The effect of high ionic strength on neptunium (V) adsorption to a halophilic bacterium
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1 Available online at Geochimica et Cosmochimica Acta 110 (2013) The effect of high ionic strength on neptunium (V) adsorption to a halophilic bacterium David A. Ams a,, Juliet S. Swanson a, Jennifer E.S. Szymanowski b, Jeremy B. Fein b, Michael Richmann a, Donald T. Reed a a Earth and Environmental Sciences Division, Los Alamos National Laboratory, Carlsbad, NM 88220, USA b Department of Civil Engineering and Geological Sciences, University of Notre Dame, Notre Dame, IN 46556, USA Received 9 September 2011; accepted in revised form 18 January 2013; available online 8 February 2013 Abstract The mobility of neptunium (V) in subsurface high ionic strength aqueous systems may be strongly influenced by adsorption to the cell wall of the halophilic bacteria Chromohalobacter sp. This study is the first to evaluate the adsorption of neptunium (V) to the surface of a halophilic bacterium as a function of ph from approximately 2 to 10 and at ionic strengths of 2 and 4 M. This is also the first study to evaluate the effects of carbonate complexation with neptunium (V) on adsorption to whole bacterial cells under high ph conditions. A thermodynamically-based surface complexation model was adapted to describe experimental adsorption data under high ionic strength conditions where traditional corrections for aqueous ion activity are invalid. Adsorption of neptunium (V) was rapid and reversible under the conditions of the study. Adsorption was significant over the entire ph range evaluated for both ionic strength conditions and was shown to be dependent on the speciation of the sites on the bacterial surface and neptunium (V) in solution. Adsorption behavior was controlled by the relatively strong electrostatic attraction of the positively charged neptunyl ion to the negatively charged bacterial surface at ph below circum-neutral. At ph above circum-neutral, the adsorption behavior was controlled by the presence of negatively charged neptunium (V) carbonate complexes resulting in decreased adsorption, although adsorption was still significant due to the adsorption of negatively charged neptunyl-carbonate species. Adsorption in 4 M NaClO 4 was enhanced relative to adsorption in 2 M NaClO 4 over the majority of the ph range evaluated, likely due to the effect of increasing aqueous ion activity at high ionic strength. The protonation/deprotonation characteristics of the cell wall of Chromohalobacter sp. were evaluated by potentiometric titrations in 2 and 4 M NaClO 4. Bacterial titration results indicated that Chromohalobacter sp. exhibits similar proton buffering capacity to previously studied non-halophilic bacteria. The titration data were used to determine the number of types, concentrations, and associated deprotonation constants of functional groups on the bacterial surface; the neptunium adsorption measurements were used to constrain binding constant values for the important neptunium (V)-bacterial surface species. Together, these results can be incorporated into geochemical speciation models to aid in the prediction of neptunium (V) mobility in complex bacteria-bearing geochemical systems. Ó 2013 Elsevier Ltd. All rights reserved. 1. INTRODUCTION Corresponding author. Address: Actinide Chemistry and Repository Science Program, Earth and Environmental Sciences Division 12, Los Alamos National Laboratory, 115 N. Main St., Carlsbad, NM 88220, USA. address: dams@lanl.gov (D.A. Ams). Extensive quantities of radioactive waste have resulted from the production of electrical power and weapons utilizing nuclear fuel, nuclear weapons testing, and nuclear fuel processing (Hu et al., 2010). A significant quantity of the radioactive waste is expected to be stored in deep geological formations. Radioactive environmental contamination /$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved.
2 46 D.A. Ams et al. / Geochimica et Cosmochimica Acta 110 (2013) exists in subsurface soil and groundwater due to nuclear accidents, leaking storage tanks, leaching from uranium mine tailings, and past dumping into waterways and unlined storage ponds. Groundwater is the primary transport pathway for radionuclides at contaminated environmental sites and in performance assessment models for geologic waste repositories. As such, understanding the mechanisms controlling the fate and transport of radionuclides in subsurface aqueous environments is critical for the development of appropriate environmental containment strategies and for evaluating the long-term efficacy of current and future radionuclide waste-storage scenarios. Neptunium (V), as the neptunyl ion (NpO 2 + ) and associated complexed species, is readily soluble and interacts weakly with geologic media under a relatively wide range of subsurface conditions (e.g., Kaszuba and Runde, 1999; Yoshida et al., 2006; Reed et al., 2010). These chemical properties, combined with a long half-life, make neptunium a primary element of concern regarding long-term nuclear waste storage and subsurface containment. Neptunium is a radioactive transuranic actinide element generated primarily as a manmade byproduct of plutonium production. Spent nuclear fuel, high level nuclear waste, and various forms of defense-related nuclear waste contain significant concentrations of neptunium (Yoshida et al., 2006). In some instances, such as for spent nuclear fuel, the contribution of neptunium to the current level of total radioactivity of the waste is low relative to the presence of shorter-lived radionuclides of very high activity. However, with time, Am-241 (t 1/2 = years), a currently abundant component of spent nuclear fuel, will decay into Np-237. Since neptunium has a relatively long half-life (t 1/2 = years) its concentration will increase considerably with time, making neptunium one of the dominant radioactive elements present in a variety of nuclear waste forms after approximately 100,000 years (Kaszuba and Runde, 1999). Although 22 isotopes of neptunium are now known, only Np-237 is produced in sufficient quantities to be of significant environmental concern (Yoshida et al., 2006). Although neptunium exhibits a complex aqueous chemistry and is predicted to exist in either the +4, +5, or +6 oxidation state under a variety of near surface environmental conditions (Yoshida et al., 2006), neptunium (V) is expected to be the predominant oxidation state in aerobic natural waters (Allard et al., 1980; Reed et al., 2010). Further, bacteria have been shown to reduce neptunium (V) to neptunium (IV) in aqueous systems in some instances (Lloyd et al., 2000; Rittmann et al., 2002; Gorman-Lewis et al. 2005a; Icopini et al., 2007; Law et al., 2010). The solubility of neptunium (V) is generally considerably higher than that of neptunium (IV) resulting in the potential for enhanced aqueous mobility (Bondietti and Francis, 1977; Lemire et al., 2001; Arnold et al., 2006). Aqueous neptunium (V) commonly exists as the highly stable neptunyl species at ph less than approximately 8; at higher ph, when carbonate is present, carbonate complexed species become increasingly important (e.g., Maya, 1983; Neck et al., 1994; Kaszuba and Runde, 1999), hydrolysis may become important at ph greater than 10 in low carbonate systems (e.g., Lierse et al., 1985; Neck et al., 1992), mixed hydroxocarbonato species may also exist at ph greater than 11 (Neck et al., 1997). The fate and transport of neptunium in the environment may be influenced by a variety of factors including adsorption onto bacterial surfaces. Metal adsorption to bacterial surfaces ties the mobility of the metal to the mobility of the bacteria (e.g., McCarthy and Zachara, 1989; Yee and Fein, 2002). Although presumed to be weakly interactive in the environment, Songkasiri et al. (2002), Gorman-Lewis et al. (2005a), Luk yanova et al. (2008), and Deo et al. (2010) have observed substantial ph-dependent adsorption of the neptunyl ion to the surface of non-halophilic bacteria under low ionic strength conditions (I < 0.5 M). To date, Gorman-Lewis et al. (2005a) performed the only study evaluating the effect of ionic strength on the adsorption of neptunium (V) to a bacterial surface; showing a decrease in neptunium (V) adsorption to the non-halophilic Gram-positive bacterium Bacillus subtilis with increasing ionic strength over the range of to 0.5 M. However, evaluation of the potential effects of ionic strength conditions greater than 0.5 M is critical for understanding the fate and transport characteristics of neptunium in high ionic strength aqueous natural environments, such as in the vicinity of salt-based nuclear waste repositories and high ionic-strength groundwater at DOE sites. To date, very few studies (Francis et al., 1998, 2004; Gillow et al., 2000) have evaluated the heavy metal adsorption potential of halotolerant and halophilic microorganisms, which dominate the microbial ecology in natural high ionic strength aqueous environments. Francis et al. (1998) showed that halotolerant and halophilic bacteria and archaea can adsorb actinides, including neptunium, to an appreciable extent. However, their study focused on evaluating adsorption at one ph and one ionic strength for each microorganism studied. To date, no study has evaluated the ph and ionic strength dependency on the adsorption of any actinide to halotolerant and halophilic microorganisms under high ionic strength conditions. In this study, the adsorption of neptunium (V) was evaluated at high ionic strength on a halophilic bacterium isolated from a briny groundwater near the Waste Isolation Pilot Plant (WIPP) in southeast New Mexico. Deprotonation constants and site concentrations for bacterial surface functional groups were characterized by application of a non-electrostatic surface complexation model to experimental bacterial potentiometric titration data. Neptunium (V) adsorption was measured as a function of ph and ionic strength. Surface complexation modeling was adapted to account for the effects of high ionic strength and was applied to the neptunium (V) adsorption data to calculate thermodynamically-based binding constants for discrete sites on the bacterial surface. This modeling approach offers an advantage over conventional adsorption models that utilize empirical distribution coefficients because surface complexation model results yield thermodynamically-based constants. Thermodynamically-based constants can be incorporated into geochemical speciation models to describe the same equilibrium reactions under more complex conditions that may differ significantly from the experimental conditions investigated. This work expands the under-
3 D.A. Ams et al. / Geochimica et Cosmochimica Acta 110 (2013) standing of actinide bacteria adsorption phenomena and serves as an aid to predicting neptunium (V) fate and transport behavior in high ionic strength environmental conditions where halotolerant and halophilic microorganisms are present ph and pc H+ 2. METHODS The measurement of ph (negative logarithm of the hydrogen ion activity) in high ionic strength solutions is not straightforward due to interferences at the liquid junctions of standard ph electrodes and lack of standard buffer solutions for calibration in high ionic strength solutions. In this study, we use the procedure initially developed by Rai et al. (1995) and modified by Borkowski et al. (2009) to relate the apparent ph reading by a standard combination ph electrode to the hydrogen ion concentration (pc H+ ) through use of the following relationship: pc Hþ ¼ ph measured þ K ð1þ where the constant K is specific for a particular ionic strength and the standard type combination electrodes used in these experiments. Borkowski et al. (2009) observed a linear relationship between the value of K and ionic strength that is represented by the following equation: K ¼ð0:1868 IÞ 0:073 ð2þ where I is the ionic strength of the solution. Eqs. (1) and (2) are used in this study to calculate pc H+. As is apparent from Eq. (2), the value of the constant K at low ionic strength (i.e., I < 0.5 M) is negligible for most applications. Thus, under low ionic strength conditions ph essentially equals pc H+. Throughout the remainder of this paper only corrected pc H+ values will be reported for experimental data. The pc H+ terminology will also be used when referring to the results of previous studies performed under low ionic strength conditions Potentiometric titrations The bacterial species used in this study was a halophilic Gram-negative Chromohalobacter sp. A detailed discussion of its collection, isolation and characterization, as well as the procedure for preparation in potentiometric titration and sorption studies is presented in the Supplemental information. Potentiometric titration experiments were performed on concentrated suspensions (approximately g wet weight/l) of Chromohalobacter sp. in order to quantify the deprotonation constants and site concentrations of the proton-active bacterial surface functional groups. Triplicate base titrations were performed at 2 and 4 M ionic strength. To evaluate reversibility, two of the base titrations for each ionic strength condition were reversed by titrating back down pc H+ with acid. Bacteria, prepared as described in the Supplemental information, were suspended in approximately 6 to 7 ml of either 2 or 4 M NaClO 4 that had been purged of CO 2 by bubbling with N 2 for 60 min. Blank titrations consisting of only the purged electrolyte solution for both 2 and 4 M conditions showed negligible proton-buffering indicating that any residual bicarbonate or carbonate that may have remained in solution after purging exhibited a negligible effect relative to the buffering observed by the bacteria (Fig. SI-1). The suspension was immediately placed into a sealed titration vessel maintained under a positive headspace pressure of N 2 at 25 C and constantly stirred with a magnetic stir bar. Titrations were conducted using an automated burette assembly and pc H+ was measured with a glass combination electrode (Thermo Orion 9203BN). The electrode was standardized periodically throughout each day of use with a four ph standard (Fisher Scientific) calibration spanning the pc H+ range of the titrations. Each suspension was first titrated down pc H+ to a starting pc H+ of approximately 3 to 4.5 using minute aliquots of N HCl. Base titrations were then performed using aliquots of N NaOH. Titrations were performed to a maximum pc H+ of approximately 10.5 to 11 to avoid potential cellular damage to the bacteria under very basic conditions. In separate experiments, aqueous total organic carbon concentrations (analyzed on a Teledyne Tekmar total organic carbon analyzer) measured over the pc H+ range of 3 to 12 in suspensions of 5 g/l Chromohalobacter sp. in 2 M NaClO 4 and 5 g/l were shown to increase significantly at pc H+ greater than approximately 10.5 to 11, suggesting cell lysis (data not shown). Reverse titrations were titrated back down pc H+ with N HCl to evaluate the extent of reversibility in the observed proton buffering behavior over the pc H+ range of the titration. During each titration, the suspension reached a pc H+ stability of 0.01 mv/s (coinciding approximately with pc H+ units/s), the smallest drift allowed by the instrument, prior to the addition of the next aliquot of acid or base. As discussed below, this stability allowed for reversibility of the titrations reported herein. The total volume of acid and base added during each of the titrations ranged from approximately 0.76% to 1.46% of the starting volume of the solution pc H+ dependent adsorption experiments A detailed discussion of the preparation and purification of the neptunium (V) stock solution used in sorption experiments is presented in the Supplemental information. An electrolyte solution of either 2 or 4 M NaClO 4 was spiked with a small aliquot (less than 200 ll) of neptunium (V) stock solution yielding a neptunium concentration of M. This concentration is below saturation with respect to solid neptunium (V) phases over the pc H+ range studied, thus any decrease in aqueous neptunium (V) concentration during the experiment is attributed to adsorption onto the bacteria. Control experiments without the addition of bacteria showed a slight loss of neptunium (V) from solution (<5%) over the entire pc H+ range evaluated for both 2 and 4 M conditions which was accounted for by subtracting from the adsorption data in experiments with bacteria. In previous studies, various bacterial species have been shown to be tolerant to concentrations of neptunium orders of magnitude higher than used in this study (e.g., Banaszak et al., 1998; Icopini et al., 2007; Law et al., 2010). The
4 48 D.A. Ams et al. / Geochimica et Cosmochimica Acta 110 (2013) pc H+ of the neptunium spiked electrolyte solution was adjusted to 6.5 prior to the addition of bacterial cells to avoid potential acid disruption of the cell wall prior to experimentation. Following the bacteria preparation procedure, the bacterial pellet was suspended in the neptunium spiked electrolyte in a volume yielding a bacterial concentration of 5 g (wet weight)/l. This bacterial concentration provided approximately two orders of magnitude excess surface sites available for adsorption relative to the total neptunium concentration in the system. Once the bacterial suspension was homogenously distributed by stirring and vortexing, 3 ml of the bacterial/neptunium suspension were transferred into 15 ml polypropylene tube reaction vessels, and the pc H+ was adjusted to a desired value with small aliquots of either 0.01 or 0.1 M HCl or NaOH. Carbon dioxide was not excluded from the experimental solutions and equilibration with atmospheric carbon dioxide partial pressure is assumed. Reaction vessels were then slowly rotated end-over-end for 2 h followed by measurement of the final equilibrium pc H+. A 200 ll aliquot from each reaction vessel was then transferred to 3 ml of liquid scintillation solution (Optiphase Hisafe 3, formulated for high ionic strength samples; Perkin Elmer) to evaluate the neptunium concentration in non-filtered samples. Another aliquot from each reaction vessel was transferred to centrifuge tubes containing spin filters with approximately 6 nm pore size (regenerated cellulose filter material; Millipore) and centrifuged for 10 min at 12,100g to remove the bacteria from the suspension. A 200 ll aliquot of the filtered supernatant was transferred to 3 ml of liquid scintillation solution to evaluate the neptunium concentration in filtered aqueous samples. Each sample was counted by a-liquid scintillation counting for 30 min. Uncertainties in measured neptunium (V) concentrations associated with counting and pipetting were determined to be less than 5% at the 95% confidence interval. The concentration of neptunium adsorbed to the bacterial surface was determined by subtraction of the final concentration in solution from the initial total concentration. Control experiments without the addition of bacteria were performed to account for the extent, if any, of neptunium adsorption to the reaction vessel walls, filter assemblies, or other experimental apparatus. The liquid scintillation solution without the addition of sample was also counted by a-liquid scintillation counting for each experiment to quantify background counts Desorption experiments Desorption experiments were performed with similar techniques as pc H+ dependent adsorption experiments. A suspension of 5 g/l bacteria in 2 M NaClO 4 electrolyte containing M neptunium (V) was prepared. The pc H+ of this suspension was adjusted to approximately 7.33 and then allowed to react for 2 h while being slowly rotated. After the initial reaction period the pc H+ was measured and an aliquot was removed from the suspension for analysis. From the remaining suspension 5 ml were transferred to four 15 ml polypropylene tube reaction vessels and the pc H+ was readjusted to either 3.92, 6.51, 8.15, or 9.03 and allowed to react for an additional 2 h followed by final pc H+ measurement and sample collection. Non-filtered and filtered samples were collected and analyzed as previously described Adsorption kinetics experiments Adsorption kinetics experiments were performed with similar techniques as pc H+ dependent experiments, except experiments were conducted as a function of exposure time. An approximately pc H+ 6 adjusted suspension of 5 g/l bacteria in 2 or 4 M NaClO 4 electrolyte containing M neptunium (V) was prepared. 3 ml aliquots of this suspension were transferred to 15 ml polypropylene tube reaction vessels and allowed to react while being slowly rotated. Individual reaction vessels were sacrificed at various time intervals, the final pc H+ was measured for each, and non-filtered and filtered samples were collected and analyzed as previously described Surface complexation modeling A surface complexation model invoking the presence of discrete proton-active bacterial surface sites was applied to the experimental titration data to quantify the proton buffering capacity of the bacterial surface. This model is used to determine deprotonation constants and concentrations of all the proton-active surface sites determined by the model. This approach has been applied previously to describe the proton buffering behavior of a variety of microorganisms under various conditions and is described in detail by Fein et al., 1997, In this study, discrete proton-active bacterial surface sites are represented as monoprotic acids according to the reaction: R-L n H x $ R-L x 1 n þ H þ ð3þ where R represents the bacterium to which the functional group type L n is attached. The corresponding expression for the deprotonation constant, K a,is K a ¼½R-L x 1 n Ša Hþ =½R-L n H x Š ð4þ where [R-L x 1 n ] and [R-L n H x ] represent the concentration of deprotonated and protonated sites, respectively, of charge x for site L n, and a H+ represents the activity of protons in the bulk solution. The surface complexation model was also applied to the experimental neptunium adsorption data to quantify adsorption behavior through the calculation of binding constants describing the adsorption of aqueous neptunium (V) species to discrete bacterial surface sites. This approach has been successfully applied previously to model sorption of a variety of metals onto a variety of bacterial species including neptunium (V) onto B. subtilis under low ionic strength conditions (Gorman-Lewis et al., 2005a; Deo et al., 2010). Aqueous neptunium (V) can undergo hydrolysis at pc H+ greater than approximately 8 and neptunium (V) carbonate complexation under basic pc H+ conditions is significant in systems equilibrated with the atmosphere. These complexes were accounted for in the neptunium (V) adsorption models by including the reactions presented in Table 1. In this study, neptunium (V) adsorption to the bac-
5 D.A. Ams et al. / Geochimica et Cosmochimica Acta 110 (2013) Table 1 Reactions and apparent constants applied in surface complexation modeling. a I =2M I =4M Water dissociation H 2 O M H + +OH Neptunyl hydrolysis NpO + 2 +OH M NpO 2 OH NpO OH M NpO 2 (OH) Carbonate speciation H 2 CO 3 M H + + HCO HCO 3 M H + 2 +CO Neptunyl-carbonate complexation NpO + 2 +CO 2 3 M NpO 2 CO NpO CO M NpO 2 (CO 3 ) NpO CO M NpO 2 (CO 3 ) a Apparent stability constants calculated using the EQ3/6 version 8a geochemical modeling software (Wolery, 2003) with the FMT_ CHEMDAT thermodynamic database. terial surface is represented as a neptunium (V) species (i.e., aquo, hydroxyl, or carbonate) with monodentate binding to a deprotonated bacterial surface site according to the reaction: NpðVÞ m þ R-L x 1 n $ R-L n NpðVÞ mþx 1 ð5þ where Np(V) m represents a neptunium (V) species with charge m. The corresponding expression for the neptunium (V) binding constant, K, is h i K ¼ R-L n NpðVÞ mþx 1 =a NpðVÞm R-L x 1 n where [R-L n Np(V) m+x 1 ] represents the concentration of the neptunium (V) species/bacterial surface site complex, for site L n, and a Np(V)m represents the activity of the neptunium (V) species in bulk solution. The non-linear regression computer program FITEQL 2.0, described by Westall (1982), was used to calculate the functional group site concentrations and proton and neptunium (V) binding constants. The relative quality of fit for each tested model was evaluated by visual comparison of fits and by comparing an associated variance function, V(Y), that is calculated by FITEQL. Lower V(Y) values signify a higher quality fit to the experimental data. Model fits with V(Y) values between 0 and 20 are generally considered acceptable. Further discussion of the experimental modeling approach for titration and adsorption data is presented in the Supplemental information. 3. RESULTS AND DISCUSSION 3.1. Potentiometric titrations The data curves for bacterial potentiometric titrations in Fig. 1 and SI-1 are presented as the net molality of protons added per gram of bacteria as a function of pc H+. The net molality of protons added is calculated from the titration data according to the expression: ð6þ net molality of H+ added per gram of bacteria (M H+ / g bacteria ) 2.5E E E E E E E E pc H+ Fig. 1. Best-fit calculated 4-site surface complexation model curves (solid curves) to representative potentiometric titration data of Chromohalobacter sp. in 2 (open circles) and 4 (open triangles) M NaClO 4. ½H þ Š net added ¼ C a C b ð7þ where [H + ] net added represents the net molality of protons added, C a represents the total concentration of 1:1 acid added, and C b represents the total concentration of 1:1 base added. The variation exhibited by replicate titration data for both the 2 and 4 M ionic strength conditions (Fig. SI- 1) is typical for titrations of bacteria (e.g., Borrok and Fein, 2005; Borrok et al., 2005; Fein et al., 2005) and indicates strong reproducibility between experiments. The similarity, within experimental variation, between acid and base titrations (Fig. SI-1) strongly suggests that the protonation/ deprotonation reactions of the bacterial surface are reversible over the pc H+ range evaluated. Control titrations of the experimental electrolyte (2 or 4 M NaClO 4 ) without bacteria showed negligible pc H+ buffering capacity over the pc H+ range studied (Fig. SI-1). The titration results show that Chromohalobacter sp. exhibits extensive proton buffering capacity over the entire pc H+ range studied, approximately 3.5 to 11, in both 2 and 4 M NaClO 4, with the greatest degree of buffering between pc H+ approximately 3.5 to 7. These data indicate that the bacterial surface is not fully protonated even at the lowest pc H+ and continues to deprotonate over the entire pc H+ range studied. Each replicate bacterial base and acid titration was modeled without correcting for bulk aqueous ion activity or surface electric field effects to determine the number of types of discrete proton active sites required to account for the observed proton buffering capacity, as well as the deprotonation constant (K a ; Eq. (4)) and site concentration for each site type. Models invoking four surface sites provide the best visual fits and V(Y) values to each replicate titration. Models utilizing one to three surface sites provide poorer visual fits and significantly higher V(Y) values than the four site model. Models utilizing five surface site types do not converge, indicating that these models are under-constrained by the data. The four site model fit to representa-
6 50 D.A. Ams et al. / Geochimica et Cosmochimica Acta 110 (2013) Table 2 Average a calculated concentrations and deprotonation constants for functional groups on the cell wall surface of Chromohalobacter sp. [site] b Std. dev. c d pk a +/ c L / 0.18 L / 0.14 L / 0.26 L / 0.76 a Average of results from all replicate acid and base titration models for 2 and 4 M ionic strength conditions. b Moles of sites per gram wet weight of bacteria. c +/ uncertainty based on one standard deviation of results from all replicate acid and base titration models for 2 M and 4 M ionic strength conditions. d Calculated with FITEQL based on Eq. (4), K a = [R-L x 1 n ]a H+ / [R-L n H x ]. tive titration curves at 2 and 4 M ionic strength are shown in Fig. 1. The four site model provides an excellent fit to the experimental data throughout the entire pc H+ range evaluated. The deprotonation constant and site concentration values calculated for each discrete surface site for each individual replicate titration at 2 and 4 M ionic strength are presented in Table SI-1. In this study, the four discrete bacterial surface sites determined from the model calculations are referred to as sites L1 through L4, and correspond to the sites with the lowest to highest pk a values, respectively. Studies have suggested that carboxyl, phosphoryl, hydroxyl, and amine moieties are the primary proton-active sites and sites responsible for metal adsorption on the surface of various non-halophilic (e.g., Beveridge and Murray 1980; Hennig et al., 2001; Kelly et al., 2002; Panak et al., 2002; Boyanov et al., 2003; Burnett et al., 2006; Ngwenya et al., 2009; Moon and Peacock 2011) and halophilic (Francis et al., 2004) Gram-positive and Gram-negative bacteria. Spectroscopic studies of metal adsorption performed by Kelly et al. (2002) and Boyanov et al. (2003) suggest that low pk a sites on the surface of B. subtilis are phosphoryl and carboxyl moieties. Boyanov et al. (2003) further identified the presence of a third, higher pk a, bacterial surface site, however its chemical identity was not determined. Bacterial cell walls of different species are comprised of similar chemical components, and it is likely that the identified chemical moieties responsible for sorption onto other bacterial species are similar to that for the Chromohalobacter sp. used in this study. The deprotonation constants and surface site densities calculated for each individual replicate titration including the acid reversal titrations are in agreement, within experimental uncertainty, (Table SI-1) further indicating that the bacterial titrations are reversible and reproducible. It should be noted that increased uncertainty between calculated concentrations and pk a values associated with the L4 high pk a site is expected because the experimental data are less well constrained at the ph extremes resulting in higher uncertainties. The shapes and positions of the bacterial titration curves in 2 and 4 M NaClO 4 are in agreement, within experimental uncertainty (Fig. 1 and SI-1), indicating that the effect of ionic strength on proton adsorption/desorption to the bacterial surface is negligible over this range of ionic strength. As a result, the calculated deprotonation constants and surface site densities for each 2 and 4 M titration data-set agree (Table SI-1), within experimental uncertainties. Consequently, the average of the calculated deprotonation constant and site concentration values from each data-set are used to represent the protonation/deprotonation behavior of the Chromohalobcater sp. used in this study. The average deprotonation constant and site concentration values for each surface functional group are presented in Table 2. Previous studies have evaluated the effect of ionic strength on proton adsorption behavior to bacteria at ionic strengths considerably lower than in this study (i.e., I M) (e.g., Daughney and Fein, 1998; Cox et al., 1999; Haas et al., 2001; Martinez et al., 2002; Borrok and Fein, 2005; Fein et al., 2005). Similar to the results presented herein, these previous studies also showed only slight to no variation in proton buffering of various bacterial species with ionic strength and any variations in calculated modeling results were, in general, determined to be statistically insignificant. Because the protonation/deprotonation behavior of bacteria appears to be independent of ionic strength, neglecting corrections for bulk aqueous ion activity and surface electric field effects does not affect the calculation of bacterial surface site concentrations and associated deprotonation constants. Therefore, these parameters may be considered as intrinsic thermodynamic parameters. In contrast to what has been observed for bacterial surfaces, Schijf and Ebling (2010) showed that the proton buffering capacity of an algae, Ulva lactuca, a eukaryotic microorganism, was dependent on ionic strength over the range of 0.01 to 5 M, and they used an extended Debye Hückel relation to model the effect on calculated site concentration and acidity constant values. It is difficult to meaningfully compare the modeling results of different bacterial titration studies because the calculated parameters are strongly dependent on a number of factors including: the pc H+ range evaluated, whether an electrostatic model was applied and the type and manner in which it was applied, and whether bulk aqueous ion activity corrections were accounted for. However, meaningful comparisons can be made by directly evaluating the proton buffering capacity of bacteria in terms of the absolute value of protons consumed per gram of bacteria versus pc H+. As shown in Fig. 1 and SI-1, the average absolute value of protons consumed in Chromohalobacter sp. titrations at both 2 and 4 M ionic strength is approximately 0.02 M H + /g in the high buffering region of the curve from pc H+ 4 to 7, and 0.01 M H + /g in the lower buffering region of the curve from pc H+ 7 to 9.7. Previous titrations of nonhalophilic Gram-positive (Fein et al., 2005) and Gram-negative bacteria (Haas et al., 2001; Borrok and Fein, 2005) show a similar proton buffering capacity in these pc H+ ranges. The results reported herein are the first to show that a halophilic bacterium, initially cultured from a groundwater with an ionic strength of approximately 4.5 M, exhibits similar protonation/deprotonation behavior as common non-halophilic soil bacteria.
7 D.A. Ams et al. / Geochimica et Cosmochimica Acta 110 (2013) Neptunium (V) adsorption and desorption experiments The results of the adsorption kinetics experiments are presented in Fig. 2 and show that at pc H+ approximately 6 in 2 and 4 M NaClO 4 the concentration of neptunium (V) adsorbed to Chromohalobacter sp. plateaus rapidly and does not, within the analytical uncertainty of ±5%, exhibit increased adsorption after approximately 2 h. These results are similar to the results of Songkasiri et al. (2002) and Gorman-Lewis et al. (2005a) who also showed rapid adsorption equilibrium (<15 min) at circum-neutral pc H+ with non-halophilic bacteria under low ionic strength conditions. Adsorption of neptunium (V) in abiotic control experiments was negligible (less than 5%) over the entire pc H+ range evaluated indicating that significant adsorption does not occur on any of the experimental apparatus. The results of the adsorption experiments performed as a function of pc H+ at 2 and 4 M ionic strength are presented in Fig. 3. Neptunium (V) exhibits a significant adsorption affinity for the cell wall of Chromohalobacter sp. over the entire pc H+ range for both ionic strength conditions evaluated, but the overall extent of adsorption is highly dependent on both ionic strength and pc H+. The sorption curve for the 4 M NaClO 4 condition is generally similar in shape to the 2 M ionic strength curve but the magnitude of adsorption is significantly greater under the high ionic strength condition, except at low pc H+. Neptunium (V) adsorption to Chromohalobacter sp. in 2 M NaClO 4 is essentially constant at approximately 15% from pc H to 3 and increases slightly with increasing pc H+ from approximately 15 to 22% from pc H+ 3 to 5; increases more sharply to approximately 63% at pc H+ 7.5; and decreases to approximately 28% at pc H Neptunium (V) adsorption to Chromohalobacter sp. in 4 M NaClO 4 gradually increases from approximately 15% to 89% from pc H+ 3 to 7.5; then decreases to approximately 48% at pc H Songkasiri et al. (2002) and Gorman-Lewis et al. (2005a) observed a % neptunium (V) adsorbed % neptunium (V) adsorbed 100 Ionic strength = 2 M hours 100 Ionic strength = 4 M hours Fig. 2. Neptunium (V) adsorption kinetics data with M neptunium (V) and 5 g/l (wet weight) Chromohalobacter sp. at approximately pc H+ 6 in 2 (top graph) and 4 (bottom graph) M NaClO 4. Error bars represent one standard deviation of at least three analyses of the same sample by the liquid scintillation counter. % neptunium (V) adsorbed L2--n L1--n pc H+ similar increase in neptunium (V) adsorption to Pseudomonas fluorescens and B. subtilis, respectively, with increasing pc H+ up to pc H+ 8. In contrast to the results reported herein, Deo et al. (2010) observed increasing neptunium (V) adsorption to Shewanella alga with increasing pc H+ from approximately pc H+ 2.5 to pc H+ 9. Because adsorption was not evaluated above pc H+ 9inDeo et al. s (2010) study, it is not known whether adsorption would decrease at more basic pc H+ in their study. However, Deo et al. (2010) did observe decreased adsorption to extracellular polymeric substances and cell wall fragments of S. alga with increasing pc H+ above a pc H+ of 9. The results reported herein also are in contrast to the ionic strength dependency observed by Gorman-Lewis et al. (2005a) which showed decreased neptunium (V) adsorption to B. subtilis with increasing ionic strength from to 0.5 M. The results of desorption experiments are depicted in Fig. 3. In general, the extent of adsorption after the initial adsorption step and after the desorption step for each neptunium-bacteria suspension pc H+ condition agrees well with the results for the pc H+ dependent adsorption experiments. The slightly higher extent of adsorption observed for the desorption experiment with pc H+ adjusted to 3.92 may indicate a small degree of irreversibility potentially due to neptunium (V) reduction at low pc H+ or slightly slower desorption kinetics at low pc H+. Gorman-Lewis et al. (2005a) attributed apparent irreversibility of neptunium (V) adsorption to non-halophilic bacteria at 0.1 M L3--n L3--cn1 L4--cn2 L4--cn3 Fig. 3. Experimental data for neptunium (V) adsorption onto Chromohalobacter sp. as a function of ph in 2 (open circles) and 4 (open triangles) M NaClO 4. Adsorption experiments were performed with M total neptunium (V) and 5 g/l (wet weight) bacteria. Solid curves represent calculated surface complexation models (see text for discussion). Solid circles represent the results of desorption experiments performed with M total neptunium (V) and 5 g/l (wet weight) bacteria in 2 M NaClO 4 (see text for discussion). Dashed curves represent model calculated speciation curves for neptunium (V)-bacterial surface species for the 2 M condition only: R-L 1 NpO x 2 (L1 n), R-L 2 NpO x 2 (L2 n), x x 2 R-L 3 NpO 2 (L3 n), R-L 3 NpO 2 CO 3 (L3 cn1), R-L 4 NpO 2 (CO 3 ) x 4 2 (L4 cn2), and R-L 4 NpO 2 (CO 3 ) x 6 3 (L4 cn3).
8 52 D.A. Ams et al. / Geochimica et Cosmochimica Acta 110 (2013) ionic strength at pc H+ less than 4 to the reduction of neptunium (V) to neptunium (IV) resulting in precipitation of NpO 2. However, Gorman-Lewis et al. (2005a) and Deo et al. (2010) also observed reversible neptunium (V) sorption to bacterial cell walls under similar experimental conditions in the slightly acidic to basic pc H+ range. Therefore, the results from the desorption experiments of this study indicate that the adsorption reaction is reversible within the timeframe and over the majority of the pc H+ range (pc H+ greater than 4) of the experiment. These results suggest that in the slightly acidic to basic pc H+ range the adsorption of neptunium (V) to bacterial surfaces under these experimental conditions is at equilibrium, that neptunium is not being reduced to neptunium (IV), and that neptunium (V) is not being transported through the bacterial cell wall Neptunium (V) adsorption surface complexation modeling A non-electrostatic surface complexation model that does not account for bulk aqueous ion activity corrections was used to model the neptunium adsorption data. The neptunium (V) adsorption data were modeled by testing likely reaction stoichiometries involving the adsorption of neptunium aqueous species (neptunyl: NpO + 2, hydroxyl: NpO 2 OH 0, NpO 2 (OH) 2, and carbonate: NpO 2 CO 3, NpO 2 (CO 3 ) 3 2, NpO 2 (CO 3 ) 5 3 ) to the four bacterial surface sites determined from bacteria titration modeling (Table 2). The models applied in this study assume a 1:1 complexation stoichiometry for the reactions describing neptunium (V) adsorption to bacterial surface functional groups. To simplify the modeling approach only the adsorption data in the pc H+ range less than approximately 8 were modeled initially, because the neptunyl ion is the only significant aqueous species in this pc H+ range. These results were then used to further constrain the model at pc H+ greater than approximately 8, where the aqueous speciation of neptunium (V) becomes more complex due to the formation of other aqueous neptunium (V) complexes. The neptunyl ion exhibits significant adsorption to Chromohalobacter sp. that is independent of pc H+ at pc H+ less than approximately 4.5 at 2 M ionic strength (Fig. 3). Invoking adsorption of the neptunyl ion onto the deprotonated form of either of the individual bacterial surface sites in models only including data at pc H+ less than 4.5 did not adequately account for the pc H+ independent sorption behavior, significantly under-predicting the extent of adsorption over most of the pc H+ range (Fig. SI-2). Models invoking neptunyl adsorption onto two or more of the deprotonated sites L1 through L4 did not converge. This is because the concentration of the deprotonated form of these sites is either too low (L x 1 3,L x 1 4 ) or changes significantly as a function of pc H+ (L x 1 1,L x 1 2 )atpc H+ less than 4.5. In order to account for the pc H+ independent adsorption data, it is necessary to invoke adsorption onto a surface site whose concentration is essentially constant at pc H+ less than 4.5. For instance, invoking neptunyl adsorption onto the protonated forms of sites L3 (L 3 H x ) and L4 (L 4 H x ), which exhibit high pk a values, can provide excellent model fits to the experimental data because their concentrations are essentially constant below pc H+ 4.5 (Fig. SI-2). It is also possible that the neptunyl ion adsorbs to a deprotonated surface site that exhibits a sufficiently low pk a such that the concentration of the deprotonated form of this site is essentially constant between pc H and 4.5. However, a surface site with such a low pk a could not be detected in this study because titration experiments could not be performed to very low pc H+ due to concerns with maintaining structural integrity of the cell wall in such acidic conditions. Thus, because the surface site speciation of the bacteria at pc H+ less than 4.5 is not well understood only the neptunium (V) adsorption data above pc H+ 4.5 was incorporated into the surface complexation model. The 4 M ionic strength neptunium (V) adsorption data do not exhibit pc H+ -independent adsorption behavior under low pc H+ conditions, but only two samples were collected below pc H+ 4 at this ionic strength, thus the low pc H+ behavior is not well constrained for the 4 M system. Because of this and for internal consistency between models, only the neptunium (V) adsorption data above pc H+ 4.5 was incorporated into the surface complexation model for the 4 M ionic strength data as well. From pc H+ approximately 4.5 to 8 the observed increase in neptunium (V) adsorption for both the 2 and 4 M ionic strength data sets coincides with the increase in concentration of the deprotonated forms of the L1, L2 and L3 bacterial surface sites. However, the extent of adsorption in this range of pc H+ could not be accounted for by invoking adsorption onto only one of these deprotonated sites (Fig. SI-3). Models invoking adsorption onto the deprotonated L1 site and either the deprotonated L2 or L3 site also significantly misfit the experimental data (Fig. SI-3). However, a model invoking neptunyl adsorption simultaneously onto the deprotonated L1, L2, and L3 surface sites provides an excellent fit to the experimental data in this pc H+ range for both ionic strength conditions (Fig. 3 and Fig. SI-3). The stoichiometry of this best-fit model is consistent with the dominant speciation of aqueous neptunium and the bacterial surface sites. Many studies have yielded similar best-fit surface complexation models invoking the adsorption of a single cationic metal species to the bacterial surface, where the extent of sorption is controlled by the successive deprotonation of bacterial surface sites with increasing pc H+ (e.g., Fein et al., 1997; Yee and Fein, 2001; Gorman-Lewis et al., 2005b). Further, Gorman-Lewis et al. (2005a) and Deo et al. (2010) also showed that invoking adsorption of the neptunyl ion onto deprotonated mid to low pk a bacterial surface sites under low ionic strength conditions provided the best model fit to their experimental data collected over a pc H+ range of 2.5 to 8 or 9, respectively. The log K values for the neptunyl- L 1 x 1, neptunyl-l 2 x 1, and neptunyl-l 3 x 1 complex for the 2 and 4 M ionic strength conditions are presented as reactions (1) through (3) in Table 3. Uncertainties for each K value were determined using predictive models to test the ability of a range of K values to fit approximately 95% of the adsorption data within the portion of the adsorption curve corresponding to the proton active pc H+ range of each site.
9 D.A. Ams et al. / Geochimica et Cosmochimica Acta 110 (2013) Table 3 Calculated neptunium (V) binding constants. Reaction 1 NpO R-L 1 x 1 M R-L 1 NpO 2 x 2 NpO R-L 2 x 1 M R-L 2 NpO 2 x 3 NpO R-L 3 x 1 M R-L 3 NpO 2 x 4 NpO 2 CO 3 + R-L 3 x 1 M R-L 3 NpO 2 CO 3 x 2 5 NpO 2 (CO 3 ) R-L 4 x 1 M R-L 4 NpO 2 (CO 3 ) 2 x 4 6 NpO 2 (CO 3 ) R-L 4 x 1 M R-L 4 NpO 2 (CO 3 ) 3 x 6 logk a I =2M I =4M / / / / / / / / / / / / 0.13 a Calculated with FITEQL based on equation 6 in main text, K = [R-L n Np(V) m+x 1 ]/a Np(V)m [R-L n x 1 ]. At pc H+ greater than 8, neptunyl-carbonate complexes dominate the aqueous speciation of neptunium (V) under the conditions of this study (Fig. SI-4), resulting in a competition between carbonate and the bacterial surface for complexation with the neptunyl ion consequently decreasing total neptunium (V) adsorption as pc H+ increases. However, predictive models for both the 2 and 4 M ionic strength conditions invoking only reactions (1 3) and their associated binding constants in Table 3 underpredict the extent of adsorption observed at pc H+ greater than approximately 8 (Fig. 4), indicating that another adsorption reaction is responsible for the observed adsorption behavior above pc H+ 8. Models including a fourth reaction, while % neptunium (V) adsorbed pc H+ Fig. 4. Experimental data for neptunium (V) adsorption onto Chromohalobacter sp. as a function of ph in 2 (open circles) and 4 (open triangles) M NaClO 4. Adsorption experiments were performed with M total neptunium (V) and 5 g/l (wet weight) bacteria. Solid curves represent predictive surface complexation models for both the 2 and 4 M ionic strength conditions invoking only reactions 1 3 in Table 3 and using the associated binding constants calculated for the pc H+ less than 8 adsorption data. keeping the binding constants for reactions (1 3) fixed, invoking the adsorption of the neptunyl ion onto the deprotonated L4 surface site, which becomes increasingly dominant with pc H+ in the basic pc H+ range, also underpredict the adsorption behavior at pc H+ greater than approximately 8. This is likely due to the scarcity of uncomplexed neptunyl ion under these conditions. Because models invoking the adsorption of only the neptunyl ion to the bacterial surface sites underpredict adsorption at high pc H+, this suggests that other neptunium (V) complexes may also adsorb to the cells in this pc H+ range. Keeping the calculated binding constants for reactions (1 3) in Table 3 fixed, the ability of models invoking the adsorption of neptunium (V)-carbonate complexes to deprotonated bacterial surface sites to account for the pc H+ greater than 8 data was evaluated. Models including reactions invoking the adsorption of either one or a combination of two of the neptunium (V) carbonate species NpO 2 CO 3, NpO 2 (CO 3 ) 2 3, and NpO 2 (- CO 3 ) 3 5 to one or a combination of the deprotonated surface sites L1 through L4 still significantly misfit the adsorption data at high pc H+ (Fig. SI-5) or did not converge. Only models including reactions invoking the adsorption of all three neptunium (V) carbonate species onto the bacterial surface sites provide reasonable fits to the experimental data at pc H+ greater than 8 for both the 2 and 4 M ionic strength conditions. Different models invoking the adsorption of the three neptunium carbonate complexes onto different combinations of the deprotonated L3 and L4 bacterial surface sites provide the best and equally excellent fits to the 2 and 4 M adsorption data sets. However, a model including reactions invoking the adsorption of NpO 2 CO 3 to the deprotonated L3 site and NpO 2 (- CO 3 ) 2 3 and NpO 2 (CO 3 ) 3 5 to the deprotonated L4 site not only provides an excellent fit to the 2 and 4 M data (Fig. 3), but is also consistent with the speciation of aqueous neptunium (V) as a function of pc H+ and with the deprotonation behavior of sites on the bacterial surface. The logk values for the R-L 3 NpO 2 CO 3 x 2, R-L 4 NpO 2 (CO 3 ) 2 x 4, and R-L 4 NpO 2 (CO 3 ) 3 x 6 complexes for the 2 and 4 M ionic strength conditions are presented as reactions (4 6) in Table 3. In some cases, inclusion of reactions
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