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Photosynthesis Research

, Volume 118, Issue 1–2, pp 83–94 | Cite as

Insights into the interactions of cyanobacteria with uranium

  • Celin Acharya
  • Shree Kumar Apte
Review

Abstract

Due to various activities associated with nuclear industry, uranium is migrated to aquatic environments like groundwater, ponds or oceans. Uranium forms stable carbonate complexes in the oxic waters of pH 7–10 which results in a high degree of uranium mobility. Microorganisms employ various mechanisms which significantly influence the mobility and the speciation of uranium in aquatic environments. Uranyl bioremediation studies, this far, have generally focussed on low pH conditions and related to adsorption of positively charged UO2 2+ onto negatively charged microbial surfaces. Sequestration of anionic uranium species, i.e. [UO2(CO3) 2 2− ] and [UO2(CO3) 3 4− ] onto microbial surfaces has received only scant attention. Marine cyanobacteria are effective metal adsorbents and represent an important sink for metals in aquatic environment. This article addresses the cyanobacterial interactions with toxic metals in general while stressing on uranium. It focusses on the possible mechanisms employed by cyanobacteria to sequester uranium from aqueous solutions above circumneutral pH where negatively charged uranyl carbonate complexes dominate aqueous uranium speciation. The mechanisms demonstrated by cyanobacteria are important components of biogeochemical cycle of uranium and are useful for the development of appropriate strategies, either to recover or remediate uranium from the aquatic environments.

Keywords

Cyanobacteria Uranium Interaction mechanisms Bioremediation Biorecovery 

Notes

Acknowledgments

The authors thank Prof. L. Uma and Dr. N. Thajuddin, NFMC, Tiruchirapalli, India for providing S. elongatus strain BDU/75042. The authors thank Dr. Daisy Joseph, Nuclear Physics Division, BARC, for extending technical help in EDXRF analyses of uranium in cyanobacterial biomass samples.

References

  1. Abdelouas A, Lutze W, Nuttall E (1998) Chemical reactions of uranium in groundwater at a mill tailings site. J Contam Hydrol 34:343–361CrossRefGoogle Scholar
  2. Acharya C, Apte SK (2013) Novel surface associated polyphosphate bodies sequester uranium in the filamentous, marine cyanobacterium, Anabaena torulosa. Metallomics. doi: 10.1039/C3MT00139C PubMedGoogle Scholar
  3. Acharya C, Joseph D, Apte SK (2009) Uranium sequestration by marine cyanobacterium Synechococcus elongatus strain BDU/75042. Bioresour Technol 100:2176–2181PubMedCrossRefGoogle Scholar
  4. Acharya C, Chandwadkar P, Apte SK (2012) Interaction of uranium with a filamentous, heterocystous, nitrogen-fixing cyanobacterium Anabaena torulosa. Bioresour Technol 116:290–294PubMedCrossRefGoogle Scholar
  5. Acharya C, Chandwadkar P, Joseph D, Apte SK (2013) Uranium (VI) recovery from saline environment by a marine unicellular cyanobacterium. Synechococcus elongatus. J Radioanal Nucl Chem 295:845–850CrossRefGoogle Scholar
  6. Akhtar K, Akhtar MW, Khalid AM (2007) Removal and recovery of uranium from aqueous solutions by Trichoderma harzianum. Water Res 41:1366–1378PubMedCrossRefGoogle Scholar
  7. Aleissa KA, Shabana EI, Al-Masoud FIS (2004) Accumulation of uranium by filamentous green algae under natural environmental conditions. J Radioanal Nucl Chem 26:683–687CrossRefGoogle Scholar
  8. Appukuttan D, Rao AS, Apte SK (2006) Engineering of Deinococcus radiodurans R1 for bioprecipitation of uranium from dilute nuclear waste. Appl Environ Microbiol 72:7873–7878PubMedCrossRefGoogle Scholar
  9. Apte SK, Thomas J (1980) Sodium is required for nitrogenase activity in cyanobacteria. Curr Microbiol 3:291–293CrossRefGoogle Scholar
  10. Arnesano F, Banci L, Bertini I, Ciofi-Baffoni S, Molteni E, Huffman DL, O’Halloran TV (2002) Metallochaperones and metal-transporting ATPases: a comparative analysis of sequences and structures. Genome Res 12:255–271PubMedCrossRefGoogle Scholar
  11. Ashford AE, Lee ML, Chilvers GA (1975) Polyphosphate in eucalypt mycorrhizas: a cytochemical demonstration. New Phytol 74:447–453CrossRefGoogle Scholar
  12. Axelsen KB, Palmgren MG (1998) Evolution of substrate specificities in the P-type ATPase superfamily. J Mol Evol 46:84–101PubMedCrossRefGoogle Scholar
  13. Bayramoglu G, Çelik G, Arica MY (2006) Studies on accumulation of uranium by fungus Lentinus sajor-caju. J Hazard Mater 136:345–353PubMedCrossRefGoogle Scholar
  14. Bengtsson L, Johansson B, Hackett TJ, McHale L, McHale AP (1995) Studies on the biosorption of uranium by Talaromyces emersonii CBS 814.70 biomass. Appl Microbiol Biotechnol 42:807–811PubMedCrossRefGoogle Scholar
  15. Beveridge TJ (1981) Ultrastructure, chemistry, and function of the bacterial wall. Int Rev Cytol 72:229–317PubMedCrossRefGoogle Scholar
  16. Bhat SV, Melo JS, Chaugule BB, D’Souza SF (2008) Biosorption characteristics of Uranium (VI) from aqueous medium onto Catenella repens, a red alga. J Hazard Mater 158:628–635PubMedCrossRefGoogle Scholar
  17. Blindauer CA, Harrison MD, Robinson AK, Parkinson JA, Bowness PW, Sadler PJ, Robinson NJ (2002) Multiple bacteria encode metallothioneins and SmtA-like zinc fingers. Mol Microbiol 45:1421–1432PubMedCrossRefGoogle Scholar
  18. Brierley CL (1990) Metal immobilization using bacteria. In: Ehrlich HL, Brierley CL (eds) Microbial mineral recovery. McGraw-Hill Publishing Co, New York, pp 303–324Google Scholar
  19. Cavet JS, Borrelly GPM, Robinson NJ (2003) Zn, Cu and Co in cyanobacteria: selective control of metal availability. FEMS Microbiol Rev 27:165–181PubMedCrossRefGoogle Scholar
  20. Choppin GR (2007) Actinide speciation in the environment. J Radioanal Nucl Chem 273:695–703CrossRefGoogle Scholar
  21. Cologgi DL, Lampa-Pastirk S, Speers AM, Kelly SD, Reguera G (2011) Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism. Proc Natl Acad Sci USA. doi: 10.1073/pnas.1108616108 PubMedGoogle Scholar
  22. Cothern CR, Lappenbusch WL (1983) Occurrence of Uranium in drinking water of US. Health Phys 45:89–99PubMedCrossRefGoogle Scholar
  23. Daniels MJ, Turner-Cavet JS, Selkirk R, Sun H, Parkinson JA, Sadler PJ, Robinson NJ (1998) Coordination of Zn2+ and Cd2+ by prokaryotic metallothionein. J Biol Chem 273:22957–22961PubMedCrossRefGoogle Scholar
  24. Darnall DW, Greene B, Henzl MT, Hosea JM, McPherson RA (1986) Selective recovery of gold and other metal ions from an algal biomass. Environ Sci Technol 20:206–208PubMedCrossRefGoogle Scholar
  25. Davison BH, McKeown CK, Kuritz T, Barton JW (2001) Green biopolymer coatings for improved decontamination of metals from surfaces. 13th Annual Technical information exchange conference, Albuquerque, 11/13/2001–11/15/2001Google Scholar
  26. Driver CJ (1994) Ecotoxicity literature review of selected Hanford Site contaminants. US Department of Energy, Pacific Northwest Laboratory, PNL-9394, Richland, p 141Google Scholar
  27. Fein JB, Daughney CJ, Yee N, Davis TA (1997) A chemical equilibrium model for metal adsorption onto bacterial surfaces. Geochim Cosmochim Acta 61:3319–3328CrossRefGoogle Scholar
  28. Fogg GE, Westlake DF (1955) The importance of extracellular products of algae in freshwater. Verhlnt Ver Theor Angew Limnol 12:219–231Google Scholar
  29. Fogg GE, Stewart WDP, Fay P, Walsby AE (1973) The blue-green algae. Academic Press, LondonGoogle Scholar
  30. Fortin C, Denison FH, Garnier-Laplace J (2007) Metal–phytoplankton interactions: modeling the effect of competing ions (H+, Ca2+, and Mg2+) on uranium uptake. Environ Toxicol Chem 26:242–248PubMedCrossRefGoogle Scholar
  31. Fowle DA, Fein JB (2000) Experimental measurements of the reversibility of metal-bacteria adsorption reactions. Chem Geol 168:27–36CrossRefGoogle Scholar
  32. Garbisu C, Hall DO, Serra JL (1993) Removal of phosphate by foam Immobilized Phormidium laminosum in batch and continuous-flow bioreactors. J Chem Technol Biotechnol 57:181–189CrossRefGoogle Scholar
  33. Garcia-Meza JV, Barrangue C, Admiraal W (2005) Biofilm formation by algae as a mechanism for surviving on mine tailings. Environ Toxicol Chem 24:573–581PubMedCrossRefGoogle Scholar
  34. Gardea Torresdey JL, Arenas JL, Webb R, Francisco NMC, Tiemann KJ, Gutierrez F (1996) Copper adsorption by inactivated cells of Mucor rouxii: effect of esterification of carboxyl groups. J Hazard Mater 48:171–180CrossRefGoogle Scholar
  35. Gardea Torresdey JL, Arenas JL, Webb R, Francisco NMC, Tiemann KJ (1998) Ability of immobilized cyanobacteria to remove metal ions from solution and demonstration of the presence of metallothionein genes in various strains. J Hazard Subst Res 1:1–18Google Scholar
  36. Gorman-Lewis D, Elias PE, Fein JB (2005) Adsorption of aqueous uranyl complexes onto Bacillus subtilis cells. Environ Sci Technol 39:4906–4912PubMedCrossRefGoogle Scholar
  37. Haas JR, Bailey EH, Purvis OW (1998) Bioaccumulation of metals by lichens; uptake of aqueous uranium by Peltigera membranacea as a function of time and pH. Am Mineral 83:1494–1502Google Scholar
  38. Heitkamp D, Wagener K (1982) New aspects of uranium recovery from seawater. Ind Eng Chem Process Des Dev 21:781–784CrossRefGoogle Scholar
  39. Hu P, Brodie EL, Suzuki Y, McAdams HH, Andersen GL (2005) Whole-genome transcriptional analysis of heavy metal stresses in Caulobacter crescentus. J Bacteriol 187:8437–8449PubMedCrossRefGoogle Scholar
  40. Jensen TE, Baxter M, Rachlin JW, Jani V (1982) Uptake of heavy metals by Plectonema boryanum (Cyanophyceae) into cellular compartments, especially polyphosphate bodies: an X-ray energy dispersive study. Environ Pollut 27:119–127CrossRefGoogle Scholar
  41. Kanamaru K, Kashiwagi S, Mizuno T (1994) A copper transporting P-type ATPase found in the thylakoid membrane of the cyanobacterium Synechococcus species PCC 7942. Mol Microbiol 13:369–377PubMedCrossRefGoogle Scholar
  42. Khani MH, Keshtkar AR, Ghannadi M, Pahlavanzadeh H (2008) Equilibrium, kinetic and thermodynamic study of the biosorption of uranium onto Cystoseira indica algae. J Hazard Mater 150:612–618PubMedCrossRefGoogle Scholar
  43. Kim J, Tsouris C, Mayes RT, Oyola Y, Saito T, Janke CJ, Dai S, Schneider E, Sachde D (2013) Recovery of uranium from seawater: a review of current status and future research needs. Sep Sci Technol 48:367–387CrossRefGoogle Scholar
  44. Li PF, Mao ZY, Rao XJ, Wang XM, Min MZ, Qiu LW, Liu ZL (2004) Biosorption of uranium by lake-harvested biomass from a cyanobacterium bloom. Bioresour Technol 94:193–195PubMedCrossRefGoogle Scholar
  45. Lovley DR, Phillips EJP, Gorby YA, Landa ER (1991) Microbial reduction of uranium. Nature 350:413–416CrossRefGoogle Scholar
  46. Macaskie LE, Dean ACR (1990) Metal-sequestering biochemicals. In: Volesky B (ed) Biosorption of heavy metals. CRC Press, Boca Raton, pp 199–248Google Scholar
  47. Macaskie LE, Bonthrone KM, Yong P, Goddard DT (2000) Enzymically mediated bioprecipitation of uranium by a Citrobacter sp. A concerted role for exocellular lipopolysaccharide and associated phosphatase in biomineral formation. Microbiology 146:1855–1867PubMedGoogle Scholar
  48. Mallick N, Rai LC (1994) Removal of inorganic ions from wastewaters by immobilized microalgae. World J Microbiol Biotechnol 10:439–443CrossRefGoogle Scholar
  49. Markich SJ (2002) Uranium speciation and bioavailability in aquatic systems: an overview. Sci World J 2:707–729CrossRefGoogle Scholar
  50. Martinez RJM, Beazley J, Teillefert M, Arakaki AK, Skolnick J, Sobecky PA (2007) Aerobic uranium (VI) bioprecipitation by metal-resistant bacteria isolated from radionuclide and metal-contaminated subsurface soils. Environ Microbiol 9:3122–3133PubMedCrossRefGoogle Scholar
  51. Merroun ML, Hennig C, Rossberg A, Reich T, Selenska-Pobell S (2003) Characterization of U(VI)–Acidithiobacillus ferrooxidans complexes by using EXAFS, transmission electron microscopy and energy-dispersive X-ray analysis. Radiochim Acta 91:583–591CrossRefGoogle Scholar
  52. Merroun ML, Raff J, Rossberg A, Hennig C, Reich T, Selenska-Pobell S (2005) Complexation of uranium by cells and S-layer sheets of Bacillus sphaericus JG-A12. Appl Environ Microbiol 71:5542–5553CrossRefGoogle Scholar
  53. Merroun ML, Nedelkova M, Rossberg A, Hennig C, Selenska-Pobell S (2006) Interaction mechanisms of uranium with bacterial strains isolated from extreme habitats. Radiochim Acta 94:723–729CrossRefGoogle Scholar
  54. Mikkat S, Hagemann M (2000) Molecular analysis of the ggtBCD gene cluster of Synechocystis sp. strain PCC6803 encoding subunits of an ABC transporter for osmoprotective compounds. Arch Microbiol 174:273–282PubMedCrossRefGoogle Scholar
  55. Misra CS, Appukuttan D, Kantamreddi VSS, Rao AS, Apte SK (2012) Recombinant D. radiodurans cells for bioremediation of heavy metals from acidic/neutral aqueous wastes. Bioeng Bugs 3:44–48PubMedCrossRefGoogle Scholar
  56. Mohamed ZA (2001) Removal of cadmium and manganese by a non-toxic strain of the freshwater cyanobacterium Gloeothece magna. Water Res 35:4405–4409PubMedCrossRefGoogle Scholar
  57. Mukherjee A, Wheaton GH, Blum PH, Kelly RM (2012) Uranium extremophily is an adaptive, rather than intrinsic, feature for extremely thermoacidophilic Metallosphaera species. Proc Natl Acad Sci USA 109:16702–16707PubMedCrossRefGoogle Scholar
  58. Nakajima A, Horikoshi T, Sakaguchi T (1982) Studies on the accumulation of heavy metal elements in biological systems XXI. Recovery of uranium by immobilized microorganisms. Eur J Appl Microbiol Biotechnol 16:88–91CrossRefGoogle Scholar
  59. Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339PubMedCrossRefGoogle Scholar
  60. Pettersson A, Hallbom L, Bergmann B (1988) Aluminium effects on uptake and metabolism of phosphorus by the cyanobacterium Anabaena cylindrica. Plant Physiol 86:112–116PubMedCrossRefGoogle Scholar
  61. Philippis RD, Vincenzini M (1998) Extracellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiol Rev 22:151–175Google Scholar
  62. Phoenix VR, Martinez RE, Konhauser KO, Ferris FG (2002) Characterization and implications of the cell surface reactivity of Calothrix sp. Strain KC97. Appl Environ Microbiol 68:4827–4834PubMedCrossRefGoogle Scholar
  63. Plummer EJ, Macaskie LE (1990) Actinide and lanthanum toxicity towards a Citrobacter sp. Uptake of lanthanum and a strategy for the biological treatment of liquid wastes containing plutonium. Bull Environ Contam Toxicol 44:173–180PubMedCrossRefGoogle Scholar
  64. Polikarpov GG (1966) Regularities of uptake and accumulation of radionuclides in aquatic organisms. In: Aberg B, Hungate FP (eds) Radioecological concentration processes. Pergamon Press, Oxford, pp 819–825Google Scholar
  65. Prakasham R, Ramakrishna SV (1998) The role of cyanobacteria in effluent treatment. J Sci Ind Res 57:258–265Google Scholar
  66. Rachlin JW, Jensen TE, Warkentine B (1984) The toxicological response of the alga Anabaena flos-aquae (Cyanophyceae) to cadmium. Arch Environ Contam Toxicol 13:143–151CrossRefGoogle Scholar
  67. Rai LC, Mallick N (1992) Removal and assessment of toxicity of Cu and Fe to Anabaena doliolum and Chlorella vulgaris using free and immobilized cells. World J Microbiol Biotechnol 8:110–114CrossRefGoogle Scholar
  68. Riley RG, Zachara JM (1992) Chemical contaminants on DOE lands and election of contaminant mixtures for subsurface science research. DOE/ER-0547T. U.S. Department of Energy, Office of Energy Res, Washington DCGoogle Scholar
  69. Sakaguchi T (1996) Bioaccumulation of uranium. Kyushu University Press, Hukuoka, pp 61–95Google Scholar
  70. Sakaguchi T, Nakajima A (1991) Accumulation of heavy metals such as uranium and thorium by microorganisms. In: Smith RW, Misra M (eds) Mineral bioprocessing. The Minerals, Metals and Materials Society, WarrendaleGoogle Scholar
  71. Sakaguchi T, Horikoshi T, Nakajima A (1978) Uptake of uranium from sea water by microalgae. J Ferment Technol 56:561–565Google Scholar
  72. Sar P, D’Souza SF (2001) Biosorptive uranium uptake by a Pseudomonas strain: characterization and equilibrium studies. J Chem Technol Biotechnol 76:1286–1294CrossRefGoogle Scholar
  73. Self WT, Grunden AM, Hasona A, Shanmugam KT (2001) Molybdate transport. Res Microbiol 152:311–321PubMedCrossRefGoogle Scholar
  74. Suzuki Y, Banfield JF (1999) Geomicrobiology of uranium. Rev Mineral Geochem 38:393–432Google Scholar
  75. Suzuki Y, Banfield JF (2004) Resistance to, and accumulation of, uranium by bacteria from a uranium-contaminated site. J Geomicrobiol 21:113–121CrossRefGoogle Scholar
  76. Swift DT, Forciniti D (1997) Accumulation of lead by Anabaena cylindrica: mathematical modeling and an energy dispersive X-ray study. Biotechnol Bioeng 55:408–418PubMedCrossRefGoogle Scholar
  77. Tsezos M, Noh SH (1984) Extraction of uranium from sea water using biological origin adsorbents. Can J Chem Eng 62:559–561CrossRefGoogle Scholar
  78. Tsezos M, Volesky B (1981) Biosorption of uranium and thorium. Biotechnol Bioeng 23:583–604CrossRefGoogle Scholar
  79. Turner JS, Robinson NJ (1995) Cyanobacterial metallothioneins: biochemistry and molecular genetics. J Ind Microbiol 14:119–125PubMedCrossRefGoogle Scholar
  80. US EPA (2003) United States Environment Protection Agency. Review of RSC analysis, vol 45. Report prepared by Wade Miller Associates, Inc. for the US Environmental Protection Agency. Health Phys, p 361Google Scholar
  81. Vanengelen MR, Szilagyi RK, Gerlach R, Lee BD, Apel WA, Peyton BM (2011) Uranium exerts acute toxicity by binding to pyrroloquinoline quinone cofactor. Environ Sci Technol 45:937–942PubMedCrossRefGoogle Scholar
  82. Vijayaraghavan R, Mohandass S, Ramamoorthy R, D’Souza SF, Prabaharan D, Lakshmanan U (2013) Siderophore mediated uranium sequestration by marine cyanobacterium Synechococcus elongatus BDU 130911. Bioresour Technol 130:204–210CrossRefGoogle Scholar
  83. Volesky B (1990) Removal and recovery of heavy metals by biosorption. In: Volesky B (ed) Biosorption of heavy metals. CRC Press, Boca Raton, pp 7–44Google Scholar
  84. Wang WX, Dei RC, Hong H (2005) Seasonal study on the Cd, Se, and Zn uptake by natural coastal phytoplankton assemblages. Environ Toxicol Chem 24:161–169PubMedCrossRefGoogle Scholar
  85. Yang J, Volesky B (1999) Biosorption of uranium on Sargassum biomass. Water Res 33:3357–3363CrossRefGoogle Scholar
  86. Yee N, Benning GL, Phoenix VR, Ferris FG (2004) Characterization of metal-cyanobacteria sorption reactions: a combined macroscopic and infrared spectroscopic investigation. Environ Sci Technol 38:775–782PubMedCrossRefGoogle Scholar
  87. Zhang X, Luo S, Yang Q, Zhang H, Li J (1997) Accumulation of uranium at low concentration by the green alga Scenedesmus obliquus 34. J Appl Phycol 9:65–71CrossRefGoogle Scholar
  88. Zhou PJ, Lin J, Shen H, Li T, Song LR, Shen YW, Liu YD (2004) Kinetic studies on the combined effects of lanthanum and cerium on the growth of Microcystis aeruginosa and their accumulation by M. aeruginosa. Bull Environ Contam Toxicol 72:711–716PubMedGoogle Scholar

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© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Molecular Biology DivisionBhabha Atomic Research CentreMumbaiIndia

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