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Applied Microbiology and Biotechnology

, Volume 74, Issue 6, pp 1342–1349 | Cite as

Fe(III)-enhanced Azo Reduction by Shewanella decolorationis S12

  • Meiying Xu
  • Jun Guo
  • Xiangyi Kong
  • Xingjuan Chen
  • Guoping SunEmail author
Applied microbial and cell physiology

Abstract

Shewanella decolorationis S12 is capable of high rates of azo dye decolorization and dissimilatory Fe(III) reduction. Under anaerobic conditions, when Fe(III) and azo dye were copresent in S12 cultures, dissimilatory Fe(III) reduction and azo dye biodecolorization occurred simultaneously. Furthermore, the dye decolorization was enhanced by the presence of Fe(III). When 1 mM Fe(III) was added, the methyl red decolorizing efficiency was 72.1% after cultivation for 3 h, whereas the decolorizing efficiency was only 60.5% in Fe(III)-free medium. The decolorizing efficiencies increased as the concentration of Fe(III) was increased from 0 to 6 mM. Enzyme activities, which mediate the dye decolorization and Fe(III) reduction, were not affected by preadaption of cells to Fe(III) and azo dye nor by the addition of chloramphenicol. Both the Fe(III) reductase and the azo reductase were membrane associated. The respiratory electron transport chain inhibitors metyrapone, dicumarol, and stigmatellin showed significantly different effects on Fe(III) reduction than on azo dye decolorization.

Keywords

Dissimilatory Fe(III) reduction Azo dye decolorization Shewanella decolorationis S12 Enhancement 

Notes

Acknowledgments

This research was supported by Chinese National Natural Science Foundations (3050009 and 30670020), Guangdong Provincial key Programs for Science and Technology Development (05100365), Guangdong Provincial Natural Science Foundation (No.015017), Guangdong Provincial Programs for Science and Technology Development (2006B36703001), and Guangzhou Programs for Science and Technology Development (2006Z3-E0461). In addition, Dr. Joy D. Van Nostrand was very kind to correct the language errors. Finally, we would like to thank the three anonymous reviewers for useful and constructive comments.

References

  1. Abdelouas A, Liu Y, Lutze W, Nuttall HE (1998) Reduction of U(VI) to U(IV) by indigenous bacteria in contaminated ground water. J Contam Hydrol 35:217–233CrossRefGoogle Scholar
  2. Achtnich CA, Bak F, Conrad R (1995) Competition for electron donors among nitrate reducers, ferric iron reducers, sulfate reducers, and methanogens in anoxic paddy soil. Biol Fertil Soils 19:65–72CrossRefGoogle Scholar
  3. Arnold RG, Hoffmann MR, DiChristina TJ, Picardal FW (1990) Regulation of dissimilatory Fe(III) reduction activity in Shewanella putrefaciens. Appl Environ Microbiol 56:2811–2817Google Scholar
  4. Beliaev AS, Saffarini DA (1998) Shewanella putrefaciens mtrB encodes an outer membrane protein required for Fe(III) and Mn(IV) reduction. J Bacteriol 180:6292–6297Google Scholar
  5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  6. Chang J-S, Chen B-Y, Lin Y-S (2004) Stimulation of bacterial decolorization of an azo dye by extracellular metabolites from Escherichia coli strain NO3. Biores Technol 91:243–248CrossRefGoogle Scholar
  7. Clément J-C, Shrestha J, Ehrenfeld JG, Jaffé PR (2005) Ammonium oxidation coupled to dissimilatory reduction of iron under anaerobic conditions in wetland soils. Soil Biol Biochem 37:2323–2328CrossRefGoogle Scholar
  8. Cooper DC, Picardal F, Rivera J, Talbot C (2000) Zinc immobilization and magnetite formation via ferric oxide reduction by Shewanella putrefaciens 200. Environ Sci Technol 34:100–106CrossRefGoogle Scholar
  9. Cooper DC, Picardal FW, Schimmelmann A, Coby AJ (2003) Chemical and biological interactions during nitrate and goethite reduction by Shewanella putrefaciens 200. Appl Environ Microbiol 69:3517–3525CrossRefGoogle Scholar
  10. DiChristina TJ (1992) Effects of nitrate and nitrite on dissimilatory iron reduction by Shewanella putrefaciens 200. J Bacteriol 174:1891–1896Google Scholar
  11. Esteve-Núňez A, Núňez C, Lovley DR (2004) Preferential reduction of Fe(III) over fumarate by Geobacter sulfurreducens. J Bacteriol 186:2897–2899CrossRefGoogle Scholar
  12. Feinberg LF, Holden JF (2006) Characterization of dissimilatory Fe(III) versus NO3 reduction in the hyperthermophilic archaeon Pyrobaculum aerophilum. J Bacteriol 188:525–531CrossRefGoogle Scholar
  13. Gorby AY, Lovley DR (1991) Electron transport in dissimilatory iron reducer GS-15. Appl Environ Microbiol 57:867–870Google Scholar
  14. He Q, Sanford RAM (2003) Characterization of Fe(III) reduction by chlororespiring Anaeromxyobacter dehalogenans. Appl Environ Microbiol 69:2712–2718CrossRefGoogle Scholar
  15. Hong Y, Xu M, Guo J, Xu Z, Chen X, Sun G (2006a) Respiration and growth of Shewanella decolorationis S12 with azo compound as sole electron acceptor. Appl Environ Microbiol. DOI 10.1128/AEM.01415-06
  16. Hong Y, Chen X, Guo J, Xu Z, Xu M, Sun G (2006b) Effects of electron donors and acceptors on anaerobic reduction of azo dyes by Shewanella decolorationis S12. Appl Microbiol Biotechnol. DOI 10.1007/s00253-006-0657-2
  17. Isik M, Sponza DT (2003) Effect of oxygen on decolorization of azo dyes by Escherichia coli and Pseudomonas sp. and fate of aromatic amines. Process Biochem 38:1183–1192CrossRefGoogle Scholar
  18. Keck A, Klein J, Kudlich M, Stolz A, Knackmuss HJ, Mattes R (1997) Reduction of azo dyes by redox mediators originating in the naphthalenesulfonic acid degradation pathway of Sphingomonas sp. strain BN6. Appl Environ Microbiol 63:3684–3690Google Scholar
  19. Knight V, Blakmore R (1998) Reduction of diverse electron acceptors by Aeromonas hydrophila. Arch Microbiol 169:239–248CrossRefGoogle Scholar
  20. Kudlich M, Keck A, Klein J, Stolz A (1997) Localization of the enzyme system involved in anaerobic reduction of azo dyes by Sphingomonas sp. strain BN6 and effect of artificial redox mediators on the rate of azo dye reduction. Appl Environ Microbiol 63:3691–3694Google Scholar
  21. Liu CG, Zachara JM, Gorby YA, Szecsody JE, Brown CF (2001) Microbial reduction of Fe(III) and sorption/precipitation of Fe (II) on Shewanella putrefaciens strain CN32. Environ Sci Technol 35:1385–1393CrossRefGoogle Scholar
  22. Lovley DR (2003) Cleaning up with genomics: applying molecular biology to bioremediation. Nat Rev Microbiol 1:36–44CrossRefGoogle Scholar
  23. Lovley DR, Baedecker MJ, Lonergan DJ, Cozzarelli IM, Phillips EJP, Siegel DI (1989) Oxidation of aromatic contaminants coupled to microbial iron reduction. Nature 339:297–299CrossRefGoogle Scholar
  24. Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe(III) and Mn (IV) reduction. Adv Microb Physiol 49:219–286Google Scholar
  25. Maier J, Kandelbauer A, Erlacher A, Cavaco-Paulo A, Gübitz GM (2004) A new alkali-thermostable azoreductase from Bacillus sp. strain SF. Appl Environ Microbiol 70:837–844CrossRefGoogle Scholar
  26. Myers CR, Myers JM (1993) Ferric iron reductase is associated with the membranes of anaerobically grown Shewanella putrefaciens MR-1. FEMS Microbiol Lett 108:15–22CrossRefGoogle Scholar
  27. Pearce CI, Lloyd JR, Guthrie JT (2003) The removal of colour from textile wastewater using whole bacterial cells: a review. Dyes Pigm 58:179–196CrossRefGoogle Scholar
  28. Pearce CI, Christie R, Boothman C, von Canstein H, Guthrie JT, Lloyd JR (2006) Reactive azo dye reduction by Shewanella strain J18 143. Biotechnol Bioeng 95:692–703CrossRefGoogle Scholar
  29. Pitts KE, Dobbin PS, Reyes-Ramirez F, Thomson AJ, Richardson DJ, Seward HE (2003) Characterization of the Shewanella oneidensis MR-1 decaheme cytochrome MtrA. J Biol Chem 278:27758–27765CrossRefGoogle Scholar
  30. Rafii F, Franklin W, Cerniglia CE (1990) Azoreductase activity of anaerobic bacteria isolated from human intestinal microflora. Appl Environ Microbiol 56:2146–2151Google Scholar
  31. Ramalho PA, Paiva S, Cavaco-Paulo A, Casal M, Cardoso MH, Ramalho MT (2005) Azo reductase activity of intact Saccharomyces cerevisiae cells is dependent on the Fre1p component of plasma membrane ferric reductase. Appl Environ Microbiol 71:3882–3888CrossRefGoogle Scholar
  32. Rau J, Knackmuss H-J, Stolz A (2002) Effects of different quinoid redox mediators on the anaerobic reduction of azo dyes by bacteria. Environ Sci Technol 36:1497–1504CrossRefGoogle Scholar
  33. Roden EE, Wetzel RG (1996) Organic carbon oxidation and suppression of methane production by microbial Fe(III) oxide reduction in vegetated and unvegetated freshwater wetland sediments. Limnol Oceanogr 41:1733–1748CrossRefGoogle Scholar
  34. Ruebush SS, Icopini GA, Brantley SL, Tien M (2006a) In vitro enzymatic reduction kinetics of mineral oxides by membrane fractions from Shewanella oneidensis MR-1. Geochim Cosmochim Acta 70:56–70CrossRefGoogle Scholar
  35. Ruebush SS, Brantley SL, Tien M (2006b) Reduction of soluble and insoluble iron forms by membrane fractions of Shewanella oneidensis grown under aerobic and anaerobic conditions. Appl Environ Microbiol 72:2925–2935CrossRefGoogle Scholar
  36. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NYGoogle Scholar
  37. Stolz A (2001) Basic and applied aspects in the microbial degradation of azo dyes. Appl Microbiol Biotechnol 56:69–80CrossRefGoogle Scholar
  38. van der Zee FP, Bouwman RHM, Strik DPBT, Lettinga G, Field JA (2001) Accelerate the transformation of reactive azo dyes in anaerobic bioreactors. Biotechnol Bioeng 75:691–701CrossRefGoogle Scholar
  39. Woźnica A, Dzirba J, Mańka D, Łabużek S (2003) Effects of electron transport inhibitors on iron reduction in Aeromonas hydrophila strain KB1. Anaerobe 9:125–130CrossRefGoogle Scholar
  40. Wu WM, Carley J, Gentry T, Ginder-Vogel MA, Fienen M, Mehlhom T, Yan H, Caroll S, Pace MN, Nyman J, Luo J, Gentile ME, Fields MW, Hickey RF, Gu BH, Watson D, Cirpka OA, Zhou JZ, Fendorf S, Kitanidis PK, Jardine PM, Criddle CS (2006) Pilot-scale in situ bioremediation of uranium in a highly contaminated aquifer. 2. Reduction of U(VI) and geochemical control of U(VI) bioavailability, Environ Sci Technol 40:3986–3995CrossRefGoogle Scholar
  41. Xu M, Guo J, Cen Y, Zhong Xn, Cao W, Sun G (2005) Shewanella decolorationis sp. nov., decolorizing bacterium isolated from activated sludge of a waste-water treatment plant. Int J Syst Evol Microbiol 55:363–368CrossRefGoogle Scholar
  42. Xu M, Guo J, Zeng G, Zhong X, Sun G (2006) Decolorization of anthraquinone dye by Shewanella decolorationis S12. Appl Microbiol Biotechnol 71:246–251CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Meiying Xu
    • 1
    • 2
  • Jun Guo
    • 1
    • 2
  • Xiangyi Kong
    • 1
    • 2
  • Xingjuan Chen
    • 1
    • 2
  • Guoping Sun
    • 1
    • 2
    Email author
  1. 1.Guangdong Institute of MicrobiologyGuangzhouPeople’s Republic of China
  2. 2.Guangdong Provincial Key Lab of Microbial Culture Collection and ApplicationGuangzhouPeople’s Republic of China

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