Applied Microbiology and Biotechnology

, Volume 68, Issue 1, pp 117–123 | Cite as

The mechanism of bacterial indigo reduction

Applied Microbial and Cell Physiology

Abstract

The reduction of water-insoluble indigo by the recently isolated moderate thermophile, Clostridium isatidis, has been studied with the aim of developing a sustainable technology for industrial indigo reduction. The ability to reduce indigo was not shared with C. aurantibutyricum, C. celatum and C. papyrosolvens, but C. papyrosolvens could reduce indigo carmine (5,5′-indigosulfonic acid), a soluble indigo derivative. The supernatant from cultures of C. isatidis, but not from cultures of the other bacteria tested, decreased indigo particle size to one-tenth diameter. Addition of madder powder, anthraquinone-2,6-disulfonic acid, and humic acid all stimulated indigo reduction by C. isatidis. Redox potentials of cultures of C. isatidis were about 100 mV more negative than those of C. aurantibutyricum, C. celatum and C. papyrosolvens, and reached −600 mV versus the SCE in the presence of indigo, but potentials were not consistently affected by the addition of the quinone compounds, which probably act by modifying the surface of the bacteria or indigo particles. It is concluded that C. isatidis can reduce indigo because (1) it produces an extracellular factor that decreases indigo particle size, and (2) it generates a sufficiently reducing potential.

Notes

Acknowledgements

We thank J. Edmonds, S. Mitchell, A.N. Padden and M. Robson for assistance; A. Cavaco-Paulo, F. Marken, M.D. Poonyth, and Spindigo Project colleagues and partners for useful discussions; and the European Commission Spindigo Project QLK5-CT-2000-30962 for financial support

References

  1. Andreaus J, Campos R, Gubitz G, Cavaco-Paulo A (2000) Influence of cellulases on indigo backstaining. Text Res J 70:628–632Google Scholar
  2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedGoogle Scholar
  3. Bechtold T, Burtscher E, Amann A, Bobleter O (1993) Alkali-stable iron complexes as mediators for the electrochemical reduction of dispersed organic dyestuffs. J Chem Soc Faraday Trans 89:2451–2456Google Scholar
  4. Bechtold T, Burtscher E, Turcanu A (1999) Anthraquinones as mediators for the indirect cathodic reduction of dispersed organics dyestuffs. J Anal Electrochem 465:80–87Google Scholar
  5. Bond AM, Marken F, Hill E, Compton RG, Hügel H. (1997) The electrochemical reduction of indigo dissolved in organic solvents and as a solid mechanically attached to a basal plane pyrolytic graphite electrode immersed in aqueous electrolyte solution. J Chem Soc Perkin Trans 2:1735–1742Google Scholar
  6. Campos R, Cavaco-Paulo A, Andreaus J, Gübitz G (2000) Indigo-cellulase interactions. Text Res J 70:532–536Google Scholar
  7. Cervantes FJ, Vu-Thi-Thu L, Lettinga G, Field JA (2004) Quinone-respiration improves dechlorination of carbon tetrachloride by anaerobic sludge. Appl Microbiol Biotechnol 64:702–711PubMedGoogle Scholar
  8. Chatterjee S, Mondal AK, Begum NA, Roychoudhury S, Das J (1998) Ordered cloned DNA map of the genome of Vibrio cholerae 569B and localization of genetic markers. J Bacteriol 180:901–908Google Scholar
  9. Clark WM (1960) Oxidation–reduction potentials of organic systems. Williams and Wilkins, Baltimore, Md., USAGoogle Scholar
  10. Compton RG, Perkin SJ, Gamblin DP, Davis J, Marken F, Padden AN, John P (2000) Clostridium isatidis colonised carbon electrodes: voltammetric evidence for direct solid state redox processes. New J Chem 24:179–181Google Scholar
  11. Davies GJ (1998) Structural studies on cellulases. Biochem Soc Trans 26:167–173PubMedGoogle Scholar
  12. Dos Santos AB, Bisschops IAE, Cervantes FJ, van Lier JB (2004) Effect of different redox mediators during thermophilic azo dye reduction by anaerobic granular sludge and comparative study between mesophilic (30 degrees C) and thermophilic (55 degrees C) treatments for decolourisation of textile waste waters. Chemosphere 55:1149–1157PubMedGoogle Scholar
  13. Gilbert KG, Cooke DT (2001) Dyes from plants: past usage, present understanding and potential. Plant Growth Regul 34:57–69Google Scholar
  14. Gusakov AV, Sinitsyn AP, Berlin AG, Markov AV, Ankudimova NV (2000) Surface hydrophobic amino acid residues in cellulase molecules as a structural factor responsible for their high denim-washing performance. Enzyme Microbiol Technol 27:664–671Google Scholar
  15. Gusakov AV, Sinitsyn AP, Markov AV, Skomarovsky AA, Sinitsyna OA, Ankudimova NV, Berlin AG (2001) Study of protein adsorption on indigo particles confirms the existence of enzyme-indigo interaction sites in cellulase molecules. J Biotechnol 87:83–90PubMedGoogle Scholar
  16. Hernandez ME, Newman DK (2001) Extracellular electron transfer. Cell Mol Life Sci 58:1562–1571PubMedGoogle Scholar
  17. Hurry JG (1930) The woad plant and its dye. Oxford University Press, LondonGoogle Scholar
  18. John P, Arghyros S, Nicholson SK (2005) Indigo-reducing bacteria from the medieval woad vat (Isatis tinctoria L.): some aspects of their interaction with indigo. Dyes Hist Archaeol (in press)Google Scholar
  19. Lovley DR, Coates JD, Blunt-Harris EL, Phillips EJP, Woodward JC (1996) Humic substances as electron acceptors for microbial respiration. Nature 382:445–448CrossRefGoogle Scholar
  20. Luu Y-S, Ramsay JA (2003) Review: microbial mechanisms of accessing insoluble Fe(III) as an energy source. World J Microbiol Biotechnol 19:215–225Google Scholar
  21. Matsushita O, Okabe A (2001) Clostridial hydrolytic enzymes degrading extracellular components. Toxicon 39:1769–1780PubMedGoogle Scholar
  22. Nevin KP, Lovley DR (2000) Lack of production of electron-shuttling compounds or solubilization of Fe(III) during reduction of insoluble Fe(III) oxide by Geobacter metallireducens. Appl Environ Microbiol 66:2248–2251CrossRefPubMedGoogle Scholar
  23. Newman DK, Kolter R (2000) A role for excreted quinones in extracellular electron transfer. Nature 405:94–97CrossRefPubMedGoogle Scholar
  24. Padden AN, Dillon VM, John P, Edmonds J, Collins MD, Alvarez N (1998) Clostridium used in mediaeval dyeing. Nature 396:225Google Scholar
  25. Padden AN, Dillon VM, Edmonds J, Collins MD, Alvarez N, John P (1999) An indigo-reducing moderate thermophile from a woad vat, Clostridium isatidis sp. nov. Int J Syst Bacteriol 49:1025–1031PubMedGoogle Scholar
  26. Padden AN, John P, Collins MD, Hutson R, Hall AR (2000) Indigo-reducing Clostridium isatidis isolated from a variety of sources, including a tenth century Viking woad vat. J Archaeol Sci 27:953–956CrossRefGoogle Scholar
  27. Prado AGS, Miranda BS, Jacintho GVM (2003) Interaction of indigo carmine dye with silica modified with humic acids at solid/liquid interface. Surf Sci 542:276–282Google Scholar
  28. Robson RL, Robson RM, Morris JG (1974) The biosynthesis of granulose by Clostridium pasteurianum. Biochem J 144:503–511PubMedGoogle Scholar
  29. Roessler A, Crettenand D, Dossenbach O, Rys P (2003a) Electrochemical reduction of indigo in fixed and fluidized beds of graphite granules. J Appl Electrochem 33:901–908Google Scholar
  30. Roessler A, Dossenbach O, Rys P (2003b) Electrocatalytic hydrogenation of indigo. J Electrochem Soc 150:D1–D5Google Scholar
  31. Roessler A, Jin X (2003) State of the art technologies and new electrochemical methods for the reduction of vat dyes. Dyes Pigments 59:223–235Google Scholar
  32. Rosso KM, Zachara JM, Fredrickson JK Gorby YA, Smith SC (2003) Nonlocal bacterial electron transfer to haematite surfaces. Geochim Cosmochim Acta 67:1081–1087Google Scholar
  33. Royer RA, Burgos WD, Fisher AS, Unz RF, Dempsey BA (2002) Enhancement of biological reduction of hematite by electron shuttling and Fe(II) complexation. Environ Sci Technol 36:1939–1946PubMedGoogle Scholar
  34. Shimizu T, Ohtani K, Hirakawa H, Ohshima K, Yamashita A, Shiba T, Ogasawara N, Hattori M, Kuhara S, Hayashi H (2002) Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater. Proc Natl Acad Sci USA 99:996–1001CrossRefPubMedGoogle Scholar
  35. Straub KL, Schink B (2003) Evaluation of electron-shuttling compounds in microbial ferric iron reduction. FEMS Microbiol Lett 220:229–233CrossRefPubMedGoogle Scholar
  36. Turick CE, Caccavo F, Tisa LS (2003) Electron transfer from Shewanella algae BrY to hydrous ferric oxide is mediated by cell-associated melanin. FEMS Microbiol Lett 220:99–104PubMedGoogle Scholar
  37. Vickerstaff T (1954) The physical chemistry of dyeing. Oliver and Boyd, LondonGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Plant Science Laboratories, School of Plant Sciences,The University of ReadingReadingUK

Personalised recommendations