Abstract
The potentially toxic effects of soluble lanthanide (L) ions, although microbially induced mineralization can facilitate the formation of tractable materials, has been one factor preventing the more widespread use of L-ions in biotechnology. Here, we propose a new mixed-L precursor method as compared to the traditional direct addition technique. L (Nd, Gd, Tb, Ho and Er)-substituted magnetites, L y Fe3 − y O4 were microbially produced using L-mixed precursors, L x Fe1 − x OOH, where x = 0.01–0.2. By combining lanthanides into the akaganeite precursor phase, we were able to mitigate some of the toxicity, enabling the microbial formation of L-substituted magnetites using a metal reducing bacterium, Thermoanaerobacter sp. TOR-39. The employment of L-mixed precursors enabled the microbial formation of L-substituted magnetite, nominal composition up to L0.06Fe2.94O4, with at least tenfold higher L-concentration than could be obtained when the lanthanides were added as soluble salts. This mixed-precursor method can be used to extend the application of microbially produced L-substituted magnetite, while also mitigating their toxicity.
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Ainsworth CC, Pilon JL, Gassman PL, van der Sluys WG (1994) Cobalt, cadmium, and lead sorption to hydrous iron oxides. Soil Sci Soc Am J 58:1615–1623
Ardizzone S, Formaro L, Sivieri E (1983) Preparation and characterization of magnetic samples having different stoichiometric compositions. J Chem Soc Faraday Trans 1:2449–2456
Bhosale DN, Suryavanshi SS, Sawant SR, Sankpal AM, Kakatkar SV, Patil SA, Khasbardar BV (1993) Bulk magnetic studies on CoxZn1−xFe2O4 substituted with Al and Gd2O3. J Magn Magn Mater 124:298–300
Bokorny T (1894) Toxicologische Notizen über einige Verbindungen des Teller, Wolfram, Cer, Thorium. Chemiker-Zeitung 18:1739
Bousserhine N, Gasser UG, Jeanroy E, Berthelin J (1999) Bacterial and chemical reductive dissolution of Mn-, Co-, Cr-, and Al-substituted goethites. Geomicrobiol J 16(3):245–259
Cabuil V, Charles S, Massart R (1996) Physico-chemistry of magnetic fluids: preparation and properties. In: Berkovski B, Bashtovoy (Eds) Magnetic fluids and applications handbook. Begell House, Inc., New York, pp 3–33
Cooper DC, Picardal F, Rivera J, Talbot C (2000) Zinc immobilization and magnetite formation via ferric oxide reduction by Shewanella putrefaciens 200. Environ Sci Technol 34(1):100–106
Cornell RM, Giovanoli R (1989) Effect of cobalt on the formation of crystalline iron oxides from ferrihydrite in alkaline media. Clays Clay Miner 37:65–70
Drossbach GP (1897) Über den Einfluss der Elemente der cen- und zircongruppe auf das Wachstum von Bakterien. Zentralbl Bakteriol Parasitenk Abt I Orig 21:57–58
Evans CH (1996) Episodes from the history of the rare earth elements. Kluwer, Dordrecht
Ford RG, Bertsch PM, Farley KJ (1997) Changes in transition and heavy metal partitioning during hydrous iron oxide aging. Environ Sci Technol 31(7):2028–2033
Fredrickson JK, Zachara JM, Kukkadapu RK, Gorby YA, Smith SC, Brown CF (2001) Biotransformation of Ni-substituted hydrous ferric oxide by an Fe(III)-reducing bacterium. Environ Sci Technol 35(4):703–712
Holligan DL, Gillies GT, Dailey JP (2003) Magnetic guidance of ferrofluidic nanoparticles in an in vitro model of intraocular retinal repair. Nanobiotech 14:661–666
Hyeon T (2003) Chemical synthesis of magnetic nanoparticles. Chem Commun 8:927–934
Karthikeyan G, Mohanraj K, Elango K, Girishkumar K (2004) Synthesis, spectroscopic characterization and antibacterial activity of lanthanide–tetracycline complexes. Trans Metal Chem 29:86–80
Kolekar CB, Lipare AY, Ladgaonkar BP, Vasambekar PN, Vaingankar AS (2002) The effect of Gd3+ and Cd2+ substitution on magnetization of copper ferrite. J Magn Magn Mater 247(2):142–146
Larson AC, von Dreele RB (2000) General structure analysis system. Report LAUR. Los Alamos National Laboratory, Los Alamos, NM 86-748
Liu S, Zhou J, Zhang C, Cole DR, Gajdarziska M, Phelps TJ (1997) Thermophilic Fe(III)-reducing bacteria from the deep subsurface: the evolutionary implication. Science 277:1106–1109
Liu CX, Gorby YA, Zachara JM, Fedrickson JK, Brown CF (2002) Reduction kinetics of Fe(III), Co(III), U(VI), Cr(VI), and Tc(VII) in cultures of dissimilatory metal-reducing bacteria. Biotechnol Bioeng 80(6):637–649
Lizon C, Fritsch P (1999) Chemical toxicity of some actinides and lanthanides towards alveolar macrophages: an in vitro study. Int J Radiat Biol 75(11):1459–1471
Love LJ, Jansen JF, McKnight TE, Roh Y, Phelps TJ (2004) A magnetocaloric pump for microfluidic application. IEEE Trans Nanobioscience 3(2):101–110
Love LJ, Jansen JF, McKnight TE, Roh Y, Phelps TJ, Yeary LW, Cunningham GT (2005) Ferrofluid field induced flow for microfluidic application. IEEE Trans Mechatron 3(2):101–110
Lovley DR (1995) Bioremediation of organic and metal contaminants with dissimilatory metal reduction. J Ind Microbiol 14:85–93
Martínez CE, McBride MB (1998a) Coprecipitates of Cd, Cu, Pb and Zn in iron oxides: solid phase transformation and metal solubility after aging and thermal treatment. Clays Clay Miner 46(5):537–545
Martínez CE, McBride MB (1998b) Solubility of Cd2+, Cu2+, Pb2+, and Zn2+ in aged coprecipitates with amorphous iron hydroxides. Environ Sci Technol 32(6):743–748
McLaughlin JR, Ryden JC, Syers JK (1981) Sorption of inorganic phosphate by iron- and aluminum-containing components. J Soil Sci 32:365–377
Moon J-W, Roh Y, Lauf RJ, Vali H, Yeary LW, Phelps TJ (2007a) Microbial preparation of metal-substituted magnetite nanoparticles. J Microbiol Methods 70:150–158
Moon J-W, Yeary LW, Rondinone AJ, Rawn CJ, Kirkham MJ, Roh Y., Love LJ, Phelps TJ (2007b) Magnetic response of microbially synthesized transition metal- and lanthanide-substituted nano-sized magnetites. J Magn Magn Mater 313(2):283–292
Palasz A, Czekaj P (2000) Toxicological and cytophysiological aspects of lanthanides action. Acta Niochimica Polonica 47(4):1107–1114
Rezlescu E, Rezlescu N, Pasnicu C, Craus ML, Popa PD (1996) Effects of rare-earth ions on the quality of a Li–Zn ferrite. Cryst Res Technol 31(3):343–352
Roh Y, Lauf RJ, McMillan AD, Zhang C, Rawn CJ, Bai J, Phelps TJ (2001) Microbial synthesis and the characterization of metal-substituted magnetites. Solid State Commun 118:529–534
Roh Y, Liu S, Li G, Huang H, Phelps TJ, Zhou J (2002) Isolation and characterization of metal-reducing Thermoanaerobacter strains from deep subsurface environments of the Piceance Basin, Colorado. Appl Environ Microbiol 68(12):6013–6020
Roh Y, Zhang C-L, Vali H, Lauf RJ, Zhou J, Phelps TJ (2003) Biogeochemical and environmental factors in Fe biomineralization: magnetite and siderite formation. Clays Clay Miner 51(1):83–95
Roh Y, Gao H, Vali H, Kennedy DW, Yang ZK, Gao W, Dohnalkova AC, Stapleton RD, Moon J-W, Phelps TJ, Fredrickson JK, Zhou J (2006) Metal reduction and iron biomineralization by a psychrotolerant Fe(III)-reducing bacterium, Shewanella sp strain PV-4. Appl Environ Microbiol 72(5):3236–3244
Shannon RD (1976) Revised effective ionic radii and systematic studies of interatomic distances in halides and chalcogenides. Acta Cryst 32:751
Sidhu PS (1988) Transformation of trace element-substituted maghemite to hematite. Clays Clay Miner 36(1):31–38
Slobodkin AI, Wiegel J (1997) Fe(III) as an electron acceptor for H2 oxidation in thermophilic anaerobic enrichment cultures from geothermal areas. Extremophiles 1:106–109
Slobodkin AI, Eroshchev-Shak VA, Kostrikina NA, Lavrushin VY, Dainyak LG, Zavarzin GA (1995) Formation of magnetite by thermophilic anaerobic microorganisms. Dokl Akad Nauk 345(5):694–697
Toby BH (2001) EXPGUI, a graphical user interface for GSAS. J Appl Cryst 34:210–213
Wielinga B, Mizuba MM, Hansel CM, Fendorf S (2001) Iron promoted reduction of chromate by dissimilatory iron-reducing bacteria. Environ Sci Technol 35:522–527
Yeary LW (2005) Curie temperature modification of mixed-metal ferrites by doping of rare earth metals for use in magnetocaloric pumping applications. Ms Thesis. Tennessee Technol Univ
Zhang C, Liu SV, Logan J, Mazumder R, Phelps TJ (1996) Enhancement of Fe(III), Co(III), and Cr(VI) reduction at elevated temperatures and by a thermophilic bacterium. Appl Biochem Biotechnol 57/58:923–932
Zhang C, Liu S, Phelps TJ, Cole DR, Horita J, Fortier SM, Elless MP, Valley JW (1997) Physiochemical, mineralogical and isotopic characterization of magnetite-rich iron oxides formed by thermophilic iron reducing bacteria. Geochim Cosmochim Acta 61:4621-4632
Zhang C, Vali H, Romanek CS, Phelps TJ, Liu S (1998) Formation of single-domain magnetite by a thermophilic bacterium. Am Miner 83:1409–1418
Acknowledgments
This research was supported by the Defense Advanced Research Projects Agency (DARPA) Biomagnetics Program under Contract 1868-HH43-X1 and the US Department of Energy’s (DOE) Office of Fossil Energy with student support provided by the DOE Environmental Molecular Science Initiative. ORNL is managed by UT-Battelle, LLC, for the U.S. DOE under Contract DE-AC05-00OR22725. We thank Dr. Scott Brooks for help with thermodynamic software, Ms. Meghan McNeilly for editing, Ms. Shannon Ulrich for protein assays, Ms. Lisa Fagan for cell counting and Mr. Kenneth A. Lowe for ICP-MS analysis. J.-W. Moon is supported by the Post-doctoral Fellowship Program of Korea Science and Engineering Foundation and in part by an appointment to the ORNL Postdoctoral Research Associates Program administered jointly by the Oak Ridge Institute for Science and Education and ORNL.
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Moon, JW., Roh, Y., Yeary, L.W. et al. Microbial formation of lanthanide-substituted magnetites by Thermoanaerobacter sp. TOR-39. Extremophiles 11, 859–867 (2007). https://doi.org/10.1007/s00792-007-0102-1
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DOI: https://doi.org/10.1007/s00792-007-0102-1