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

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.

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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 35:217–233

  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 19:65–72

  3. Arnold RG, Hoffmann MR, DiChristina TJ, Picardal FW (1990) Regulation of dissimilatory Fe(III) reduction activity in Shewanella putrefaciens. Appl Environ Microbiol 56:2811–2817

  4. Beliaev AS, Saffarini DA (1998) Shewanella putrefaciens mtrB encodes an outer membrane protein required for Fe(III) and Mn(IV) reduction. J Bacteriol 180:6292–6297

  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 72:248–254

  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 91:243–248

  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 37:2323–2328

  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 34:100–106

  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 69:3517–3525

  10. DiChristina TJ (1992) Effects of nitrate and nitrite on dissimilatory iron reduction by Shewanella putrefaciens 200. J Bacteriol 174:1891–1896

  11. Esteve-Núňez A, Núňez C, Lovley DR (2004) Preferential reduction of Fe(III) over fumarate by Geobacter sulfurreducens. J Bacteriol 186:2897–2899

  12. Feinberg LF, Holden JF (2006) Characterization of dissimilatory Fe(III) versus NO3 reduction in the hyperthermophilic archaeon Pyrobaculum aerophilum. J Bacteriol 188:525–531

  13. Gorby AY, Lovley DR (1991) Electron transport in dissimilatory iron reducer GS-15. Appl Environ Microbiol 57:867–870

  14. He Q, Sanford RAM (2003) Characterization of Fe(III) reduction by chlororespiring Anaeromxyobacter dehalogenans. Appl Environ Microbiol 69:2712–2718

  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 https://doi.org/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 https://doi.org/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 38:1183–1192

  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 63:3684–3690

  19. Knight V, Blakmore R (1998) Reduction of diverse electron acceptors by Aeromonas hydrophila. Arch Microbiol 169:239–248

  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 63:3691–3694

  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 35:1385–1393

  22. Lovley DR (2003) Cleaning up with genomics: applying molecular biology to bioremediation. Nat Rev Microbiol 1:36–44

  23. Lovley DR, Baedecker MJ, Lonergan DJ, Cozzarelli IM, Phillips EJP, Siegel DI (1989) Oxidation of aromatic contaminants coupled to microbial iron reduction. Nature 339:297–299

  24. Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe(III) and Mn (IV) reduction. Adv Microb Physiol 49:219–286

  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 70:837–844

  26. Myers CR, Myers JM (1993) Ferric iron reductase is associated with the membranes of anaerobically grown Shewanella putrefaciens MR-1. FEMS Microbiol Lett 108:15–22

  27. Pearce CI, Lloyd JR, Guthrie JT (2003) The removal of colour from textile wastewater using whole bacterial cells: a review. Dyes Pigm 58:179–196

  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 95:692–703

  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 278:27758–27765

  30. Rafii F, Franklin W, Cerniglia CE (1990) Azoreductase activity of anaerobic bacteria isolated from human intestinal microflora. Appl Environ Microbiol 56:2146–2151

  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 71:3882–3888

  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 36:1497–1504

  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 41:1733–1748

  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 70:56–70

  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 72:2925–2935

  36. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

  37. Stolz A (2001) Basic and applied aspects in the microbial degradation of azo dyes. Appl Microbiol Biotechnol 56:69–80

  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 75:691–701

  39. Woźnica A, Dzirba J, Mańka D, Łabużek S (2003) Effects of electron transport inhibitors on iron reduction in Aeromonas hydrophila strain KB1. Anaerobe 9:125–130

  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 40:3986–3995

  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 55:363–368

  42. Xu M, Guo J, Zeng G, Zhong X, Sun G (2006) Decolorization of anthraquinone dye by Shewanella decolorationis S12. Appl Microbiol Biotechnol 71:246–251

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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.

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Correspondence to Guoping Sun.

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Xu, M., Guo, J., Kong, X. et al. Fe(III)-enhanced Azo Reduction by Shewanella decolorationis S12. Appl Microbiol Biotechnol 74, 1342–1349 (2007). https://doi.org/10.1007/s00253-006-0773-z

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Keywords

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