Impact of Ionic Strength on Cd(II) Partitioning between Alginate Gel

Jan 14, 2009 - Wageningen University. , ‡. University of Montreal. , §. University of Southern Denmark. Cite this:Environ. Sci. Technol. 2009, 43, ...
0 downloads 0 Views 196KB Size
Download PDF
Environ. Sci. Technol. 2009, 43, 1091–1096

Impact of Ionic Strength on Cd(II) Partitioning between Alginate Gel and Aqueous Media E R W I N J . J . K A L I S , * ,† THOMAS A. DAVIS,‡ RAEWYN M. TOWN,§ AND HERMAN P. VAN LEEUWEN† Laboratory of Physical Chemistry and Colloid Science, Wageningen University, The Netherlands, Department of Chemistry, University of Montreal, Canada, and Institute for Physics and Chemistry, University of Southern Denmark, Denmark

Received August 18, 2008. Revised manuscript received November 28, 2008. Accepted November 29, 2008.

Alginate gel is representative of polysaccharide-based components of cell walls which contain a large number of negatively charged functional groups. The structural charge gives rise to a Donnan potential in the gel, which impacts significantly on the partitioning of ions between the aqueous medium and the gel. We measured the Donnan potential and partitioning of Cd2+ in alginate gel as a function of ionic strength in the range 1-100 mM. The Cd2+ partition coefficient between gel and medium, as measured by in situ microelectrode voltammetry, reaches values between 10 and 100 in the 0.1-1 mM ionic strength range, and agrees well with Donnan partition calculations based on the charge density of the gels. The total Cd(II) concentration in the gel correlates approximately linearly with the free [Cd2+]gel. The results imply that metal ion activities in the biopolymer gel phase may generally differ drastically from those in the bulk medium to an extent that strongly depends on ionic strength. This feature must be taken into account in estimations of exposure conditions for predictions of bioavailability.

Introduction It is widely accepted that total metal ion concentrations are not good indicators for metal availability in natural waters (1). Rather, metal uptake by organisms such as algae and plants has been correlated with free (2) or labile (3) metal concentrations in the bulk medium. To date, minimal attention has been paid to the local metal speciation at the biointerface, i.e. in the cell wall, or within closely associated capsular or exocellular material. Charged groups of the biointerface can lead to a significantly higher free metal ion activity near the uptake sites of an organism than that in bulk solution. The cell walls of brown algae, for example, possess substantial metal binding capacity via complexing sites in alginates and fucoidans (4, 5). In particular, the alginates produced by Sargassum display a remarkably high affinity for metal cations such as Cd which is ascribed to the macromolecular conformation of their guluronic acid-rich alginate chains that are able to selectively bind divalent * Corresponding author e-mail: [email protected]. † Wageningen University. ‡ University of Montreal. § University of Southern Denmark. 10.1021/es802305n CCC: $40.75

Published on Web 01/14/2009

 2009 American Chemical Society

cations (6, 7). Alginates comprise a family of polysaccharides containing 1,4-linked β-D-mannuronic (M) and R-L-guluronic (G) acid residues arranged in a block-wise, nonregular order along the chain. This block-wise arrangement of M and G residues determines both the cation specific affinity of the alginate gel as well as its fundamental physicochemical and rheological properties (8, 9). Alignment of two homopolymeric guluronic chains forms an array of coordination sites which can easily accommodate calcium and other divalent cations. This mode of binding cations is known as the “egg-box model” (10). Polysaccharides such as alginates contain a large number of negatively charged functional groups, mainly carboxylates. They form gels due to both specific and physicochemical binding of adjacent chain sequences, often as a result of cation cross-linking. Typically, this cross-linking (e.g., Ca2+ for alginates) does not lead to complete charge compensation. The result is a net negative charge within the biogel, usually quantified by its charge density, which gives rise to a Donnan potential with respect to the medium. As a consequence, the gel/medium system exhibits charge-specific ion partitioning which strongly depends on the ionic strength of the bulk solution. Thus, for a given constant bulk solution concentration, the cation concentration is enhanced in the biological gel phase (hereafter denoted as “biogel”) to an extent that varies with the ionic strength, which in turn may largely influence the biouptake of cations. The adsorption and uptake of metals by organisms is often ionic strength dependent, e.g., Cu adsorption by dried algal material (11) and Pb adsorption by living algae (12). Ca-alginate gels have previously been chosen (13) as a model biogel system for cell walls and biofilms. A large body of literature and basic knowledge is available for these polysaccharides and their charge. In addition to variation of the Donnan potential, there are specific structural changes within the gel that occur as a function of ionic strength. Both the gel conductivity and the swelling factor, which is defined as the ratio between the mass of the gel in equilibrium with a reference electrolyte solution and the mass of the gel after preparation, increase with decreasing ionic strength (14). The change in gel structure results from a more compressed configuration of the polymer network at high ionic strength. Conversely, at low ionic strength the increased osmotic pressure in the water phase within the gel forces the crosslinked network of polymer chains to swell (15). In this work we investigate the effects of ionic strength on the Donnan potential and resulting Donnan partitioning of metal cations between model alginate gels and aqueous electrolyte. In doing so, we develop an independent estimation of the charge density via analysis of Ca and Cd binding data over a wide range of ionic strengths. In support of this effort we have characterized the limits of gel stability as a function of ionic strength in solutions devoid of the network forming calcium cation. Donnan partitioning of Cd between solution and gel phase is related to the specifically bound Cd, which also varies as a function of ionic strength. We address the implications of our Cd(II) biogel speciation data for predictions of bioavailability based on equilibrium models such as the free ionic activity (FIAM (1)) and the biotic ligand model (BLM (16)).

Material and Methods Alginate Gels. The internal gelation method of Draget et al. (17) was employed to prepare homogeneous Ca-alginate gels. To make the gels, 1% Na-alginate solutions were prepared from Na-alginate and Milli-Q water and left stirring overVOL. 43, NO. 4, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

9

1091

night. The Na-alginate was from Sigma (A-2033, lot 128F0050). Additional details on its NMR structural characterization are given in ref 13. CaCO3 (Sigma Aldrich) was added to give a final concentration of 15 mM. This concentration of Ca is considered to be the initially bound Ca content of the gel which varies with the Ca and Na concentrations in the equilibrating solution only as a result of mass changes as a function of ionic strength, as demonstrated in Figure S1 in the Supporting Information. After the mixing with CaCO3, the viscous Na-alginate suspension was degassed. As a final step, slowly hydrolyzing D-glucono-δ-lactone (GDL; Sigma) was added to give a final concentration of 30 mM which permits the controlled release of H+ and subsequent liberation of calcium ions from CaCO3 to the suspension. The viscous suspension was then divided into small cylindrical wells of approximately 1 cm in diameter and 2 cm in height and left to solidify. Approximately 1 mL of suspension was used per well. Finally, the gels were taken out of the wells and equilibrated in 50 mM Ca(NO3)2 + 20 mM NaNO3, which is a standard fixing solution for preparation of laboratory alginates after internal setting. Subsequently, they were equilibrated in different Cd solutions. Voltammetric measurements on both the gel and solution were performed after several weeks of Cd exposure, in which solutions were refreshed several times, to ensure that a true Donnan equilibrium was achieved. Prior to measurement, the gels were deoxygenated overnight. Reagents. All solutions and gels were prepared with distilled, deionized water from an EasyPure UV system (barnstead, resistivity 18.3 MΩ cm). Ca(NO3)2 was obtained from J.T. Baker BV, NaNO3 from Fluka, and Cd(NO3)2 from Sigma-Aldrich. Measuring Free Cd2+ in the Gel Phase. For the voltammetric measurements, an Ecochemie µAutolab type II potentiostat was used together with a Metrohm 663 VA stand with an amalgamated gold electrode as the working electrode. Two different gold electrodes (CH instruments) with diameters of 10 and 25 µm were used. A glassy carbon electrode was used as the counter electrode with a Ag-AgCl-3 M KCl reference electrode encased in a jacket containing a 0.25 M KNO3 solution. The gold electrode was first polished by wet grinding with 1000 and 2400 grit silicacarbide polishing paper (Struers). The electrode was then polished using a polishing cloth (DPNAP, Struers) and successively finer diamond paste (9, 6, 3, 1, 0.25 µm) together with DP-lubricant red (HG, Struers). The electrode tip was sonicated in between each polishing step. Mercury was plated onto the gold electrode at -0.4 V (vs Ag-AgCl-3 M KCl /0.25 M KNO3) in deoxygenated 5 mM Hg(CH3COO)2 and 0.1 M HClO4 until approximately 65 µC charge was accumulated. Amalgam formation between Hg and Au was controlled according to the procedure of Brendel et al. (18). A custom-made copper-wire mesh Faraday cage was fitted around the measurement cell to reduce the background noise. The following conditions were applied in dc voltammetry: initial potential -0.4 V; step potential 0.15 mV; scan rate 1.5 mV/s. The working electrode was used to first measure the Cd reduction signal in the solution phase, and then it was placed in direct contact with the gel phase. The reference electrode remained in the solution phase for both measurements. Thus, the different limiting currents represent the different free Cd concentrations in solution and gel phase as previously described by Davis et al. (13, 19). To confirm that the dc wave for the gel phase measures only the free Cd2+ concentration in the gel phase, the transient chronoamperometric Cd reduction was measured prior to establishment of steady-state diffusion. This transient signal reveals whether any immobile Cd-complexes in the gel phase contribute to the Cd flux toward the electrode before steady1092

9

ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 43, NO. 4, 2009

state is achieved. In other words, this experiment shows whether or not the immobile Cd-complexes are inert on the effective time scale of the microelectrodic technique. For the transient measurements, the potential was fixed at a value in the limiting current regime of Cd (Ed ) -0.8 V) and the reduction current was measured as a function of time. Ionic Strength Adjustments. Measurements on gels equilibrated with solutions of varying ionic strength (I ) 0.5Σcz2, in mM) were performed at a Cd2+ concentration of 1 × 10-5 M at pH 6. The pH was adjusted with NaOH (SigmaAldrich). Two different background electrolyte solutions were used to vary the ionic strength: a Ca/Na background and a Na-background (see Supporting Information Table S1). To investigate the influence of the ionic strength and the background electrolyte on the gel structure, the mass and volume of the gels were measured following their equilibration with the various solution compositions given in Supporting Information Table S1. Total Ca and Cd Content of the Gels. The total Cd, Ca, and Na contents of the gels equilibrated with the various solutions (Supporting Information Table S1) were determined on acid-leachates (1 M HNO3) by ICP-AES (Spectroflame).

Theory The uncompensated immobile charges within the alginate gel give rise to a negative Donnan potential. Consequently, the Cd2+ concentration inside the gel phase is enhanced with respect to the bulk medium. For a gel with known charge density, the Donnan potential, ψD, can be calculated (20). For a symmetrical z-z electrolyte, it is given by ΨD )

( )

zgF RT arcsin zF 2zc

(1)

where, R is the gas constant, T the (absolute) temperature, F the Faraday constant, zg the charge number of the functional groups in the gel, F the volume charge density of the gel, and c the bulk electrolyte concentration in the medium. For a more complex mixture of 2-1 and 1-1 electrolytes (e.g., Ca(NO3)2 + NaNO3), Ohshima and Kondo (20) derived the following set of expressions: -

F 1 - η -y η -2y 3 - η y )0 e - e + e 2 3 6 2c1 + 6c2 FΨD RT

(3)

3c2 c1 + 3c2

(4)

y) η)

(2)

where c1 and c2 are the concentrations of the 1:1 and 2:1 electrolytes, respectively. In biogels, F normally has a negative value due to the presence of carboxylate and other functional groups such as sulfonates (21). For pH values not far from the pKa of relevance, the protonation of the functional group sites must be taken into account in computations of ΨD (19). For most biogels the charge density is not known a priori, thus the Donnan potential must be measured in order to calculate the enhancement of the metal ion concentration in the gel according to [Mz+]gel [Mz+]sol

)

-zF Ψ D ) ΠD eRT

(5)

where Mz+ is a metal ion with charge z and ΠD is the Donnan partition coefficient. Both the Donnan potential ΨD and the enhanced free Cd2+ concentration in the gel can be measured directly using an in situ analytical technique such as microelectrode

voltammetry (13, 19). If only free metal ions are measured and the diffusion coefficient of Cd2+ in the gel is not significantly different from the one in solution (13), the ratio between the limiting Cd2+ current for the gel phase and that for the bulk solution phase represents the current-derived Donnan partition coefficient, ΠD (I) (eq 5). The observed shift in voltammetric half-wave potential (∆E1/2) between gel and solution represents the potential-derived Donnan potential, ΨD (E) (see Supporting Information Figure S2) (13, 19).

Results and Discussion Gel Stability and Swelling Behavior. To study the effects of a wide range of ionic strengths on the Donnan potentials generated by Ca-alginate gels, it was necessary to determine the ionic conditions (e.g., composition of Ca and Na) under which the alginate gel network remains sufficiently intact and thus arguably representative of cell wall matrices. While there has been significant study of the stability of alginates prepared at higher ionic strengths (e.g., >100 mM, 22, 23) data are limited for low ionic strength freshwater conditions. Typically, a minimum concentration of divalent cations is required to stabilize the alginate gel network. To characterize the significance of Ca for the integrity of alginate gels, we examined the stability and swelling behavior of the gels under a variety of combinations of Ca and Na concentrations. First, a series of experiments was performed on Ca-alginate gels that were exposed to pure Na containing solutions. Supporting Information Figure S3 demonstrates that below an ionic strength of 9 mM the gel swelling is rather small and constant. This implies that up to this ionic strength the gels retain structural stability, i.e., the level of Ca cross-linking remains approximately constant. In contrast, above an ionic strength of 9 mM, the gels swell to approximately double their initial volume, at which point they deform or are easily broken apart. This result is ascribed to competition of Na for Ca occupied sites which leads to a decrease in the number of Ca network linkages rendering the gel loosely structured, as documented in the literature (24). Establishment of this ionic strength limit for preparation of the alginate gels allowed us to focus experimentation on the range of ionic strengths for which gel integrity is maintained. Ca plays a fundamental role in alginate gelation in natural systems. Even in freshwaters, it is present at appreciable concentrations and thus we conducted experiments within the ionic strength range of 0.04-100 mM at constant Ca/Na ratio. Under these conditions, the gels remained fully stable. Following exposure of the gels for 5 days to a 50 mM Ca(NO3)2 + 20 mM NaNO3 solution, the gels syneresed (shrank) to 39% ((1%) of their original volume. Next, the gels were equilibrated in the varying ionic strength solutions (Supporting Information Table S1). The final difference in gel volume between the lowest and highest ionic strength conditions examined was approximately a factor of 2 (see Supporting Information Figure S4). These results are relative to the initial 39% syneresis which represents the original setting of the Ca-alginate network, prior to the exposure of the varying (and low) ionic strength solutions. The difference in gel volume leads to a proportional difference in charge densities for the varying ionic strengths. Immobilized Cd in the Gel Network. Conventional steady-state voltammetry was used to determine the free Cd2+ in the gel phase according to the method previously outlined by Davis et al. (13, 19). To assess the stabilization of the Cd bound by the alginate and the retardation of the release of specifically bound Cd under conditions of an ongoing Cd flux through the biogel, we applied transient voltammetry in the gel phase. The area under the timedependent reduction current (I) represents the amount of Cd2+ reduced at the electrode (Figure 1). The transient

FIGURE 1. Current transient for Cd reduction at constant potential in gel and solution. ([Cd2+] ) 10-5 M; I ) 7 mM; r0 ) 10 µm; Ed ) -0.8 V). The hatched areas represent the transient responses as enhanced relative to the eventual steady-state currents.

FIGURE 2. (a) Donnan potential ΨD and (b) Donnan partition coefficient ΠD as a function of ionic strength, measured at constant bulk solution concentration of [Cd2+]sol ) 10-5 M. Error bars represent the standard deviation (n ) 3-6). reduction current for Cd2+ in solution, Isol, is purely diffusion controlled without any contribution from Cd-complexes. If the bound Cd in the gel dissociates sufficiently fast, then the transient current in the gel, Igel, would be more than proportionally enhanced as compared to Isol due to the Cd2+ released by the gel matrix. In the eventual steady-state the concentration profiles no longer change with time, and immobile species do not contribute to the steady-state flux. Our results show that in the transient regime the increase in transient responses (Figure 1, hatched areas) is just proportional to that of Igel and Isol in the steady-state. This implies that on the time scale of (10-1 to 10+1 s the immobile Cdcomplexes in the biogel do not contribute to the Cd flux and confirms that the present voltammetric technique measures the free Cd2+ concentration in the alginate gel phase. Free Cd2+ in the Gel and the Donnan Potential. The Donnan potential can be derived from the experimental measurements as ΨD(I) and ΨD(E). As shown in Figure 2a, the so-derived Donnan potentials, and the enrichment of free Cd2+ (Figure 2b), are ionic strength dependent. In the ionic strength regime above 100 mM, the Cd concentrations VOL. 43, NO. 4, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

9

1093

FIGURE 3. Total Cd content of the gel as a function of ionic strength in a Ca/Na background at constant bulk solution concentration of [Cd2+]sol ) 10-5 M. Error bars represent the standard deviation (n ) 2-3). in the gel and in the solution are equal (ΠD ) 1), but when the ionic strength decreases, the [Cd2+] in the gel is increased compared to that in solution. The modeled Donnan potential ΨD(m) can also be calculated independently of the measured ΨD(E) and ΠD(I) by estimating the charge density F and applying eqs 2-4. Based on previous potentiometric titration of the alginate gels prepared under the same experimental conditions (13), the value of F was estimated from the total site density of the alginate gels, i.e., 113 mM at I ) 10 mM. Subsequently, the swelling/syneresis data were used to calculate the total site densities at the various ionic strengths. Finally, the amount of specifically bound Ca was subtracted from the total site density to arrive at the charge density. The results in Figure 2 show that eq 2, which has been derived for a mixture of 2-1 and 1-1 electrolytes (20), is indeed applicable for calculation of Donnan potentials in gel layers, as suggested by refs 25 and 26. The three independent methods give similar results for the Donnan potential and Donnan partitioning. Below 1 mM ionic strength, the estimates start to deviate from one another, which may be related to complications in voltammetric data interpretation. For I < 0.1 mM, the electrical transport number of Cd2+ is no longer negligible, which leads to a conductive migration component in the Cd current and an ensuing overestimation of [Cd2+] (27). Total Cd in the Gel. In the gel phase, Cd is generally present in the form of free Cd2+ and matrix-bound complexes. More specifically, the alginates provide a multidentate environment that consists of the carboxylate groups, the ring oxygens, and the hydroxyl groups of the G-residues, all of which contribute to the binding of the cations (13, 28). At constant Cd bulk solution concentration, the total Cd content of the gel increases with decreasing ionic strength (Figure 3). This increase is not related to the gel volume, because the swelling of the gels lowers the charge density, which, by itself, would lead to a decrease of the specifically bound Cd content. We observe that the specifically bound Cd is (approximately linearly) related to the free Cd2+ concentration in the gel (Figure 4). Across the ionic strength range studied, the binding coefficient in the gel phase (([Cd(II)]bound/[Cd2+]gel) is approximately 19, which is similar to the coefficient determined previously (13) for varying Cd concentrations at fixed ionic strength. The change in specifically bound Cd(II) is not due to competition with Ca2+. Variation of the ionic strength by adjusting only [Na+]sol at constant [Ca2+]sol of approximately 1 mM yields a similar dependence of the specifically bound Cd(II) on free Cd2+ in the gel phase (Supporting Information Figure S5). In addition, the binding coefficient ([Cd(II)]bound/ [Cd2+]gel (slope in Supporting Information Figure S5)) is similar to the binding coefficient when both [Ca2+] and [Na+] are varied (Figure 4). 1094

9

ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 43, NO. 4, 2009

FIGURE 4. Specifically bound Cd in the alginate gel phase as a function of free Cd2+ in the gel phase in a Ca/Na background at constant bulk solution concentration of [Cd2+]sol ) 10-5 M. Different free Cd2+ concentrations in the gel result from differing ionic strengths (several ionic strength values are indicated) and corresponding ΨD. Error bars represent the standard deviation (n ) 2-6). Implications for Bioavailability. Rather high Donnan potentials have been measured in cell walls of plants and algae, ranging from approximately -30 to -60 mV (I ) 1 to 10 mM) (29). These values compare favorably with our results even though the cell wall composition is likely to be more chemically heterogeneous than the alginate model gel, e.g., at I ) 2 mM and ΨD ) -50 mV the charge density of plant cell walls (29) is approximately 14 mM which is similar to that calculated for our 1% w/w alginate gels (ca. 16 mM). Even higher Donnan potentials are reported for bacterial cell walls: -110 to -40 mV for I ) 1 to 100 mM (30), which translates to charge densities of 78 to 468 mM and partition coefficients for divalent cations of up to 6000 (30). Even though a biological cell wall is rather thin (on the order of tens of nm), its Donnan potential can be considered approximately constant (30). However, at ionic strengths so low that the thickness of the diffuse double layer (1/κ) is comparable to the thickness of the cell wall, a position dependent Donnan potential profile is in effect. This greatly complicates the situation because all Cd(II) species concentrations then become position-dependent within the biogel layer. Figure 4 indicates that metal binding by cell walls can vary significantly as with ionic strength due to the changes in local free metal ion concentration. If we assume that the binding behavior of the active transporter ligands is similar to that of the mere adsorption sites (2), the changes in metal binding by the cell wall would lead to a similar change in metal biouptake by algae or root cells. Indeed, approximately linear relationships between metal adsorption at root surfaces and metal content of the roots have previously been reported (31, 32). There are also clear relationships between metal uptake by roots and shoots (31, 32), thus a decreased ionic strength leads to an enhanced metal uptake by plant shoots at constant metal concentration. Several studies on dried (e.g., refs 11, 33, 34) and living (e.g., refs 12, 35) algae have also shown that the amount of metal sorbed generally increases with decreasing ionic strength. A 2-fold increase in the rate of uptake of Cd by living marine macroalgae was observed on decreasing salinity from 28 to 19‰ (36); this may reflect an enhanced Cd2+ concentration in the cell wall matrix. However, the ionic strength dependent free metal ion concentration in the cell wall is rarely used as an explanation for these observations and insufficient information is available to allow a quantitative reconstruction in terms of Donnan effects. Most studies explain the ionic strength dependent metal uptake in terms of changes in the free metal ion concentration in bulk solution due to complexation (34), competition with other cations (33), change of charge of the biogel (11) or activity coefficient effects (37).

All these phenomena may certainly play a role. The present study shows that for organisms with cell walls the Donnan enhancement seems to be the most significant factor. For example, for the alginates considered herein, the enhancement factor increases from approximately 2.6 to 11 upon lowering the ionic strength from 10 to 1 mM. This factor is much larger than that due to the other ionic strength dependent factors. For example, in the mentioned ionic strength interval the activity coefficient can only explain uptake differences up to 30% (38). The main difficulty in quantifying and generalizing ionic strength effects for living organisms (e.g., ref 39,) is involved with the accuracy of the measurements or estimations of the charge and metal binding site densities for biological matrices (40, 41). Most studies of metal biouptake are performed at constant ionic strength, hence the free metal concentration in the bulk solution can be used as input for FIAM and BLM correlations. However, large differences in metal uptake can be expected along estuarine gradients and in the comparison between freshwater organisms and marine organisms. Consequently, the application of equilibrium models, such as the FIAM and the BLM, is subject to restrictions, especially when a charged cell wall is present. The primary input should be the free metal concentration at the biointerface (e.g., cell wall) rather than that in the bulk medium. In addition, as proposed by Slaveykova and Wilkinson (42), the experimentally observed stabilities of metal transporter site complexes should be corrected for the Donnan partition coefficient ΠD in order to represent the real intrinsic stability. Likewise, a Boltzmann type correction for the electric double layer potential at the biointerface should be applied in case of organisms that lack a cell wall. In situ measurement of metal speciation within biogels is an interesting new field that promises to provide considerable support for elucidating the relationships between metal speciation in the exposure media and the effective species concentrations experienced by the organism at the biointerface. This approach provides a generic analytical tool that is useful for estimating metal speciation in other biogel systems, e.g., those dominated by pectins. This study shows that large differences can exist between metal speciation (i.e., bound and free Cd) in the aqueous medium and that in the biogel. For a given biogel, the actual proportion of specifically and electrostatically bound Cd will depend on the nature of the functional groups present. When this model gel system is extrapolated to living systems, the elevated free metal concentration in a charged biogel sets greater demands on the buffering and transport capacities of the surrounding medium (43), and accordingly requires consideration of dynamic factors, i.e., lability of metal complex species which then become essential in assessing and predicting bioavailability.

Acknowledgments This work was performed within the framework of the ECODIS project funded by the European Commission’s sixth framework program, subpriority 6.3 “Global Change and Ecosystems”, under contract 518043. Prof. J. P. Pinheiro is gratefully acknowledged for his contribution to the early development of voltammetric measurements in gel phases along with Profs. Bjørn Sundby, George W. Luther III, and Dr. Cédric Magen. We also gratefully acknowledge early discussions on the topic of alginate gels with Dr. Synnøve Holtan, Dr. Kurt I. Draget and Prof. Olav Smidsrød, Department of Biotechnology, NTNU, Trondheim, Norway.

Supporting Information Available Information concerning the equilibrating solution compositions, the Ca content of the gels, a schematic representation of the interpretation of the measured voltammetric waves, variations of the mass of the gels, and additional data on the

speciation of bound and free Cd in the gel phase. This material is available free of charge via the Internet at http:// pubs.acs.org.

Literature Cited (1) Campbell, P. G. C. Interactions between trace metals and aquatic organisms: A critique of the free ion activity model. In Metal Speciation and Bioavailability in Aquatic Systems; Tessier, A. and Turner D. R., Eds.;, 1995; Vol. 3, 45-102. (2) Slaveykova, V. I.; Wilkinson, K. J. Physicochemical aspects of lead bioaccumulation by Chlorella vulgaris. Environ. Sci. Technol. 2002, 36, 969–975. (3) Mylon, S. E.; Twining, B. S.; Fisher, N. S.; Benoit, G. Relating the speciation of Cd, Cu, and Pb in two Connecticut rivers with their uptake in algae. Environ. Sci. Technol. 2003, 37, 1261– 1267. (4) Davis, T. A.; Volesky, B.; Mucci, A. A review of the biochemistry of heavy metal biosorption by brown algae. Water Res. 2003, 37, 4311–4330. (5) Fourest, E.; Volesky, B. Alginate properties and heavy metal biosorption by marine algae. Appl. Biochem. Biotechnol. 1997, 67, 215–226. (6) Davis, T. A.; Llanes, F.; Volesky, B.; Mucci, A. Metal selectivity of Sargassum spp. and their alginates in relation to their R-Lguluronic acid content and conformation. Environ. Sci. Technol. 2003, 37, 261–267. (7) Rees, D. A. Polysaccharide shape and their interactionsssome recent advances. Pure Appl. Chem. 1981, 53, 1–14. (8) Draget, K. I.; Smidsrød, O. Swelling and partial solubilization of alginic acid gel beads in acidic buffer. Carbohydr. Polym. 1996, 29, 209–215. (9) Moe, S. T.; Draget, K. I.; Skjåk-Bræk, G.; Smidsrød, O. Temperature dependence of the elastic modulus of alginate gels. Carbohydr. Polym. 1992, 19, 279–284. (10) Morris, E. R.; Rees, D. A. Competitive inhibition of interchain interactions in polysaccharide systems. J. Mol. Biol. 1980, 16, 88–91. (11) Vilar, V. J. P.; Botelho, M. S.; Boaventura, R. A. R. Copper removal by algae Gelidium, agar extraction algal waste and granulated algal waste: Kinetics and equilibrium. Bioresour. Technol. 2008, 99, 750–762. (12) Crist, R. H.; Oberholser, K.; McGarrity, J.; Crist, D. R.; Johnson, J. K.; Brittsan, J. M. Interactions of metals and protons with algae. 3. Marine algae, with emphasis on lead and aluminum. Environ. Sci. Technol. 1992, 26, 496–502. (13) Davis, T. A.; Kalis, E. J. J.; Pinheiro, J. P.; Town, R. M.; van Leeuwen, H. P. Cd(II) speciation in alginate gels. Environ. Sci. Technol. 2008, 42, 7242–7247. (14) Yezek, L. P.; van Leeuwen, H. P. An electrokinetic characterization of low charge density cross-linked polyacrylamide gels. J. Colloid Interface Sci. 2004, 278, 243–250. (15) Yezek, L. P.; Duval, J. F. L. Interpretation of data on the polyacrylamide/water interface. Langmuir 2005, 21, 6220–6227. (16) Di Toro, D. M.; Allen, H. E.; Bergman, H. L.; Meyer, J. S.; Paquin, P. R.; Santore, R. C. Biotic ligand model of the acute toxicity of metals. 1. Technical basis. Environ. Toxicol. Chem. 2001, 20, 2383–2396. (17) Draget, K. I.; Østgaard, K.; Smidsrød, O. Homogeneous alginate gels: a technical approach. Carbohydr. Polym. 1991, 14, 159– 178. (18) Brendel, P. J.; Luther, G. W. Development of a gold amalgam voltammetric microelectrode for the determination of dissolved Fe, Mn, O2, and S(-II) in porewaters of marine and freshwater sediments. Environ. Sci. Technol. 1995, 29, 751–761. (19) Davis, T. A.; Yezek, L. P.; Pinheiro, J. P.; van Leeuwen, H. P. Measurement of Donnan potentials in gels by in situ microelectrode voltammetry. J. Electroanal. Chem. 2005, 584, 100– 109. (20) Ohshima, H.; Kondo, T. Relationship among the surface potential, Donnan potential and charge density of ionpenetrable membranes. Biophys. Chem. 1990, 38, 117–122. (21) Fourest, E.; Volesky, B. Contribution of sulfonate groups and alginate to heavy metal biosorption by the dry biomass of Sargassum fluitans. Environ. Sci. Technol. 1996, 30, 277–282. (22) Haug, A.; Smidsrød, O. The effect of divalent metals on the properties of alginate solutions. II. Acta Chem. Scand. 1965, 19, 341–351. (23) Smidsrød, O.; Haug, A. Dependence upon uronic acid composition of some ion-exchange properties of alginates. Acta Chem. Scand. 1968, 22, 1989–1997. VOL. 43, NO. 4, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

9

1095

(24) Smidsrød, O.; Haug, A. The effect of divalent metals on the properties of alginate solutions. I. Calcium ions. Acta Chem. Scand. 1965, 19, 329–340. (25) Higa, M.; Tanioka, A.; Kira, A. A novel measurement method of Donnan potential at an interface between a charged membrane and mixed salt solution. J. Membr. Sci. 1998, 140, 213–220. (26) Wasserman, E.; Felmy, A. R. Computation of the electrical double layer properties of semipermeable membranes in multicomponent electrolytes. Appl. Environ. Microbiol. 1998, 64, 2295– 2300. (27) Heyrorsky´, J.; Kuta, J. Principles of Polarography; Academic Press: New York, 1966. (28) Jodra, Y.; Mijangos, F. Ion exchange selectivities of calcium alginate gels for heavy metals. Water Sci. Technol. 2001, 43, 237–244. (29) Shomer, I.; Novacky, A. J.; Pike, S. M.; Yermiyahu, U.; Kinraide, T. B. Electrical potentials of plant cell walls in response to the ionic environment. Plant Physiol. 2003, 133, 411–422. (30) van der Wal, A.; Minor, M.; Norde, W.; Zehnder, A. J. B.; Lyklema, J. Electrokinetic potential of bacterial cells. Langmuir 1997, 13, 165–171. (31) Kalis, E. J. J.; Temminghoff, E. J. M.; Visser, A.; van Riemsdijk, W. H. Metal uptake by Lolium perenne in contaminated soils using a four-step approach. Environ. Toxicol. Chem. 2007, 26, 335–345. (32) Kalis, E. J. J.; Temminghoff, E. J. M.; Weng, L. P.; van Riemsdijk, W. H. Effects of humic acid and competing cations on metal uptake by Lolium perenne. Environ. Toxicol. Chem. 2006, 35, 702–711. (33) Lodeiro, P.; Barriada, J. L.; Herrero, R.; Sastre de Vicente, M. E. The marine macroalga Cystoseira baccata as biosorbent for cadmium(II) and lead(II) removal: Kinetic and equilibrium studies. Environ. Pollut. 2006, 142, 264–273.

1096

9

ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 43, NO. 4, 2009

(34) Tsui, M. T. K.; Cheung, K. C.; Tam, N. F. Y.; Wong, M. H. A comparative study on metal sorption by brown seaweed. Chemosphere 2006, 65, 51–57. (35) Santana-Casiano, J. P.; Gonzalez-Davilla, M.; Perez-Pen ˜ a, J.; Millero, F. J. Pb2+ interactions with the marine phytoplankton Dunaliella tertiolecta. Mar. Chem. 1995, 48, 115–129. (36) Wang, W. X.; Dei, R. C. H. Kinetic measurements of metal accumulation in two marine macroalgae. Mar. Biol. 1999, 135, 11–23. (37) Osman, M. S.; Bandyopadhyay, M. Cadmium removal from water environment by a fungus Volveriella volvacea. Bioprocess Eng. 1996, 14, 249–254. (38) Davies, C. W. Ion Associations; Butterworths: Washington DC, 1962. (39) Turner, A.; Pedroso, S. S.; Brown, M. T. Influence of salinity and humic substances on the uptake of trace metals by the marine macroalga, Ulva lactuca: Experimental observations and modelling using WHAM. Mar. Chem. 2008, 110, 176–184. (40) Gelabert, A.; Pokrovsky, O. S.; Viers, J.; Schott, J.; Boudou, A.; Feurtet-Mazel, A. Interaction between zinc and freshwater and marine diatom species: Surface complexation and Zn isotope fractionation. Geochim. Cosmochim. Acta 2006, 70, 839–857. (41) Meychik, N. R.; Nikolaeva, Y. I.; Yermakov, I. P. Ion-exchange properties of cell walls of Spinacia oleracea L. roots under different environmental salt conditions. Biochemistry-Moscow 2006, 71, 781–789. (42) Slaveykova, V. I.; Wilkinson, K. J. Predicting the biovailability of metals and metal complexes: Critical review of the Biotic Ligand Model. Environ. Chem. 2005, 2, 9–24. (43) Yezek, L. P.; van Leeuwen, H. P. Donnan effects in the steadystate diffusion of metal ions through charged thin films. Langmuir 2005, 21, 10342–10347.

ES802305N