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Adsorption of Rare Earth Elements Onto Bacterial Cell Walls and Its Implication for REE Sorption Onto Natural Microbial Mats

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Adsorption of Rare Earth Elements Onto Bacterial Cell Walls and Its Implication for REE Sorption Onto Natural Microbial Mats Chemical Geology 219 (2005) 53–67 www.elsevier.com/locate/chemgeo Adsorption of rare earth elements onto bacterial cell walls and its implication for REE sorption onto natural microbial mats Yoshio Takahashia,b,T, Xavier Chaˆtellierc, Keiko H. Hattorid, Kenji Katoe, Danielle Fortind aDepartment of Earth and Planetary Systems Science, Hiroshima University, Hiroshima 739-8526, Japan bLaboratory for Multiple Isotope Research for Astro- and Geochemical Evolution (MIRAGE), Hiroshima University, Hiroshima 739-8526, Japan cGe´osciences Rennes, CNRS, Rennes, F-35042 Rennes Cedex, France dDepartment of Earth Sciences, University of Ottawa, Ottawa, ON, K1N 6N5, Canada eDepartment of Biology and Geosciences, Faculty of Science, Shizuoka University, Shizuoka 422-8529, Japan Received 8 May 2004; received in revised form 7 January 2005; accepted 15 February 2005 Abstract Adsorption of rare earth elements (REE) onto the cell walls of Bacillus subtilis (a gram-positive bacterium) and Escherichia coli (a gram-negative bacterium) was studied between pH 2.5 and 4.5 and at various bacterial concentrations. The distribution coefficients of REE between the bacterial cell surface and water showed a pattern with a prominent enrichment of heavy REE (HREE), including a maximum around Sm and Eu. There was also an enrichment around Pr accompanied by a decline for Nd, which was attributed to the tetrad effect. The occurrence of M-type tetrad effect suggests that REE form inner sphere complexes during their adsorption onto bacteria. The enrichment of the distribution coefficients in the HREE region was more enhanced at higher bacterial concentrations, which could not be explained by one type of binding sites on the bacterial surface. Instead, the data are consistent with two ligand types for the sorption of REE. The pattern of bacterial distribution coefficients can be explained by the stability constants of REE with carboxylate and phosphate groups, suggesting that they are most likely responsible for the adsorption of REE on the bacterial cell surface. Microbial mats and thermal waters at the Nakafusa hot spring (Nagano Prefecture, Japan) were also examined to evaluate whether the REE patterns of natural samples could be used as indicators of the presence of bacteria. The apparent distribution coefficients of REE displayed a pattern similar to that obtained in the laboratory experiments using pure bacterial strains. The results suggest that the REE pattern of chemical sedimentary rocks may be used to identify the bacterial contribution to the deposition of the rocks in the geological record. D 2005 Elsevier B.V. All rights reserved. Keywords: Rare earth elements; Bacteria; Cell walls; Adsorption; Microbial mat T Corresponding author. Department of Earth and Planetary Systems Science, Hiroshima University, Hiroshima 739-8526, Japan. Tel.: +81 82 4247460; fax: +81 82 4240735. E-mail address: [email protected] (Y. Takahashi). 0009-2541/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.chemgeo.2005.02.009 54 Y. Takahashi et al. / Chemical Geology 219 (2005) 53–67 1. Introduction Daughney and Fein, 1998; Daughney et al., 2001; Kelly et al., 2002; Markai et al., 2003; Boyanov et Rare earth elements (REE; including Y in this al., 2003). The binding functional groups on the paper) commonly behave coherently in nature, but a bacterial cell walls were evaluated by comparing the variety of processes can cause fractionation (e.g., distribution coefficients for bacteria and the stability Henderson, 1984; Taylor and McLennan, 1988). The constants of REE complexes with a variety of fractionation pattern of REE, commonly expressed as organic ligands based on the linear free energy normalized values on a logarithmic scale, provides relationship of complex formation between solute information related to the origin of the samples and to complex and corresponding surface complex (Stumm, the process leading to their formation. Furthermore, 1992). Such an approach has been adopted by Byrne the study of REE is relevant to the dispersion of and Kim (1990) to evaluate the influence of REE elements from radioactive waste sites because acti- complexation with organic ligands at the surface of nides, especially Am (III) and Cm (III), have similar particulate matter in marine systems. The nature of geochemical properties as REE (e.g., Brookins, the adsorption sites onto bacterial cell walls is still a 1984). relatively open question for any cations including The concentrations of REE in natural waters are REE. Although spectroscopic analyses such as laser- influenced by their adsorption onto inorganic and induced fluorescence (Ozaki et al., 2002; Markai et organic substances and soluble complex formation al., 2003) and EXAFS (Kelly et al., 2002; Boyanov with a variety of ligands (e.g., Erel and Stopler, 1993; et al., 2003) have been performed, there are still Sholkovitz et al., 1994; Ingri et al., 2000; Tanizaki et some discrepancies between the conceptual models al., 1992; Takahashi et al., 1997). It is likely that the proposed by the various studies (Boyanov et al., biota in natural systems can also affect the behavior of 2003; Chaˆtellier and Fortin, 2004). It is possible that REE. For instance, bacteria, which have a very high the REE patterns can give new insight into the surface area per unit weight due to their small size, are nature of the adsorption sites. known to efficiently adsorb various dissolved metal The laboratory data for the REE sorption are ions (Beveridge and Murray, 1980; Beveridge and compared to those from natural microbial mat samples Doyle, 1989; Fein et al., 1997; Daughney and Fein, from the Nakafusa hot spring in the Nagano Pre- 1998; Martinez et al., 2002; Chaˆtellier and Fortin, fecture, Japan. These mats are ideal for the examina- 2004). Some studies have looked at the sorption of tion of the role of bacteria on REE fractionation selected REE onto bacterial cells (Ferris and Bever- because the hot spring does not contain Fe- and Mn- idge, 1984; Mullen et al., 1989; Texier et al., 2000; oxyhydroxides, which adsorb large quantities of REE Ozaki et al., 2002; Merroun et al., 2003; Markai et al., (Koeppenkastrop and De Carlo, 1992; Kawabe et al., 2003), but they did not include the data for all REE. 1999a,b). Brantley et al. (2001) reported uptake of all REE by a soil bacterium, but the distribution of REE between the bacterial and aqueous phases was not reported due 2. Samples and experimental methods to the low concentrations of dissolved REE at equilibrium. To our knowledge, there are still few 2.1. Bacterial suspensions adsorption data of all REE onto pure bacterial cells and thus no clear understanding of the potential role The bacterial suspensions were prepared as of bacteria on REE fractionation processes. described in Chaˆtellier et al. (2001) and Daughney This paper reports for the first time the patterns of and Fein (1998). B. subtilis cells were cultivated in REE adsorbed onto Bacillus subtilis (B. subtilis), a Tryptic soy broth (Difco, 30 g/L) with yeast extract gram-positive bacterium, and Escherichia coli (Difco, 5.0 g/L). Pre-culture tubes of 3 mL were first (E.coli), a gram-negative bacterium. These two inoculated from a Petri dish and incubated at 37 8C for bacteria are commonly found in the environment 24 h. Then, 4 Erlenmeyers containing 1 L of sterile and their cell wall properties are well characterized culture medium were inoculated with the pre-cultures (e.g., Beveridge and Doyle, 1989; Fortin et al., 1997; and grown for 7.5 h until exponential growth phase Y. Takahashi et al. / Chemical Geology 219 (2005) 53–67 55 was reached (Daughney and Fein, 1998). E. coli cells that the amount of REE sorbed on the containers and were grown in Tryptic soy broth (Difco, 30 g/L). A 50 filters in the experiments at pH below 6 was less than mL pre-culture was incubated for 24 h, and sub- 3% of the amount of REE initially added to the samples (10 mL) of this pre-culture were used to system, which is similar to the precision, F2%, of inoculate 4 Erlenmeyers containing 1 L of the culture ICP-MS measurements. medium. The bacteria were cultivated for 2.5 h and The filtrate was acidified with conc. HNO3 harvested in exponential phase. The bacteria were (TAMAPURE AA-100, Tama Chemicals Co., Ltd, separated from the growth media by centrifugation at Tokyo) to a final concentration of 2% for the 6000 rpm for 15 min, washed 5 times in 1.0 mM determination of the concentration of REE using an NaCl, left to rest overnight at 4 8C, and washed again inductively coupled plasma-mass spectrometer (ICP- twice in 1.0 mM NaCl before being used for the MS; Agilent 4500 or VG PQ-3). Indium and Bi were sorption experiments. The dry weight of the bacteria also added at a concentration of 10 Ag/L to serve as was determined by dehydrating the suspension (15 internal standards. The precision of the ICP-MS mL) in an oven at 60 8C. The optical density (at 600 measurement was better than 2%. The distribution nm) of the stock suspension diluted 100 times was coefficient (Kd) of REE between the bacterial and the also determined in order to estimate its concentration aqueous phases is defined as before use. ½REE init À ½REE fil KdðÞ¼L=g ð1Þ 2.2. REE sorption experiments on bacteria and c½REE fil inorganic compounds where [REE]fil is the concentration of REE in the All experiments were carried out in Teflon contain- filtrate, while [REE]init is the initial concentration of ers. An REE standard solution (Spex CertiPrep., dissolved REE (=100 Ag/L). The c (g/L) is the ratio of Edison, New Jersey) containing all REE elements, bacteria (dry weight) and water, which ranged from except Pm, at a concentration of 10.0 mg/L each was 0.067 g/L to 1.4 g/L.
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