

Azo-reactive Red Formazan Blue Phytalocyanine Blue Tremella fuciformis

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Activated sludge Activated sludge Anaerobic sludge Anaerobic granular sludge

[103] [104] [105] [43]

Anaerobic granular sludge

[41] [102] [106] [99] [95] [40]

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

1a 1a 1a 4 4 221 4 250 250 1a 1a 1a 1a 250 4

[110] [102] [102] [112] [112] [95]

Sporothrix cyanescens Zooglea ramigera

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

Z. Aksu / Process Biochemistry 40 (2005) 9971026

[63] [64] [65]

Potrebbero piacerti anche