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Relationship Between Sulphate Starvation and Chromate Reduction in a H2-fed Fixed-film Bioreactor

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Abstract

While developing a low-sulphate system combining indirect chromate-reduction by biologically-produced hydrogen sulphide and direct biological chromate-reduction to treat chromate-bearing waters, the aim of the present work was to evaluate the influence of sulphate and H2 starvation on chromate reduction. Chromate-reduction was performed under continuous-feed conditions in a fixed-film column bioreactor originally inoculated with a bacterial consortium containing Desulfomicrobium norvegicum, and fed with H2. With 500 mg l−1 of sulphate in the feed solution, total chromate-reduction was observed in the effluent whereas sulphate-reduction was strongly decreased, as also confirmed by measurements of isotopic ratios for sulphur. In the absence of sulphate, a chromate-reduction activity was still observed but was lower than in the presence of sulphate, and chromate-reduction was H2-dependent. Molecular biology techniques revealed the composition of the bacterial population in the effluent. D. norvegicum together with other micro-organisms of the Bacteria domain were detected. They include members related to the genera Acinetobacter, Acetobacterium and Rhodocyclus. Even when sulphate-reduction was strongly decreased, the presence of sulphate enhances the efficiency of the H2-dependent chromate-reduction. A H2- and CO2-consuming bacterial population may be used in a globally autotrophic process to reduce chromate at low sulphate concentration, thus avoiding excess sulphide production.

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References

  • Arias, Y. M., & Tebo, B. M. (2003). Cr(VI) reduction by sulphidogenic and non-sulphidogenic microbial consortia. Applied and Environmental Microbiology, 69, 1847–1853.

    Article  CAS  Google Scholar 

  • Battaglia-Brunet, F., Touze, S., Michel, C., & Ignatiadis, I. (2006). Treatment of a chromate-polluted groundwater in a 200-dm3 pilot bio-reactor fed with hydrogen. Journal of Chemical Technology and Biotechnology, 81, 1506–1513.

    Article  CAS  Google Scholar 

  • Battaglia-Brunet, F., Foucher, S., Denamur, A., Margraff, M., Morin, D., & Ignatiadis, I. (2004a). Chromate reduction at low sulphate concentration in hydrogen-fed bioreactors. Environmental Technology, 25(1), 101–109.

    Article  CAS  Google Scholar 

  • Battaglia-Brunet, F., Foucher, S., Morin, D., & Ignatiadis, I. (2004b). Chromate (\( {\rm CrO}^{{2 - }}_{4} \)) reduction in ground waters by using reductive bacteria in fixed-bed bioreactors. Water, Air & Soil Pollution, Focus, 4(4–5), 127–135.

    Article  CAS  Google Scholar 

  • Battaglia-Brunet, F., Foucher, S., Ignatiadis, I., Michel, C., & Morin, D. (2002). Reduction of chromate by fixed films of sulphate-reducing bacteria using hydrogen as electron source. Journal of Industrial Microbiology & Biotechnology, 28, 154–159.

    Article  CAS  Google Scholar 

  • Benson, D., Boguski, M. S., Lipman, D. J., Ostell, J., Ouellette, B. F., Rapp, B. A., et al. (1999). GenBank. Nucleic Acids Research, 27, 12–17.

    Article  CAS  Google Scholar 

  • Bhide, J. V., Dhakephalkar, P. K., & Paknikar, K. M. (1996). Microbiological process for the removal of Cr(VI) from chromate-bearing cooling tower effluent. Biotechnology Letters, 18, 667–672.

    Article  CAS  Google Scholar 

  • Blasiak, J., & Kowalik, J. (2000). A comparison of the in vitro genotoxicity of tri- and hexavalent chromium. Mutation Research, 469, 135–145.

    CAS  Google Scholar 

  • Böttcher, M. E., Brumsack, H. J., & De Lange, G. J. (1998a). Sulphate reduction and related stable isotope (34S, 18O) variations in interstitial waters from the Eastern Mediterranean. Proceedings of Ocean Drilling Program, Scientific Results, 160, 365–373.

    Google Scholar 

  • Böttcher, M. E., Oelshläger, B., Höpner, T., Brumsack, H. J., & Rullkötter, J. (1998b). Sulphate reduction related to the early diagenesic degradation of organic matter and “black spot” formation in tidal sandflats of the German Wadden Sea (Southern North Sea): Stable isotope (13C, 34S, 18O) and other geochemical results. Organic Geochemistry, 29, 1517–1560.

    Article  Google Scholar 

  • Caron, F., Tessier, A., Kramer, J. R., Schwarcz, H. P., & Rees, C. E. (1986). Sulphur and oxygen isotopes of sulphate in precipitation and lakewater, Quebec, Canada. Applied Geochemistry, 1, 601–606.

    Article  CAS  Google Scholar 

  • Cervantes, C. (1991). Bacterial interaction with chromate. Antonie van Leeuwenhoek, 59, 229–233.

    Article  CAS  Google Scholar 

  • Chardin, B., Giudici-Orticoni, M. T., De Luca, G., Guigliarelli, B., & Bruschi, M. (2003). Hydrogenases in sulphate-reducing bacteria function as chromium reductase. Applied Microbiology and Biotechnology, 63, 315–321.

    Article  CAS  Google Scholar 

  • Cheung, K. H., & Gu, J. D. (2003). Reduction of chromate (\( {\rm CrO}^{{2 - }}_{4} \)) by an enrichment consortium and an isolate of marine sulphate-reducing bacteria. Chemosphere, 52, 1523–1529.

    Article  CAS  Google Scholar 

  • Chulsung, K., Gunhui, Z., Baolin, D., Thornton, E. C., & Huifang, X. (2001). Chromium(VI) reduction by hydrogen sulphide in aqueous media: Stoichiometry and kinetics. Environmental Science and Technology, 35, 2219–2225.

    Article  CAS  Google Scholar 

  • Cole, J. R., Chai, B., Marsh, T. L., Farris, R. J., Wang, Q., Kulam, S. A., et al. (2003). The Ribosomal Database Project (RDP-II): Previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Research, 31, 442–443.

    Article  CAS  Google Scholar 

  • Dilek, F. B., & Gökçay, C. F. (1996). Microbiology of activated sludge treating wastewater containing Ni(II) and Cr(VI). Water Science and Technology, 34, 183–191.

    Article  CAS  Google Scholar 

  • Epstein, S. & Mayeda, T. (1953). Variation of 18O content of waters from natural sources. Geochimica et Cosmochimica Acta, 4, 213–224.

    Article  CAS  Google Scholar 

  • Fauque, G., & Ollivier, O. (2003). Anaerobes: The sulphate-reducing bacteria as an example of metabolic diversity. In A. T. Bull (Ed.) Microbial Diversity and Bioprospecting (vol. 17, pp. 169–176). Washington: ASM.

    Google Scholar 

  • Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39, 783–791.

    Article  Google Scholar 

  • Francisco, R., Alpoim, M. C., & Morais, P. V. (2002). Diversity of chromium-resistant and -reducing bacteria in a chromium-contaminated activated sludge. Journal of Applied Microbiology, 92, 837–843.

    Article  CAS  Google Scholar 

  • Gruber, J. E., & Jennette, K. W. (1978). Metabolism of the carcinogen chromate by rat liver microsomes. Biochemical and Biophysical Research Communications, 82, 700–706.

    Article  CAS  Google Scholar 

  • Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

    CAS  Google Scholar 

  • Horita, J., Ueda, A., Mizukami, K., & Takatori, I. (1989). Automatic δD and δ18O analyses of multi-water samples using H2- and CO2-water equilibration methods with a common equilibration set-up. Applied Radiation and Isotopes, 40, 801–805.

    Article  CAS  Google Scholar 

  • Joulian, C., Ramsing, N. B., & Ingvorsen, K. (2001). Congruent phylogenies of most common small-subunit rRNA and dissimilatory sulphite reductase gene sequences retrieved from estuarine sediments. Applied and Environmental Microbiology, 67, 3314–3318.

    Article  CAS  Google Scholar 

  • Jukes, T. H., & Cantor, C. R. (1969). Evolution of protein molecules. In H. N. Munro (Ed.) Mammalian Protein Metabolism (pp. 211–232). New York: Academic.

    Google Scholar 

  • Kim, C., Zhou, Q., Deng, B., Thornton, E., & Xu, H. (2001). Chromium reduction by hydrogen sulphide in aqueous media: Stoichiometry and kinetics. Environmental Science and Technology, 35, 2219–2225.

    Article  CAS  Google Scholar 

  • Kimura, M. (1980). A simple model for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120.

    Article  CAS  Google Scholar 

  • Krumholz, L. R., Harris, S. H., Tay, S. T., & Sulfita, J. M. (1999). Characterization of two subsurface H2-utilizing bacteria, Desulfomicrobium hypogeium sp. nov. and Acetobacterium psammolithicum sp. nov. and their ecological roles. Applied and Environmental Microbiology, 65, 2300–2306.

    CAS  Google Scholar 

  • Lojou, E., Bianco, P., & Bruschi, M. (1998). Kinetic studies on the electron transfer between bacterial c-type cytochromes and metal oxides. Journal of Electroanalytical Chemistry and Interfacial Electrochemistry, 452, 167–177.

    CAS  Google Scholar 

  • Lomans, B. P., Leijdekkers, P., Wesselink, J.-J., Bakkes, P., Pol, A., van der Drift, C., et al. (1991). Obligate sulphide-dependent degradation of methoxylated aromatic compounds and formation of methanethiol and dimethyl sulphide by a freshwater sediment isolate, Parasporobacterium paucivorans gen. nov., sp. nov. Applied and Environmental Microbiology, 67, 4017–4023.

    Article  Google Scholar 

  • Lovley, D. R. (1994). Microbial reduction of iron, manganese and other metals. Advances in Agronomy, 54, 175–229.

    Article  Google Scholar 

  • Lovley, D. R., & Phillips, E. J. P. (1994). Reduction of chromate by Desulfovibrio vulgaris and its c3 cytochrome. Applied and Environmental Microbiology, 60, 726–728.

    CAS  Google Scholar 

  • Lupton, F. S., DeFilippi, L. J., & Goodman, J.R. (1991). Bioremediation of chromium (VI) contaminated aqueous systems by sulphate reducing bacteria. US patent n° 5,062,956.

  • Michel, C., Brugna, M., Aubert, C., Bernadac, A., & Bruschi, M. (2001). Enzymatic reduction of chromate: Comparative studies using sulphate-reducing bacteria. Key role of polyheme cytochromes c and hydrogenases. Applied Microbiology and Biotechnology, 55, 95–100.

    Article  CAS  Google Scholar 

  • Pettine, M., Millero, F. J., & Passiro, R. (1994). Reduction of chromium (VI) with hydrogen sulphide in NaCl media. Marine Chemistry, 46, 335–344.

    Article  CAS  Google Scholar 

  • Rai, D., Moore, D. A., Hess, N. J., Rao, L., & Clark, S. B. (2004). Chromium(III) hydroxide solubility in the aqueous \({\text{Na}}^{ + } - {\text{OH}}^{ - } - {\text{H}}_{2} {\text{PO}}^{ - }_{4} - {\text{HPO}}^{{2 - }}_{4} - {\text{PO}}^{3}_{4} - {\text{H}}_{2} {\text{O}}\) system. A thermodynamic model. Journal of Solution Chemistry, 33, 1213–1242.

    Article  CAS  Google Scholar 

  • Rai, D., Sass, B. M., & Moore, D. A. (1987). Chromium (III) hydrolysis constants and solubility of chromium (III) hydroxide. Inorganic Chemistry, 26, 345–349.

    Article  CAS  Google Scholar 

  • Saitou, N., & Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 405–425.

    Google Scholar 

  • Sakai, H., & Krouse, H. R. (1971). Elimination of memory effects in 18O–16O determination in sulphates. Earth and Planetary Science Letters, 11, 361–373.

    Article  Google Scholar 

  • Smith, W., & Gadd, G. (2000). Reduction and precipitation of chromate by mixed culture sulphate-reducing bacterial biofilms. Journal of Applied Microbiology, 88, 983–991.

    Article  CAS  Google Scholar 

  • Sinha, S. N., & Barnerjee, R. D. (1997). Ecological role of thiosulphate and sulphide utilizing purple nonsulphur bacteria of a riverine ecosystem. FEMS Microbiology Ecology, 24, 211–220.

    Article  CAS  Google Scholar 

  • Tebo, B. M., & Obraztsova, A. Y. (1998). Sulphate-reducing bacterium grows with Cr(VI), U(VI), Mn(IV), and Fe(III) as electron acceptors. FEMS Microbiology Letters, 162, 193–198.

    Article  CAS  Google Scholar 

  • Thode, H. G., Monster, J., & Dunford, H. B. (1961). Sulphur isotope geochemistry. Geochimica and Cosmochimica Acta, 25, 50–174.

    Article  Google Scholar 

  • Thomsen, T. R., Finster, K., & Ramsing, N. B. (2001). Biogeochemical and molecular signatures of anaerobic methane oxidation in a marine sediment. Applied and Environmental Microbiology, 67, 1646–1656.

    Article  CAS  Google Scholar 

  • Turick, C. E., & Appel, W. A. (1997). Method for in situ or ex situ bioremediation of hexavalent chromium contaminated soils and/or groundwater. US Patent n° 5,681,739.

  • Turpeinen, R., Kairesalo, T., & Häggblom, M. M. (2004). Microbial community structure and activity in arsenic-, chromium- and copper- contaminated soils. FEMS Microbiology Ecology, 47, 39–50.

    Article  CAS  Google Scholar 

  • Vainshtein, M., Kuschk, P., Mattusch, J., Vatsourina, A., & Wiessner, A. (2003). Model experiments on the microbial removal of chromium from contaminated groundwater. Water Research, 37, 1401–1405.

    Article  CAS  Google Scholar 

  • Van de Peer, Y., & De Wachter, R. (1994). TREECON for Windows: A software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Computer Applications in the Biosciences, 10, 569–570.

    Google Scholar 

  • Wagner, M., Roger, A., Flax, J., Brusseau, G. & Stahl, D. (1998). Phylogeny of dissimilatory sulphite reductases supports an early origin of sulphate respiration. Journal of Bacteriology, 180, 2975–2982.

    CAS  Google Scholar 

  • Wang, Y. T. (2000). Microbial reduction of chromate. In D. R. Lovley (Ed.), Environmental microbe-metal interactions, chap. 10 (pp. 225–235). Washington D.C.: ASM.

    Google Scholar 

  • Zilles, J. L., Peccia, J., Kim, M. W., Hung, C. H., & Noguera, D. R. (2002). Involvement of Rhodocyclus-related organisms in phosphorus removal in full-scale wastewater treatment plants. Applied and Environmental Microbiology, 68, 2763–2769.

    Article  CAS  Google Scholar 

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Acknowledgements

This is the BRGM contribution n° 02811. This work was carried out in the framework of the Commission of European Union contract no EVK1-CT-1999-00033 (METALBIOREDUCTION project) and received financial support from a BRGM research project (BIOPROC project). We thank M. Marggraff from Munters-Euroform for providing filling materials and C. Flehoc from Metrology, Monitoring and Analysis Division, BRGM/MMA, for the isotopic determinations.

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  1. BRGM, Environment and Process Division, 3 av. Claude Guillemin, BP 36009, 45060, Orleans, Cedex 2, France

    F. Battaglia-Brunet, C. Michel, C. Joulian & I. Ignatiadis

  2. IRD, UR 101, Laboratoire de Microbiologie, CESB-ESIL, 13288, Marseille Cedex 9, France

    C. Joulian & B. Ollivier

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  1. F. Battaglia-Brunet
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  2. C. Michel
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  3. C. Joulian
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  5. I. Ignatiadis
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Correspondence to I. Ignatiadis.

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Battaglia-Brunet, F., Michel, C., Joulian, C. et al. Relationship Between Sulphate Starvation and Chromate Reduction in a H2-fed Fixed-film Bioreactor. Water Air Soil Pollut 183, 341–353 (2007). https://doi.org/10.1007/s11270-007-9383-3

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