Abstract
Bacteria and archaea are the most ubiquitous organisms in terrestrial and aquatic environments. They play a major role in deposition and weathering of a large variety of minerals enriched with or consisting mainly of different metals, such as iron, manganese, copper, gold, and even radionuclides (e.g., uranium). The structure of biologically synthesized minerals is strongly influenced by the metabolic properties of the bacterial or archaeal strains involved in their production and also by the metal binding potentials of their cell wall components.
This chapter is focused on cell wall-dependent accumulation and biomineralization of iron and uranium. By using transmission electron microscopic analysis in combination with x-ray absorption and time-resolved laser-induced fluorescence spectroscopic analysis, it is demonstrated that the Gram-negative and most of the Gram-positive bacteria as well as some archaea immobilize U(VI) at their cell walls or extracellularly in a form of uranyl phosphate compounds. However, some Gram-positive bacteria which possess highly ordered proteinaceous surface layers (S-layers), immobilize U(VI) not only by phosphate groups mainly from their peptidoglycan but also by the carboxylic groups of the aspartate and glutamate stretches of their S-layers.
In addition, the cell wall-supported formation of metallic palladium nanoclusters by some bacteria is presented. Despite the different mechanisms of the biological deposition of Pd by Gram-negative and Gram-positive bacteria, the nanoparticles formed by both organisms have almost identical size and catalytic activity.
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References
Anderson RT, Vrionis HA, Ortiz-Bernad I, Resch CT, Lonh PE, Dayvault R, Karp K, Marutzky S, Metzler DR, Peacock A, White DC, Lowe M, Lovley DR (2003) Stimulating the in situ activity of Geobacter species to remove uranium from the groundwater of a uranium contaminated aquifer. Appl Environ Microbiol 69:5884–5891
Bäuerlein E (2003) Biomineralization of unicellular organisms: unusual membrane biochemistry for the production of inorganic nano- and microstructures. Angew Chem Int Ed 42(6):615–641
Bazylinski DA, Frankel RB (2003) Biologically controlled mineralization in prokaryotes. Rev Mineral Geochem 54(1):217–247
Beazley MJ, Martinez RJ, Sobecky PA, Webb SM, Taillefert M (2007) Uranium biomineralization as a result of bacterial phosphatase activity: insight from bacterial isolates from a contaminated subsurface. Environ Sci Technol 41:5701–5707
Beveridge TJ (1989) Role of cellular design in bacterial metal accumulation and mineralisation. Annu Rev Microbiol 43:147–71
Beveridge TJ (2005) Bacterial cell wall structures and implications for interactions with metal ions and minerals. J Nucl Radiochem Sci 6(1):7–10
Bonthrone KM, Quarmby J, Hewitt CJ, Allan VJM, Paterson-Beedle M, Kennedy JF, Macaskie LE (2000) The effect of the growth medium on the composition and metal binding behaviour of the extracellular polymeric material of a metal-accumulating Citrobacter sp. Environ Technol 2:123–134
Brown DA, Beveridge TJ, Keevil CW, Sherriff BL (1998) Evaluation of microscopic techniques to observe iron precipitation in a natural microbial biofilm. FEMS Microbiol Ecol 26:297–310
Chaudhuri SK, Lack JG, Goates JI (2001) Biogenic magnetite formation through anaerobic bio-oxidation of Fe (II). Appl Environ Microbiol 67:2844–2848
Creamer NJ, Mikheenko IP, Yong P, Deplanche K, Sanyahumbi WDJ, Pollmann K, Merroun M, Selenska-Pobell S, Macaskie LE (2007) Novel supported Pd hydrogenation bionanocatalyst for hybrid homogeneous/heterogeneous catalysis. Catal Today 128:80–87
De Luca G, De Philip P, Dermoun Z, Rousset M, Vermeglio A (2001) Reduction of technetium(VII) by Desulfovibrio fructosovorans is mediated by the nickel-iron hydrogenase. Appl Environ Microbiol 67:4583–4587
De Windt W, Boon N, Van den Bulcke J, Rubberecht L, Prata F, Mast J, Hennebel T, Verstraete W (2006) Biological control of the size and the reactivity of catalytic Pd(0) produced Shewanella oneidensis. Antonie Van Leeuwenhoek 90:377–389
DiChristina T, Moore CM, Haller CA (2002) Dissimilatory Fe(III) and Mn(IV) reduction by Shewanella putrefaciens requires ferE, a homolog of the pulE (gspE) type II protein secretion gene. J Bacteriol 184:142–151
Douglas S, Beveridge TJ (1998) Mineral formation by bacteria in natural microbial communities. FEMS Microbiol Ecol 26:79–88
Ehrlich HL (1998) Geomicrobiology: its significance for geology. Earth-Sci Rev 45:45–60
Elias DA, Suflita JM, McInerney MJ, Krumholz LR (2004) Periplasmic cytochrome C3 of Desulfovibrio vulgaris is directly involved in H2-mediated metal but not sulphate reduction. Appl Environ Microbiol 70:413–420
Fahmy K, Merroun M, Raff J, Pollmann K, Hennig Ch, Savchuk O, Selenska-Pobell S (2006) Secondary structure and Pd(II) co-ordination in S-layer proteins from Bacillus sphaericus studied by infrared and X-ray absorption spectroscopy. Biophys J 91:996–1007
Finneran KT, Housewright ME, Lovley DR (2002) Multiple influences of nitrate on uranium solubility during bioremediation of uranium-contaminated subsurface sediments. Environ Microbiol 4:510–516
Fortin D, Davis B, Beveridge TJ (1996) Role of Thiobacillus and sulfate-reducing bacteria in iron biocycling in oxic and acidic mine tailings. FEMS Microbiol Ecol 21:11–24
Francis AL, Gillow JB, Dodge CJ, Harris R, Beveredge TJ, Papenguth HW (2004) Uranium association with halophilic and non-halophilic bacteria and archaea. Radiochim Acta 92:481–488
Frankel RB, Bazylinski DA (2003) Biologically induced mineralization by bacteria. Rev Mineral Geochem 54(1):95–114
Gehrke T, Telegi J, Thierry D, Sand W (1998) Importance of extracellular polymeric substances from Thiobacillus ferrooxidans for bioleaching. Appl Environ Microbiol 64:2743–2747
Geissler A (2007) Prokaryotic micro-organisms in uranium mining waste piles and their interactions with uranium and other heavy metals. PhD Thesis. TU Bergakademie Freiberg, Freiberg, Germany
Geissler A, Selenska-Pobell S (2005) Behavior of U(VI) added to a uranium mining waste pile sample and the resulting changes in the indigenous bacterial community. Geobiology 3:275–285
Geissler A, Merroun M, Geipel G, Reuther H, Selenska-Pobell S (2009) Biogeochemical changes induced in uranium mining waste pile samples by uranyl nitrate treatments under anaerobic conditions. Geobiology 7:282–294
Glasauer S, Landley S, Beveridge TJ (2001) Sorption of Fe(hydr)oxides to the surface of Shewanella putrefaciens: cell-bound fine grained minerals are not always formed de novo. Appl Environ Microbiol 67:5544–5550
Glasauer S, Landley S, Beveridge TJ (2002) Intracellular iron minerals in a dissimilatory iron reducing bacterium. Science 295(4):117–119
Glasauer S, Landley S, Boyanov M, Lai B, Kemner K, Beveridge TJ (2007) Mixed valence cytoplasmic iron granules are linked to anaerobic respiration. Appl Environ Microbiol 73:993–996
Hanert HH (2006) The genus Siderocapsa (and other iron- and manganese-oxidizing Eubacteria). In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes, vol 7. Springer, New York, pp 1005–1015
Istok JD, Senko JM, Krumholz LR, Watson D, Bogle MA, Peacock A, Chang Y-J, White DC (2004) In situ bioreduction of technetium and uranium in a nitrate-contaminated aquifer. Environ Sci Technol 38:468–475
Jroundi F, Merroun M, Arias JM, Rossberg A, Selenska-Pobell S, Gonzalez-Munoz MT (2007) Spectroscopic and microscopic characterization of uranium biomineralization by Myxococcus xanthus. Geomicrobiol J 24:441–449
Kashefi K, Tor JM, Nevin KP, Lovley D (2001) Reductive precipitation of gold by dissimilatory Fe(III)-reducing bacteria and archaea. Appl Environ Microbiol 67:3275–3279
Kashefi K, Shelobolina ES, Elliot WC, Lovley DR (2008) Growth of thermophilic and hyperthermophilic Fe(III)-reducing micro-organisms on a ferruginous smectite as a sole electron acceptor. Appl Environ Microbiol 74:251–258
Kelly SD, Kemner KM, Fein JB, Fowle DA, Boyanov MI, Bunker BA, Yee N (2002) X-ray absorption fine structure determination of pH-dependent U-bacterial cell wall interactions. Geochim Cosmochim Acta 65:3855–3871
Koban A, Geipel G, Roßberg A, Bernhard G (2004) Uranyl (VI) complexes with sugar phosphates in aqueous solution. Radiochim Acta 92:903–908
Lloyd JR (2003) Microbial reduction of metals and radionuclides. FEMS Microb Rev 27:411–425
Lloyd JR, Yong P, Macaskie L (1998) Enzymatic recovery of elemental palladium by using sulphate-reducing bacteria. Appl Environ Microbiol 64:4607–4609
Lovley DR (1993) Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol Rev 55:259–287
Lovley DR (2002) Dissimilatory metal reduction: from early life to bioremediation. ASM News 68(5):231–237
Lovley DR, Phillips GYA, Landa ER (1991) Microbial reduction of uranium. Nature 350:413–416
Lovley DR, Widman PK, Woodward JC, Phillips EJP (1993) Reduction of uranium by cytochrome c3 of Desulfovibrio vulgaris. Appl Environ Microbiol 59:3572–3576
Macaskie LE, Empson RM, Cheetham AK, Grey CP, Scarnulis AJ (1992) Uranium bioaccumulation by Citrobacter sp. as a result of enzymatically mediated growth of polycrystalline HUO2PO4. Science 257:782–784
Macaskie LE, Bonthrone KM, Yong P, Goddart DT (2000) Enzymatically mediated bioprecipitation of uranium by a Citrobacter sp.: a concerted role for exocellular lipopolysaccharide and associated phosphatase in biomineral formation. Microbiology 146:1855–1867
Macaskie LE, Baxter-Plant VS, Creamer NJ, Humphries AC, Mikheenko IP, Mikheenko PM, Penfold DW, Yong P (2005) Applications of bacterial hydrogenases in waste decontamination, manufacture of novel bionanocatalysts and in sustainable energy. Biochem Soc Trans 33:76–79
Marqués AM, Roca X, Simon-Pujol MD, Fuste MC, Congregado F (1991) Uranium accumulation by Pseudomonas sp. ESP-5028. Appl Microbiol Biotechnol 35:406–410
Marshall MJ, Beliaev AS, Dohnalkova AC, Kennedy DW, Shi L, Wang Z, Boyanov MI, Lai B, Kemner K, McLean JS, Reed SB, Culley DE, Bailey VL, Simonson CJ, Saffarini DA, Romine MF, Zachara JM, Fredrickson JK (2006) C-type cytochrome-dependent formation of U(VI) nanoparticles by Shewanella onediensis. PLos 4(8):1324–1333
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 9:3122–3133
Merroun M, Selenska-Pobell S (2001) Interactions of three eco-types of Acidithiobacillus ferrooxidans strains with U(VI). BioMetals 14:171–179
Merroun M, Hennig C, Rosberg A, Geipel G, Reich T, Selenska-Pobell S (2002) Molecular and atomic analysis of uranium complexes formed by three eco-types of Acidithiobacillus ferrooxidans. Biochem Soc Trans 30:669–672
Merroun M, Hennig C, Rossberg A, Reich T, Selenska-Pobell S (2003) Characterization of U(VI)-Acidithiobacillus ferrooxidans complexes using EXAFS, transmission electron microscopy, and energy-dispersive X-ray analysis. Radiochim Acta 91:583–592
Merroun M, 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 71:5532–5543
Merroun M, Nedelkova M, Rossberg A, Hennig C, Selenska-Pobell S (2006) Interaction mechanisms of bacteria from extreme habitats with uranium as a function of pH. Radiochim Acta 94:723–729
Merroun ML, Nedelkova M, Ojeda, J Hennig C, Rossberg A, Romero-Gonzalez M, Selenska-Pobell S (2008) Bio-precipitation of uranium by natural bacterial isolates: a combined potentiometric titration, TEM and X-ray absorption spectroscopy study. FEMS Microbiol Ecol (In press)
Nedelkova M, Merroun ML, Rossberg A, Hennig C, Selenska-Pobell S (2007) Microbacterial isolates from the vicinity of a radioactive waste depository and their interactions with uranium. FEMS Microbiol Ecol 59:694–705
Nevin KP, Finneran KT, Lovley DR (2003) Micro-organisms associated with uranium bioremediation in a high-salinity subsurface sediment. Appl Environ Microbiol 69:3672–3675
Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339
Nyman JL, Marsh TL, Ginder-Vogel MA, Gentile M, Fendorf S, Criddle C (2006) Heterogeneous response to biostimulation for U(VI) reduction in replicated sediment microcosms. Biodegradation 17:303–316
Petrie L, North NN, Dollhopf SL, Balkwill DL, Kostka JE (2003) Enumeration and characterization of iron(III)-reducing microbial communities from acidic subsurface sediments contaminated with uranium(VI). Appl Environ Microbiol 69:7467–7479
Pollmann K, Raff J, Schnorpfeil M, Radeva G, Selenska-Pobell S (2005) Novel surface layer protein genes in Bacillus sphaericus associated with unusual insertion elements. Microbiology 151:2961–2973
Pollmann K, Raff J, Merroun M, Fahmy K, Mikheenko I, Selenska-Pobell S (2006) Bacteria from uranium mining waste piles and their technological applications. Biotechnol Adv 24:58–68
Raff J, Soltmann U, Matys S, Selenska-Pobell S, Böttcher H, Pompe W (2003) Biosorption of uranium and copper by biocers. Chem Mater 15:240–244
Redwood MD, Deplanche K, Baxter-Plant VS, Macaskie LE (2007) Biomass-supported palladium catalysts on Desulfovibrio desulfuricans and Rhodobacter sphaeroides. Biotechnol Bioengin. DOI: On line publication: 10.1002/bit.21689
Renninger N, Knopp R, Nitsche H, Clark DS, Keasling JD (2004) Uranyl precipitation by Pseudomonas aeruginosa via controlled polyphosphate metabolism. Appl Environ Microbiol 70:7404–7412
Roh Y, Gao H, Vali H, Kennedy DW, Yang ZK, Gao W, Dohnalkova AC, Stapelton RD, Moon J-W, Phels TJ, Fredricson JK, Zhou J (2006) Metal reduction and iron iomineralization by a psychrotolerant Fe(III)-reducing bacterium, Shewanella sp. strain PV-4. Appl Environ Microbiol 72:3236–3244
Rosen R, Becher D, Buttner K, Biran D, Hecker M, Ron EZ (2004) Highly phosphorylated bacterial proteins. Proteomics 4:3068–3077
Schulze-Lam S, Harauz G, Beveridge TJ (1992) Participation of a cyanobacterial S-layer in fine-grain mineral formation. J Bacteriol 174:7971–7981
Selenska-Pobell S (2002) Diversity and activity of bacteria in uranium waste piles. In: Keith-Roach MJ, Livens FR (eds) Interactions of micro-organisms with radionuclides. Elsevier Sciences Ltd, Oxford, UK, pp 225–254
Selenska-Pobell S, Miteva V, Boudakov I, Panak P, Bernhard G, Nitsche H (1999) Selective accumulation of heavy metals by three indigenous Bacillus isolates, B. cereus, B. megaterium and B. sphaericus in drain waters from a uranium waste pile. FEMS Microbiol Ecol 29:59–67
Sillitoe RH, Folk RL, Saric N (1996) Bacteria as mediators of copper sulfide enrichment during weathering. Science 272:1153–1155
Sleytr UB, Messner P, Pum D, Sára MRG (1996) Crystalline bacterial cell surface proteins. Academic Press, Landes Company
Suzuki Y, Banfield JF (2004) Resistance to and accumulation of uranium by bacteria from a uranium-contaminated site. Geomicrobiol J 21:113–121
Suzuki Y, Kelly SD, Kemner KM, Banfield JF (2003) Microbial populations stimulated for hexavalent uranium reduction in uranium mine sediment. Appl Environ Microbiol 69:1337–1346
Urrutia Mera M, Kemper M, Doyle R, Beveridge TJ (1992) The membrane-induced proton motive force influences the metal binding ability of Bacillus subtilis cell walls. Appl Environ Microbiol 58:3834–3844
Vargas M, Kashefi K, Blunt-Harris EL, Lovley DR (1998) Microbiological evidence for Fe(III) reduction on early Earth. Nature 395:65–67
Wahl R, Mertig M, Raff J, Selenska-Pobell S, Pompe W (2001) Electron-beam induced formation of highly ordered palladium and platinum nanoparticle arrays on the S-layer of Bacillus sphaericus NCTC 9602. Adv Mater 13:736–740
Wan J, Tokunaga TK, Brodie E, Wang Z, Zheng Z, Herman D, Hazen TC, Firestone MK, Sutton SR (2005) Reoxidation of bioreduced uranium under reducing conditions. Environ Sci Technol 39:6162–6169
Yong P, Rowson NA, Farr JPG, Harris IR, Macaskie LM (2002) Bioreduction and biocrystallization of palladium by Desulfovibrio desulfuricans NCIMB 8307. Biotechnol Bioeng 80:369–379
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Selenska-Pobell, S., Merroun, M. (2010). Accumulation of Heavy Metals by Micro-organisms: Biomineralization and Nanocluster Formation. In: König, H., Claus, H., Varma, A. (eds) Prokaryotic Cell Wall Compounds. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-05062-6_17
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