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Bioaccumulation of nickel by intercalation into polycrystalline hydrogen uranyl phosphate deposited via an enzymatic mechanism

Abstract

A Citrobacter sp. accumulates uranyl ion (UO22+) as crystalline HUO2PO4 · 4H2O (HUP), using enzymati-cally generated inorganic phosphate. Ni was not removed by this mechanism, but cells already loaded with HUP removed Ni2+ by intercalative ion-exchange, forming Ni(UO2PO4)2 · 7H2O, as concluded by x-ray diffraction (XRD) and proton induced x-ray emission (PIXE) analyses. The loaded biomass became saturated with Ni rapidly, with a molar ratio of Ni:U in the cellbound deposit of approx. 1:6; Ni penetration was probably surface-localized. Cochallenge of the cells with Ni2+ and UO22+, and glycerol 2-phosphate (phosphate donor for phosphate release and metal bioprecipitation) gave sustained removal of both metals in a flow through bioreactor, with more extensively accumulated Ni. We propose ‘Microbially Enhanced Chemisorption of Heavy Metals’ (MECHM) to describe this hybrid mechanism of metal bioaccu-mulation via intercalation into preformed, biogenic crystals, and note also that MECHM can promote the removal of the transuranic radionuclide neptunium, which is difficult to achieve by conventional methods.

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References

  1. Macaskie, L.E., Empson, R.M., Cheetham, A.K., Grey, C.P. and Skarnulis, A.J. 1992. Uranium bioaccumulation by a Citrobacter sp. as a result of enzymically-mediated growth of polycrystalline HUO2PO4. Science 257: 782–784.

    Article  CAS  Google Scholar 

  2. Macaskie, L.E., Bonthrone, K.M. and Rouch, D.A. 1994. Phosphatase-mediated heavy metal accumulation by a Citrobacter sp. and related enterobacteria. FEMS Microbiol. Lett. 121: 141–146.

    Article  CAS  Google Scholar 

  3. Macaskie, L.E. and Dean, A.C.R. 1982. Cadmium accumulation by micro-organisms. Environ. Technol. Lett. 3: 49–56.

    Article  CAS  Google Scholar 

  4. Macaskie, L.E. 1990. An immobilized cell bioprocess for the removal of heavy metals from aqueous flows. J. Chem. Technol. Biotechnol. 49: 357–379.

    Article  CAS  Google Scholar 

  5. Clark, P.J., Shama, G. and Streat, M. 1992. in Bioprecipitation of metals from wastewaters. Inst. Chem. Eng. Res. Event, UMIST, UK. pp. 308–311.

    Google Scholar 

  6. Macaskie, L.E., Jeong, B.C. and Tolley, M.R. 1994. Enzymically-accelerated biomineralization of heavy metals: application to the removal of americium and plutonium from aqueous flows. FEMS Microbiol. Rev. 14: 351–368.

    Article  CAS  Google Scholar 

  7. Macaskie, L.E., Empson, R.M., Lin, F. and Tolley, M.R. 1995. Enzymatically-mediated uranium accumulation and uranium recovery using a Citrobacter sp. immobilized as a biofilm within a plug-flow reactor. J. Chem. Technol. Biotechnol. 63: 1–16.

    Article  CAS  Google Scholar 

  8. Sittig, M. (ed.). 1975. in Environmental Sources and Emissions Handbook. Noyes Data Corp, New Jersey. p. 97.

    Google Scholar 

  9. Macaskie, L.E. 1991. The application of biotechnology to the treatment of wastes produced from the nuclear fuel cycle: biodegradation and bioaccumulation as a means of treating radbnuclide-contaminated streams. CRC Grit. Rev. in Biotechnol. 11: 41–112.

    Article  CAS  Google Scholar 

  10. Patterson, J.W. 1985. in Industrial Wastewater Treatment Technology. Butterworth, Boston. p. 217.

    Google Scholar 

  11. Bhattacharyya, D. and Cheng, C.Y.R. 1987. Activated carbon adsorption of heavy metal chelates from single and multicomponent systems. Envir. Prog. 6: 110–118.

    Article  CAS  Google Scholar 

  12. Zouboulis, A.I. and Kydros, K.A. 1993. Use of red mud for toxic metals removal—the case of nickel. J. Chem. Technol. Biotechnol. 58: 95–101.

    Article  CAS  Google Scholar 

  13. Corder, S. and Reeves, M. 1994. Biosorption of nickel in complex aqueous waste streams by Cyanobacteria. Appl. Biochem. Biotechnol. 45/46: 847–859.

    Article  Google Scholar 

  14. Volesky, B. (ed.). 1991. Biosorption of Heavy Metals. CRC Press, Boca Raton, USA.

    Google Scholar 

  15. Tsezos, M., Remoudaki, E. and Agelatou, V. 1995. A systematic study on equilibrium and kinetics of biosorptive accumulation.The case of Ag and Ni. Int. Biodeterior. Biodegr. 35: 129–154.

    Article  CAS  Google Scholar 

  16. Kumar, C.H.S., Sastry, K.S. and Mohan, P.M. 1992. Use of wildtype and nickel resistant Neurospora crassafor removal of Ni2+ from aqueos medium. Biotechnol. Lett. 14: 1099–1202.

    Article  CAS  Google Scholar 

  17. Diels, L., Van Roy, S., Taghavi, S., Doyen, W., Leysen, R. and Mergeay, M. 1993. The use of Alcaligenes eurotrphus immobilized in a tubular membrane reactor for heavy metal recuperation, in Biohydrometallurgicat Technologies. Torma, A. E. et al. (eds.). Proc. Int. Symp. Biohydrometallurgy, Jackson Hole, Wyoming, August 1993. The Minerals, Metals and Materials Society, USA. pp. 133–144.

    Google Scholar 

  18. Macaskie, L.E., Hewitt, C.J., Shearer, J.A. and Kent, C.A. 1995. Biomass production for the removal of heavy metals from aqueous solution at low pH using growth-decoupled cells of a Citrobacter sp. Int. Biodeter. Biodegr. 35: 73–92.

    Article  CAS  Google Scholar 

  19. Dean, J.A. (ed.). 1992. Lange's Handbook of Chemistry, 14th ed. McGraw-Hill, New York.

    Google Scholar 

  20. Good, N.G., Winget, G.D., Winter, W., Connolly, T.N., Izawa, S. and Singh, R.M.M. 1966. Hydrogen ion buffers for biological research. Biochemistry 5: 467–477.

    Article  CAS  Google Scholar 

  21. Baes, C.F. and Mesmer, R.E. 1976. The Hydrolysis of Cations. Wiley, New York.

    Google Scholar 

  22. Fu-Sheng, W., Pei-Hua, Q., Nai-Kui, S. and Fang, Y. 1989. Sensitive spectrophotometric determination of nickel(ll) with 2-(5-bromo-2-pyridylazo)-5-diethylaminophenol. Talanta 28: 189–191.

    Article  Google Scholar 

  23. Torrance, K. 1984. Determination of ionic nickel and cobalt in simulated PWR coolant by differential-pulse polarography. Analyst 109: 1035–1038.

    Article  CAS  Google Scholar 

  24. Hughes, M.N. and Poole, R.K. 1991. Metal speciation and microbial growth—the hard (and soft) facts. J. Gen. Microbiol. 137: 725–734.

    Article  CAS  Google Scholar 

  25. Morosin, B. 1978. Hydrogen uranyl phosphate tetrahydrate, a hydrogen solid electrolyte. Acta Cryst. 634: 3732–3734.

    Article  Google Scholar 

  26. Hunsberger, L.R. and Ellis, A.B. 1990. Excited-state properties of lamellar solids derived from metal complexes and hydrogen uranyl phosphate. Coord. Chem. Rev. 97: 209–224.

    Article  CAS  Google Scholar 

  27. Pozas-Torma, R., Moreno-Real, L., Martinez-Lara, M. and Bruque-Gamez, S. 1986. Layered metal phosphates, retention of divalent ions by amine intercalates of uranyl phosphates. Can. J. Chem. 64: 30–34.

    Article  Google Scholar 

  28. Pozas-Torma, R., Bruque-Gamez, S., Martinez-Lara, M. and Moreno-Real, L. 1988. Interlayer ammine complexes of metal uranyl phosphate. Can. J. Chem. 66: 2849–2854.

    Article  Google Scholar 

  29. Powder diffraction file Card No. 29-670,1992. JCPDS, Swarthmore, PA.

  30. Powder diffraction file Card No. 35-317,1992. JCPDS, Swarthmore, PA.

  31. A part of the DIFFRAC-AT V3.2 program written by SOCABIM for SEAMMAN, June 1993.

  32. Grime, G.W., Dawson, M., Marsh, M., McArthur, I.C. and Watt, F., 1991. Oxford submicron nuclear microscopy facility. Nucl. Inst. Meth. 854: 52–63.

    Article  Google Scholar 

  33. Johannson, S.A.E. and Campbell, J.L. 1988. PIXE—a Novel Technique for Elemental Analysis. Wiley, Chichester, U.K.

    Google Scholar 

  34. Watt, F. and Grime, G. (eds.). 1989. Principles and Applications of High Energy Ion Microbeams. Hilger, Bristol, U.K.

    Google Scholar 

  35. Tamana, H., Griddle, A., Grime, G.W., Vaughan, D. and Spratt, J. 1994. Trace elements in platinum group minerals studied using nuclear microscopy. Nucl. Instr. Meth. 89: 213–218.

    Article  CAS  Google Scholar 

  36. Langford, J.I. 1973. The accuracy of cell dimensions determined by Cohen's method of least squares and the systematic indexing of powder data. J. Appl. Cryst 6: 190–196.

    Article  CAS  Google Scholar 

  37. Langford, J.I. 1971. Powder pattern programs. J. Appl. Cryst. 4: 259–260.

    Article  CAS  Google Scholar 

  38. Tolley, M.R. and Macaskie, L.E. 1971. Metal removal from aqueous solutions. Patent application pet No. GB94/00626.

  39. Tolley, M.R. 1993. The biological treatment of liquid wastes containing heavy metals. D. Phil Thesis, University of Oxford, U.K.

  40. Rosenthal, G.L. and Ellis, A.B. 1988. Structural and photoluminescent properties of fully-hydrated lanthanon uranyl phosphates. J. Less Comm. Met. 139: 299–304.

    Article  CAS  Google Scholar 

  41. Dorhout, P.K., Kissane, R.J., Abney, K.D., Eller, R.G., and Ellis, A.B. 1989. Intercalation reactions of the neptunyl (VI) dication with hydrogen uranyl phosphate and hydrogen neptunyl phosphate host lattices. Inorg. Chem. 28: 2926–2930.

    Article  CAS  Google Scholar 

  42. Tolley, M.R., Strachan, L.F. and Macaskie, L.E. 1995. Lanthanum accumulation from acidic solutions using a Citrobacter sp. immobilized in a flow-through reactor. J. Ind. Microbiol. 14: 271–280.

    Article  CAS  Google Scholar 

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Bonthrone, K., Basnakova, G., Lin, F. et al. Bioaccumulation of nickel by intercalation into polycrystalline hydrogen uranyl phosphate deposited via an enzymatic mechanism. Nat Biotechnol 14, 635–638 (1996). https://doi.org/10.1038/nbt0596-635

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