Int. J. Miner. Process. 62 2001. 111120 www.elsevier.

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Biosorption of metals onto plant biomass: exchange adsorption or surface precipitation?

Ivo A.H. Schneider a , Jorge Rubio b, Ross W. Smith c, )
a Ciil Engineering Department, Uniersity of Paso Fundo, Paso Fundo RS, Brazil Department of Mining Engineering r PPGEMM, Federal Uniersity of Rio Grande do Sul, Porto Alegre RS, Brazil Department of Chemical and Metallurgical Engineering, Uniersity of Neada-Reno, Reno, NV 89557 USA b

Received 15 August 1999; accepted 17 July 2000

Abstract Heavy metal ions readily adsorb onto the nonliving biomass of many aquaphytes. Further, in many cases the metal ions can be readily desorbed from the biomass by use of a suitable eluting agent. It has been shown in certain cases, at least, that the biomass can be subjected to a number of loading and elution cycles without the biomass losing its adsorption capacity. It has been widely reported that the adsorption is through a specific ion exchange mechanism and a number of researchers have shown experimental evidence supporting such a mechanism. However, there is also evidence that the adsorption is through simple surface precipitation of metal hydroxide species. The present study examines some of the existing data on adsorption of metal ions onto aquaphyte biomass and attempts to evaluate which mechanism is the more likely. q 2001 Elsevier Science B.V. All rights reserved.
Keywords: aquaphyte; adsorption; precipitation; heavy metals

1. Introduction Heavy metal ions sorb onto many solid surfaces including the surfaces of living and dead microorganisms and higher plants. A characteristic of the sorption of heavy metal ions onto surfaces, both biotic and abiotic surfaces, is that at a set bulk solution heavy metal concentration the sorption is greatest at a pH value that is just slightly more acidic
Corresponding author. Fax: q 1-775-327-5059. E-mail addresses: ivoandre@fear.upf.br I.A.H. Schneider., jrubio@vortex.ufrgs.br J. Rubio., smithrw@scs.unr.edu R.W. Smith.. 0301-7516r01r$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 1 - 7 5 1 6 0 0 . 0 0 0 4 7 - 8
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than the pH at which there is bulk precipitation of the metal hydroxide. As pH is further raised, once the bulk solubility limit is reached, the sorption is greatly reduced because the metal ion is removed from solution by the bulk precipitation. It has long been reported that the sorption of heavy metal ions onto algae, bacteria and higher plants is through a specific ion exchange mechanism. The sorption is thought to involve the replacement of protons, alkali, alkaline earth, or other cations by the heavy metal ions. Evidence presented by various researchers includes evidence that for each heavy metal ion sorbing an equivalent of protons andror other metal ions appear in solution Crist et al., 1991: Schneider et al., 1999.. Further evidence is the fit, or approximate fit, of the sorption data obtained to the Langmuir isotherm Wang, 1995; Schneider, 1995; Wang et al., 1998, Schneider et al., 1999.. The former is apparent direct evidence that a replacement phenomenon is taking place. The Langmuir fit is considered to be evidence that sorption stops at one monolayer, consistent with specific and strong sorption onto specific sites. Because the exchange reaction between surface sites and previously adsorbed ions is of only a monolayer or less, there is an accumulation of matter at the solidsolution interface without the creation of a three-dimensional structure. Thus, the phenomenon is adsorption. Evidence against such a mechanism is the often reported very low sorption activation energy, which is not consistent with strong sorption onto specific sites, the extreme rapidity with which the sorption takes place and the very rapid and easy and rapid desorption Schneider, 1995; Wang et al., 1998, Schneider et al., 1999.. In addition, it can often be observed that sorption of heavy metal ions onto biomass is partly in patches Golab et al., 1991; Golab and Smith, 1992; Bauer, 1999.. An alternate sorption mechanism is the surface precipitation or condensation of heavy metal hydroxides onto the biosurfaces. Such precipitation is possible if there is an accumulation of the heavy metals within the diffuse part of the electrical double layer. The accumulation will take place if there is a net negative charge on the solid surface. Thus, although the concentration of the metal ion in solution may be much less than the solubility limit with respect to metal hydroxide and oxide solids, the solubility limit near the solid surfaces is exceeded and precipitation onto the solid surface takes place. The concentration of heavy metal ions within the electrical double layer can be roughly calculated by use of the Boltzmann equation Gaudin and Fuerstenau, 1955.: Ci surf . s Ci bulk . exp yzFfdrRT .

1.

where Ci surf. s concentration of species i at the surface; Ci bulk. s concentration of species i in the bulk of the solution; z s formal charge on the cation; F s Faraday constant; fd s potential at the Stern plane; R s gas constant; T s absolute temperature. In the present paper an attempt is made to evaluate the magnitude of the effect of the concentration of CuII. within the electrical double layer and determine if the concentration is sufficient to account for the sorption of CuII. onto a macrophyte. 2. Results and discussion Fig. 1 shows a log concentration diagram, adapted from Baes and Mesmer 1986. for Cu II. in equilibrium with solid CuOH. 2 . It can be seen at pH values more acidic than

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Fig. 1. Logarithm concentration diagram for CuII. in equilibrium with solid CuOH. 2 .

pH 7 that the solubility increases rapidly with decrease in pH and that the solubility is about 10y3 .36 molrL at pH 6.0. If a 1.0 = 10y 4 molrl CuII. solution is considered, the bulk solubility limit is reached at about pH 6.3 Fig. 2 from Schneider 1995., based on data of Baes and Mesmer 1986., shows CuII. species distribution for a total CuII. concentration of 1 = 10y4 molrL. Fig. 3 from Schneider et al. 1995. shows the sorption of CuII. onto Potomogenten luscens as a function of pH. The curves of this figure should be compared to the curves of Figs. 1 and 2. It is noted that maximum sorption of CuII. occurs at a pH value slightly more acidic than the pH of bulk precipitation of CuOH. 2 .

Fig. 2. Relative concentration of CuII. species in a system containing 1=10y4 molrl CuII.; from Schneider 1995..

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Fig. 3. Final concentration of CuII. in solution as a function of pH; total CuII. in the system s 1=10y4 molrl CuII.; from Schneider 1995..

Fig. 4 from Schneider 1995. shows the zeta potential z . of P. luscens as a function of pH. Using z data from this figure and substituting z for fd in the Boltzmann equation, it is possible to approximately solve the Boltzmann for the concentration of CuII. within the electrical double for the biomass at different pH values. The substitution is necessary since fd is an inner potential and is not measurable while z is an outer, measurable, potential. In the calculation, it should be kept in mind that at all pH values more basic than the isoelectric point of the plant biomass, fd will be more negative than z and, thus, the calculation will always underestimate the concentration of CuII. within the electrical double layer. It can be noted from Fig. 1 that the pH value of bulk solution precipitation of CuOH. 2 for a CuII. solution containing 1.0 = 10y4 molrl CuII. is at about pH 6.3. This means that at pH values more basic than this pH, there will be a precipitate of CuOH. 2 present in the system. From Fig. 4 it is seen that the zeta potential values for

Fig. 4. Zeta potential of P. luscens as a function of pH; 1=10y3 molrl NaNO 3 added for ionic strength control; from Schneider 1995..

I.A.H. Schneider et al. r Int. J. Miner. Process. 62 (2001) 111120 Table 1 Concentration of CuII. within the electrical double layer at selected pH values pH Concentration of CuII. within double layer molrl; total bulk concentration CuII. s 1=10y4 molrl. 10y 1.87 10y1 .38 10y1 .03 10y0 .86 bulk solubility limit reached. 10y1 .4 bulk solubility limit exceeded. Maximum concentration of soluble CuII. in equilibrium with solid CuOH. 2 molrl. 10 0.64 10y 1.36 10y 3.36 10y 4 10y 5.36

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4.0 5.0 6.0 6.3 7.0

the P. luscens biomass at pH 4, 5, 6 and 7 are approximately y60, y75, y85 and y100 mV, respectively. For a total bulk CuII. concentration of 1.0 = 10y4 molrl and using the Boltzmann equation the concentrations of CuII. within the diffuse part of the double layer can be roughly calculated. Table 1 shows the amount of CuII. in the electrical double layer as a function of pH. Thus, it can be seen that at all pH values more acidic than pH 6.3, the solubility limit of CuII. is exceeded and there should be precipitation of CuOH. 2 within the double layer. Assuming different values for the total concentration of CuII. in a system, the pH value at which the double layer concentration of CuII. approximately equals the solubility limit in the bulk solution can be determined for these total concentrations of CuII.. This data is presented in Table 2 for CuII. concentrations from 1 = 10y8 to 1 = 10y 4 molrl. Recent work by Schneider 1995. shows that the sorption of CuII., NiII., and ZnII. onto P. luscens, Salinia herzogii , and Eichhornia crassipes can be fitted to a Langmuir isotherm. Furthermore, the sorption of these ions appears to involve an ion exchange mechanism whereby either the ions exchange with protons or with other cations in equivalent amounts Wang, 1995; Wang et al., 1997; Schneider et al., 1999.. It was deduced that the surface group responsible for the exchange was primarily the carboxylate group. In addition, this work confirmed previous work that the isoelectric point iep. of all three macrophytes is at about pH 2.0. The p K a of the carboxylate groups in fatty acids is at pH 4.7, but there is evidence that it is at a more acidic value in

Table 2 The pH value at which the concentration of CuII.aq. species within the double layer equals the maximum concentration of CuII.aq. species in the bulk solution as a function of total CuII. in the system Total concentration of CuII. in system molrl. The pH at which the concentration of CuII.aq. within the double layer equals the maximum concentration in the bulk of the solution 5.0 5.4 5.8 6.3 6.8

1=10y4 1=10y5 1=10y6 1=10y7 1=10y8

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other structures Smith, 1989.. From the iep data, assuming that there is no inherent space charge in the macrophytes, it appears that the p K a of the macrophytes is near pH 2.0. Thus, since the number of positive and negative sites on the macrophytes are equal at the iep, the carboxylate groups must be primarily ionized at pH values only slightly more basic than pH 2. In the absence of foreign cations, hydrogen ions, thus, at pH values more basic than the iep must be primarily located in the diffuse part of the double layer. Any exchange by introduced cations must be with double layer protons and the observed experimental exchange is primarily due to coulombic interaction between the cations and the charged surface. Schneider 1995. observed that, although there was some loss of CuII. sorptive capacity of a P. luscens biomass after several loading and elution cycles using a O.5% solution of HCl as eluant, the sorptive capacity remained essentially unchanged for up to 100 loading and elution cycles. However, after subjecting the plant biomass to 50 cycles, analysis of the biomass indicated that there remained a substantial amount of CuII. on the biomass. The data are shown in Table 3. This CuII. was only partially removed with 5% HCl treatment. Thus, there must be both CuII. adsorption onto specific sites and non-specific, reversible, sorption through coulombic interaction between the CuII. ions and the negative biomass surface. Electrostatic models for exchange reactions at humicwater interfaces Hummel, 1997., at hydrous ferric hydroxide surfaces Dzombak and Morel, 1990., and at geological solids surfaces Banwart, 1997. have been suggested. In such cases, the model may include surface precipitation. The model for surface precipitation generally includes an initial, rapid, adsorption mechanism followed by a slower surface precipitation. Thus, there is adsorption on the surface with a surface precipitation layer covering the adsorbed layer. A rough sketch of the conceptual model is shown in Fig. 5 based on figures from Banwart 1997. and Dzombak and Morel 1990.. In addition to the various models, there is considerable question about the true surface areas of dried plant biomass and soil organic matter SOM. since various surface areas can be measured depending on measurement technique and there is the possibility of the materials swelling upon reaction with water. Table 4 shows some measured values of selected materials. Immediately evident from the table is that BET surface area measurements using N2 determined at 77 K, the vaporization temperature of N2 , are much less than those

Table 3 Amount of CuII. remaining in the biomass after 50 loading and elution cycles and after a final elution cycle with both 0.5% and 5% HCl solutions Cu concentration natural dead biomass before sorption and elution cycles mg Curkg biomass. Cu concentration biomass after 50 cycles of loading and elution using 0.5% HCl solution as eluant Cu concentration biomass after 50 cycles of loading and elution using 0.5% HCl solution as eluant followed by a cycle using 5% HCl as eluant 187 129

E. cressipes P. lucens

46 19

384 327

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Fig. 5. Representation of the model from Dzombak and Morel 1990. representing the relative contribution of adsorption and surface precipitation to metal sorption.

determined using other methods. These much larger surface areas of materials such as soil organic matter SOM. as measured by ethylene glycol EG. or ethylene glycol

Table 4 Selected values for the specific surface areas of porous solids measured by different techniques Adsorbent E. crassipes roots. E. crassipes roots. E. crassipes roots. E. crassipes aerial parts. E. crassipes roots. E. crassipes aerial parts. Salinia sp. Salinia sp. P. lucens Soil organic matter SOM. SOM SOM Pretreatment Adsorbate N2 0.1 M H 2 SO4 N2 Temperature Surface area Reference K. M 2 rg. 77 77 7.4 6. 7 ) 150 Wang 1995. Wang 1995. Schneider et al. 1995.

N2 slow drift 77 toward equilibrium. N2 slow drift 77 toward equilibrium. Methylene blue ; 298 Methylene blue ; 298 Methylene blue Hydrophobic Methylene blue surface removed Methylene blue N2 CO 2 ; 298 ; 298 ; 298 77 273

; 280

This study

243 223 274 278 415 0.891.1 94174 560800

Schneider et al. 1995. Schneider et al. 1995. Schneider 1995. Ribeiro et al. 1998. Schneider 1995. De Jonge and MittlemeijerHazeleger 1996. De Jonge and MittlemeijerHazeleger 1996. Bower and Gschwend 1952.

Ethylene glycol 298"2

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monethyl ether EGME. uptake Heilman et al., 1965., compared to areas measured by the BET method, has led to the suggestion that the larger surface areas are not real. For example, Chiou et al. 1990, 1992. have argued that to consider that surface areas measured by fluids such as EG or EGME onto SOM would require the existence of an Ainner surfaceB that is accessible to these fluids but somehow excludes smaller molecules such as N2 . Their suggested alternate mechanisms involve the expansion of the clays or SOM by the fluids creating new surface and, importantly, the solubility of the AadsorbateB in the AadsorbentB. Pennell and Rao 1992. take strong exception to this interpretation of EG and EGME sorption and propose that SOM, for example, behaves as a three dimensional system in a semi-structural framework. Further, they note the very high ion exchange capacity for SOM is not consistent with the model of Chiou et al. 1990.. Although De Jonge and Mittlemeijer-Hazeleger 1996. believe that EG and EGME give unrealistically high values for the surface areas of SOM, BET surface areas using N2 at 77 K give values that only represent an Aexternal surfaceB and exclude micropores and inner surfaces. As evidence, their work measuring the surface areas of SOMs showed that N2 adsorption at 77 K gave values between 0.89 and 4.94 m2rg and that CO 2 adsorption at 273 K gave values between 94 and 174 m2rg. Furthermore, the work of Rodriguez-Reinoso et al. 1982, 1984. indicates that CO 2 adsorption at 195 and 273 K and N2 adsorption at 90 K yield much greater surface areas of activated carbons than N2 adsorption at 77 K. However, a slow drift was noted in the latter system. Then, if the system was allowed to drift for 6 weeks, apparent equilibrium was reached and the surface area values were comparable to those measured by CO 2 adsorption and N2 adsorption at 90 K. The conclusion De Jonge and Mittlemeijer-Hazeleger, 1996. is that N2 adsorption at 77 K will not measure pores with restrictions less than 0.5 nm unless long adsorption times weeks. are considered. Since the surface area of SOMs estimated by microscopic examination is about 0.05 m2rg, they also believe that the surface areas measured by fast N2 adsorption at 77 K includes pores between 0.5 and 2 nm where capillary condensation can take place.. Schneider et al. 1995. attempted to measure the surface area of various parts of E. crassipes. It was found that it initially appeared that the surface areas were between 2 and 5 m2rg. However, a slow drift was noted in the systems and after several days measured areas between 150 and 280 m2rg. It was still not certain that equilibrium had been reached. Ruthven and Kaul 1993. have suggested that in such systems the rate of diffusion into pores of porous solids is governed primarily by the rotational freedom of the diffusing molecule rather than the energy barrier associated with the penetration of pore restrictions. Thus, metal ions can either be present on the surface of the biomass or can go into expanded pores. In this latter case, the metal ions should be difficult to desorb. Furthermore, regardless of mechanisms involved, displacement of protons from the anchored layer and diffuse layer by metal cations will take place. In addition, the replacement of one species of metal ion by another species should take place both at and near the biomass surface. Although the data can usually be fitted to a Langmuir isotherm, careful inspection of the data often shows some evidence, at low equilibrium concentrations of the metal ion, of a stronger sorption mechanism also taking place Schneider et al. 1995; Wang, 1995.. For HgII. sorption onto P. natans biomass electron microscopy evidence shows that, although HgII. was present over the entire

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biomass surface, there were patches where definite multilayer sorption occurred Bauer, 1999.. Also, in the case of sorption of PbII. onto algae and bacteria dead biomass Golab et al., 1991; Golab and Smith, 1992., there is physical evidence from electron microscopic examination of the microorganisms that the PbII. has sorbed in discrete patches onto the biomass. This suggests that not only is the sorption at least in part a precipitation phenomenon, but also that there may be reactive sites or patches on the biomass surface. A similar sorption was observed with uranyl sorption onto a Streptomyces sp., although the evidence is not quite as convincing as with PbII.. In attempting to distinguish between adsorption and surface precipitation in the accumulation of metal ions onto solid surfaces, Sposito 1986. deduced that it is not possible to differentiate between the two phenomena based solely on sorption data. Rather, determination of the mechanism must be achieved through close spectroscopic determination of the molecular structure of the sorbed layer. Considering the data and analysis presented in this paper, it is suggested that both mechanisms can be thought of as taking place in sorption of heavy metal ions such as CuII. onto plant biomass surfaces.

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