Role of extracellular polymeric substances in metal ion complexation on Shewanella oneidensis: Batch uptake, thermodynamic modeling, ATR-FTIR, and EXAFS study

Geochimica et Cosmochimica Acta

Volumn 74, Issue 1, 2010, Pages 1-15

  Ha, Juyoung ^a   Gélabert, Alexandre ^a   Spormann, Alfred M ^b   Brown Jr , Gordon E ^a,b,c  

^a STANFORD UNIVERSITY   (United States)

^b Stanford University   (United States)

^c SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADSORPTION; COMPLEXATION; DIFFUSION; FTIR SPECTROSCOPY; SPECTRAL ANALYSIS; THERMODYNAMICS;

NEGIBACTERIA; SHEWANELLA ONEIDENSIS;

EID: 70449466966     PISSN: 00167037     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gca.2009.06.031     Document Type: Article

References (81)

1. Abrahams S.C., and Bernstein J.L. Remeasurement of the structure of hexagonal ZnO. Acta Crystallogr. B 25 (1969) 1233-1236
2. Ankudinov A.L., Ravel B., Rehr J.J., and Conradson S.D. Real-space multiple-scattering calculation and interpretation of X-ray-absorption near-edge structure. Phys. Rev. B: Condens. Matter. 58 (1998) 7565-7576
3. Bates S.S., Tessier A., Campbell P.G.C., and Létourneau M. Zinc-phosphorus interactions and variation in zinc accumulation during growth of Chlamydomonas variabilis (Chlorophyceae) in batch culture. Can. J. Fish. Aquat. Sci. 42 (1985) 86-94
4. Beveridge T.J., and Murray R.G.E. Sites of metal deposition in the cell wall of Bacillus subtilis. J. Bacteriol. 141 (1980) 876-887
5. Beveridge T.J., and Fyfe W.S. Metal fixation by bacterial cell walls. Can. J. Earth Sci. 22 (1985) 1893-1898
6. Beveridge T.J. Role of cellular design in bacterial metal accumulation and mineralization. Ann. Rev. Microbiol. 43 (1989) 147-171
7. Boyanov M.L., Kelly S.D., Kemner K.M., Bunker B.A., Fein J.B., and Fowle D.A. Adsorption of cadmium to Bacillus subtilis bacterial cell walls: a pH-dependent X-ray absorption fine structure spectroscopy study. Geochim. Cosmochim. Acta 67 (2003) 3299-3311
8. Boyanov M.I., O'Loughlin E.J., Roden E.E., Fein J.B., and Kemner K.M. Adsorption of Fe(II) and U(VI) to carboxyl-functionalized microspheres: the influence of speciation on uranyl reduction studied by titration and XAFS. Geochim. Cosmochim. Acta 71 (2007) 1898-1912
9. Brown Jr. G.E., and Sturchio N.C. An overview of synchrotron radiation applications to low temperature geochemistry and environmental science. Rev. Mineral. Geochem. 49 (2002) 1-115
10. Bruinsma G.M., Rustema-Abbing M., van der Mei H.C., and Busscher H.J. Effects of cell surface damage on surface properties and adhesion of Pseudomonas aeruginosa. J. Microbiol. Methods 45 (2001) 95-101
11. Burnett P.-G.G., Heinrich H., Peak D., Bremer P.J., McQuillan J., and Daughney C.J. The effect of pH and ionic strength on proton adsorption by the thermophilic bacterium Anoxybacillus flavithermus. Geochim. Cosmochim. Acta 70 (2006) 1914-1927
12. Claessens J., Behrends T., and Van Cappellen P. What do acid-base titrations of live bacteria tell us? A preliminary assessment. Aquat. Sci. 66 (2004) 19-26
13. 2+ to live cells of Shewanella putrefaciens. Environ. Sci. Technol. 41 (2007) 909-914
14. Comte S., Guibaud G., and Baudu M. Biosorption properties of extracellular polymeric substances (EPS) resulting from activated sludge according to their type: soluble or bound. Process Biochem. 41 (2006) 815-823
15. Costerton J.W., Lewandowski Z., Caldwell D.E., Korber D.R., and Lappin-Scott H.M. Microbial biofilms. Ann. Rev. Microbiol. 49 (1995) 711-745
16. 2+ by Bacillus subtilis and Bacillus licheniformis: a surface complexation model. J. Colloid Interface Sci. 198 (1998) 53-77
17. Daughney C.J., Fein J.B., and Yee N. A comparison of the thermodynamics of metal adsorption onto two common bacteria. Chem. Geol. 144 (1998) 161-176
18. Daughney C.J., Fowle D.A., and Fortin D. The effect of growth phase on proton and metal adsorption by Bacillus subtilis. Geochim. Cosmochim. Acta 65 (2001) 1025-1035
19. Doonan B.B., Crang R.E., Jensen T.E., and Baxter M. In situ X-ray energy dispersive microanalysis of polyphosphate bodies in Aureobasidium pullulans. J. Ultrastruc. Res. 69 (1979) 232-238
20. Effenberger H., Mereiter K., and Zemann J. Crystal structure refinements of magnesite, calcite, rhodochrosite, siderite, smithonite, and dolomite, with the discussion of some aspects of the stereochemistry of calcite type carbonates. Z. Kristallogr. 156 (1982) 233-243
21. Fein J.B. Quantifying the effects of bacteria on adsorption reactions in water-rock systems. Chem. Geol. 169 (2000) 265-280
22. Fein J.B. Thermodynamic modeling of metal adsorption onto bacterial cell walls: current challenges. Adv. Agron. 90 (2007) 179-202
23. Fein J.B., Daughney C.J., Yee N., and Davis T.A. A chemical equilibrium model for metal adsorption onto bacterial surfaces. Geochim. Cosmochim. Acta 61 (1997) 3319-3328
24. Fein J.B., Martin A.M., and Wightman P.G. Metal adsorption onto bacterial surfaces: development of a predictive approach. Geochim. Cosmochim. Acta 65 (2001) 4267-4273
25. Felmy A.R., Girvin D.C., and Jenne E.A. MINTEQ-A Computer Program for Calculating Aqueous Geochemical Equilibria (1984), US Environmental Protection Agency, Athens, GA
26. Gélabert A., Pokrovsky O.S., Schott J., Boudou A., Feurtet-Mazel A., Mielczarski J., Mielczarski E., Mesmer-Dudons N., and Spalla O. Study of diatom/aqueous solution interface. I. Acid-base equilibria and spectroscopic observation of freshwater and marine species. Geochim. Cosmochim. Acta 68 (2004) 4039-4058
27. Gonzalez-Davila M. The role of phytoplankton cell on the control of heavy metal concentrations in seawater. Marine Chem. 48 (1995) 215-236
28. Guibaud G., Tixier N., Bouju A., and Baudu M. Relation between extracellular polymers' composition and its ability to complex Cd, Cu and Pb. Chemosphere 52 (2003) 1701-1710
29. Guine V., Spadini L., Sarret G., Muris M., Delolme C., Gaudet J.P., and Martins J.M.F. Zinc sorption to three Gram-negative bacteria: combined titration, modeling, and EXAFS study. Environ. Sci. Technol. 40 (2006) 1806-1813
30. Guine V., Martins J.M.F., Causse B., Durand A., Gaudet J.P., and Spadini L. Effect of cultivation and experimental conditions on the surface reactivity of the metal-resistant bacteria Cupriavidus metallidurans CH34 to protons, cadmium and zinc. Chem. Geol. 236 (2007) 266-280
31. Ha J., Trainor T.P., Farges F., and Brown Jr. G.E. Interaction of aqueous Zn(II) with hematite nanoparticles and microparticles: part 1. EXAFS study of Zn(II) adsorption and precipitation. Langmuir 25 (2009) 5574-5585
32. Haas J.R., Dichristina T.J., and Wade Jr. R. Thermodynamics of U(VI) sorption onto Shewanella putrefaciens. Chem. Geol. 180 (2001) 33-54
33. Harding M.M. The geometry of metal-ligand interactions relevant to proteins. Acta Crystallogr., Sect. D 55 (1999) 1432-1443
34. Herbelin A.L., and Westall J.C. FITEQL Version 3.2, A Computer Program for Determination of Chemical Equilibrium Constants from Experimental Data (1996), Dept. of Chemistry, Oregon State University, Corvallis, OR
35. Heinrich H.T.M., Bremer P.J., McQuillan A.J., and Daughney C.J. Modeling of the acid-base properties of two thermophilic bacteria at different growth times. Geochim. Cosmochim. Acta 72 (2008) 4185-4200
36. Jiang W., Saxena A., Song B., Ward B.B., Beveridge T.J., and Myneni S.C.B. Elucidation of functional groups on Gram-positive and Gram-negative bacterial surfaces using infrared spectroscopy. Langmuir 20 (2004) 11433-11442
37. Juillot F., Morin G., Ildefonse P., Trainor T.P., Benedetti M., Galoisy L., Calas G., and Brown Jr. G.E. Occurrence of Zn/Al hydrotalcite in smelter-impacted soils from northern France:eEvidence from EXAFS spectroscopy and chemical extractions. Am. Mineral. 88 (2003) 509-526
38. Kang S.Y., Bremer P.J., Kim K.W., and McQuillan A.J. Monitoring metal ion binding in single-layer Pseudomonas aeruginosa biofilms using ATR-IR spectroscopy. Langmuir 22 (2006) 286-291
39. Karlsson T., and Skyllberg U. Complexation of zinc in organic soils - EXAFS evidence for sulfur associations. Environ. Sci. Technol. 41 (2007) 119-124
40. Kawahara A., and Gan K. The syntheses, thermal and structural studies of hopeite. J. Mineral. 7 (1972) 289-297
41. Kelly S.D., Kemner K.M., Fein J.B., Fowle D.A., Boyanov M.I., Bunker B.A., and Yee N. X-ray absorption fine structure determination of pH-dependent U-bacterial cell wall interactions. Geochim. Cosmochim. Acta 66 (2002) 3855-3871
42. Kramer U., Cotter-Howells J.D., Charnock J.M., Baker A.J.M., and Smith J.A.C. Free histidine as a metal chelator in plants that accumulate nickel. Nature 379 (1996) 635-638
43. 2+ binding properties of the bacterial exopolysaccharides. Chemosphere 65 (2006) 1362-1370
44. Leone L., Ferri D., Manfredi C., Persson P., Shchukarev A., Sjoberg S., and Loring J. Modeling the acid-base properties of bacterial surfaces: a combined spectroscopic and potentiometric study of the Gram-positive bacterium Bacillus subtilis. Environ. Sci. Technol. 41 (2007) 6465-6471
45. Liu Y., Yang C.H., and Li J. Influence of extracellular polymeric substances on Pseudomonas aeruginosa transport and deposition profiles in porous media. Environ. Sci. Technol. 41 (2007) 198-205
46. Lutzenkirchen J. The constant capacitance model and variable ionic strength: an evaluation of possible applications and applicability. J. Colloid Interface Sci. 217 (1999) 8-18
47. Matsukawa M., and Greenberg E.P. Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development. J. Bacteriol. 186 (2004) 4449-4456
48. Merroun M.L., Ben Chekroun K., Arias J.M., and Gonzalez-Munoz M.T. Lanthanum fixation by Myxococcus xanthus: cellular location and extracellular polysaccharide observation. Chemosphere 52 (2003) 113-120
49. Mullen M.D., Wolf D.C., Ferris F.G., Beveridge T.J., Flemming C.A., and Bailey G.W. Bacterial sorption of heavy metals. Appl. Environ. Microbiol. 55 (1989) 3143-3149
50. Neal A.L., Rosso K.M., Geesey G.G., Gorby Y.A., and Little B.J. Surface structure effects on direct reduction of iron oxides by Shewanella oneidensis. Geochim. Cosmochim. Acta 67 (2003) 4489-4503
51. Newman D.K. Microbiology: how bacteria respire minerals. Science 292 (2001) 1312-1313
52. Ngwenya B.T., Sutherland I.W., and Kennedy L. Comparison of the acid-base behaviour and metal adsorption characteristics of a Gram-negative bacterium with other strains. Appl. Geochem. 18 (2003) 527-538
53. Panak P.J., Booth C.H., Caulder D.L., Bucher J.J., Shuh D.K., and Nitsche H. X-ray absorption fine structure spectroscopy of plutonium complexes with Bacillus sphaericus. Radiochim. Acta 90 (2002) 315-321
54. Pokrovsky O.S., Schott J., and Thomas F. Processes at the magnesium-bearing carbonates/solution interface. I. A surface speciation model for magnesite. Geochim. Cosmochim. Acta 63 (1999) 863-880
55. Pokrovsky O.S., and Schott J. Experimental study of brucite dissolution and precipitation in aqueous solutions: surface speciation and chemical affinity control. Geochim. Cosmochim. Acta 68 (2004) 31-45
56. Pokrovsky O.S., Pokrovski G.S., Gélabert A., Schott J., and Boudou A. Speciation of Zn associated with diatoms using X-ray absorption spectroscopy. Environ. Sci. Technol. 39 (2005) 4490-4498
57. Sarret G., Manceau A., Hazemann J.L., Gomez A., and Mench M. EXAFS study of the nature of zinc complexation sites in humic substances as a function of Zn concentration. J. Phys. IV 7 (1997) 799-802
58. Sarret G., Manceau A., Spadini L., Roux J.C., Hazemann J.L., Soldo Y., Eybert-Berard L., and Menthonnex J.J. Structural determination of Zn and Pb binding sites in Penicillium chrysogenum cell walls by EXAFS spectroscopy. Environ. Sci. Technol. 32 (1998) 1648-1655
59. Sarret G., Manceau A., Cuny D., Van Haluwyn C., Deruelle S., Hazemann J.L., Soldo Y., Eybert-Berard L., and Menthonnex J.J. Mechanisms of lichen resistance to metal pollution. Environ. Sci. Technol. 32 (1998) 3325-3330
60. Sarret G., Saumitou-Laprade G., Bert V., Proux O., Hazemann J., Traverse A., Marcus A., and Manceau A. Forms of zinc accumulated in the hyperaccumulator Arabidopsis halleri. Plant Physiol. 130 (2002) 1815-1826
61. Slaveykova V.I., and Wilkinson K.J. Physicochemical aspects of lead bioaccumulation by Chlorella vulgaris. Environ. Sci. Technol. 36 (2002) 969-975
62. Sposito G. Distinguishing adsorption from surface precipitation. In: Davis J.A., and Hayes K.F. (Eds). Geochemical Processes at Mineral Surfaces. ACS Symp. Ser. vol. 323 (1986), American Chemical Society, Washington, DC 217-228
63. Templeton A.S., Trainor T.P., Traina S.J., Spormann A.M., and Brown Jr. G.E. Pb(II) distribution at biofilm-metal oxide interfaces. Proc. Nat. Acad. Sci. USA 98 (2001) 11897-11902
64. Templeton A.S., Trainor T.Ap., Spormann A.M., Newville M., Sutton S., Dohnalkova A., Gorby Y., and Brown Jr. G.E. Sorption vs. biomineralization of Pb(II) within Burkholderia cepacia biofilms on alumina. Environ. Sci. Technol. 37 (2003) 300-307
65. Thormann K.M., Duttler S., Saville R.M., Hyodo M., Shukla S., Hayakawa Y., and Spormann A.M. Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic di-GMP. J. Bacteriol. 188 (2006) 2681-2691
66. Toner B., Manceau A., Marcus M.A., Millet D.B., and Sposito G. Zinc sorption by a bacterial biofilm. Environ. Sci. Technol. 39 (2005) 8288-8294
67. Torres E., Cid A., Fidalgo P., Herrero C., and Abalde J. Long-chain class III metallothioneins as a mechanism of cadmium tolerance in the marine diatom Phaeodactylum tricornutum Bohlin. Aquat. Toxicol. 39 (1997) 231-246
68. Tourney J., Ngwenya B.T., Mosselmans J.W.F., Tetley L., and Cowie G.L. The effect of extracellular polymers (EPS) on the proton adsorption characteristics of the thermophile Bacillus licheniformis S-86. Chem. Geol. 247 (2008) 1-15
69. Tribe L., Kwon K.D., Trout C.D., and Kubicki J.D. Molecular orbital study on surface complex structures of glyphosate on goethite: calculation of vibrational frequencies. Environ. Sci. Technol. 40 (2006) 3836-3841
70. Urrutia M.M., and Beveridge T.J. Remobilization of heavy metals retained as oxyhydroxides or silicates by Bacillus subtilis cells. Appl. Environ. Microbiol. 59 (1993) 4323-4329
71. Walker S. L. and Chen G. (2006) Adhesion kinetics of freshwater and marine bacteria: role of solution chemistry. In Preprints of Extended Abstracts Presented at the ACS National Meeting, vol. 46. American Chemical Society, Division of Environmental Chemistry, pp. 1258-1260.
72. Wang S.L., Chuang C.H., and Lin S.Y. PH-dependent coordination of metal-lisinopril complex investigated by attenuated total reflection/Fourier transform infrared spectroscopy. Chem. Pharm. Bull. 58 1 (2002) 78-82
73. Webb S.M., Gaillard J.F., Jackson B.E., and Stahl D.A. An EXAFS study of zinc coordination in microbial cells. J. Synchrotron Radiation 8 (2001) 943-945
74. Webb S. SIXPACK: a graphical user interface for XAS analysis using IFEFFIT. Phys. Scripta T115 (2004) 1011-1014
75. Westall J.C. FITEQL, A Computer Program for Determination of Chemical Equilibrium from Experimental Data. Version 2.0. Report 82-02 (1982), Dept. of Chemistry, Oregon State University, Corvallis, OR
76. 4 concentration. Environ. Sci. Technol. 29 (1995) 951-959
77. 2+ binding sites in soil humic substances using X-ray absorption spectroscopy. Geochim. Cosmochim. Acta 61 (1997) 2211-2221
78. Xia K., Bleam W., and Helmke P.A. Studies of the nature of binding sites of first row transition elements bound to aquatic and soil humic substances using X-ray absorption spectroscopy. Geochim. Cosmochim. Acta 61 (1997) 2223-2235
79. Yee N., and Fein J.B. Cd adsorption onto bacterial surfaces: a universal adsorption edge?. Geochim. Cosmochim. Acta 65 (2001) 2037-2042
80. 3+ oxides in single phase suspensions and subsurface materials. Am. Mineral. 83 (1998) 1426-1443
81. Zachara J.M., Fredrickson J.K., Smith S.C., and Gassman P.L. Solubilization of Fe(III) oxide-bound trace metals by a dissimilatory Fe(III) reducing bacterium. Geochim. Cosmochim. Acta 65 (2001) 75-93