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Archives of Microbiology

, Volume 157, Issue 2, pp 161–168 | Cite as

Oxidation of reduced sulphur compounds by intact cells of Thiobacillus acidophilus

  • Rogier Meulenberg
  • Jack T. Pronk
  • Wim Hazeu
  • Piet Bos
  • J. Gijs Kuenen
Original Papers
  • 69 Downloads

Abstract

Oxidation of reduced sulphur compounds by Thiobacillus acidophilus was studied with cell suspensions from heterotrophic and mixotrophic chemostat cultures. Maximum substrate-dependent oxygen uptake rates and affinities observed with cell suspensions from mixotrophic cultures were higher than with heterotrophically grown cells. ph Optima for oxidation of sulphur compounds fell within the pH range for growth (pH 2–5), except for sulphite oxidation (optimum at pH 5.5). During oxidation of sulphide by cell suspensions, intermediary sulphur was formed. Tetrathionate was formed as an intermediate during aerobic incubation with thiosulphate and trithionate. Whether or not sulphite is an inter-mediate during sulphur compound oxidation by T. acidophilus remains unclear. Experiments with anaerobic cell suspensions of T. acidophilus revealed that trithionate metabolism was initiated by a hydrolytic cleavage yielding thiosulphate and sulphate. A hydrolytic cleavage was also implicated in the metabolism of tetrathionate. After anaerobic incubation of T. acidophilus with tetrathionate, the substrate was completely converted to equimolar amounts of thiosulphate, sulphur and sulphate. Sulphide- and sulphite oxidation were partly inhibited by the protonophore uncouplers 2,4-dinitrophenol (DNP) and carbonyl cyanide m-chlorophenylhydrazone (CCCP) and by the sulfhydryl-binding agent N-ethylmaleimide (NEM). Oxidation of elemental sulphur was completely inhibited by these compounds. Oxidation of thiosulphate, tetrathionate and trithionate was only slightly affected. The possible localization of the different enzyme systems involved in sulphur compound oxidation by T. acidophilus is discussed.

Key words

Thiobacillus acidophilus Acidophiles Sulphur metabolism Sulphide Elemental sulphur Thiosulphate Tetrathionate Trithionate Sulphite Hydrolytic polythionate cleavage 

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References

  1. Bacon M, Ingledew WJ (1989) The reductive reactions of Thiobacillus ferrooxidans on sulphur and selenium. FEMS Microbiol Lett 58: 189–194CrossRefGoogle Scholar
  2. Guay R, Silver M (1975) Thiobacillus acidophilus sp. nov.; isolation and some physiological characteristics. Can J Microbiol 21: 281–288CrossRefGoogle Scholar
  3. Hanes CS (1932) Studies on plant amylases. I. The effect of starch concentration upon the velocity of hydrolysis by the amylase of germinated barley. Biochem J 26: 1406–1421CrossRefGoogle Scholar
  4. Hazeu W, Bijleveld W, Grotenhuis JTC, Kakes E, Kuenen JG (1986) Kinetics and energetics of reduced sulfur oxidation by chemostat cultures of Thiobacillus ferrooxidans. Antonie van Leeuwenhoek 52: 507–518CrossRefGoogle Scholar
  5. Hazeu W, Batenburg-van der Vegte WH, Bos P, Pas RK van der, Kuenen JG (1988) The production and utilization of inter-mediary sulfur during the oxidation of reduced sulfur compounds by Thiobacillus ferrooxidans. Arch Microbiol 150: 574–579CrossRefGoogle Scholar
  6. Hooper AB, DiSpirito AA (1985) In bacteria which grow on simple reductants, generation of a proton gradient involves extracytoplasmic oxidation of substrate. Microbiol Rev 49: 140–157PubMedPubMedCentralGoogle Scholar
  7. Ingledew WJ (1982) Thiobacillus ferrooxidans. the bioenergetics of an acidophilic chemolithotroph. Biochim Biophys Acta 683: 89–117CrossRefGoogle Scholar
  8. Kelly DP (1985) Physiology of the thiobacilli: elucidating the sulphur oxidation pathway. Microbiol Sci 2: 105–109PubMedGoogle Scholar
  9. Kelly DP (1989) Physiology and biochemistry of unicellular sulfur bacteria. In: Schlegel HG, Bowien B (eds) Autotrophic bacteria. Springer, Berlin Heidelberg New York, pp 193–219Google Scholar
  10. Kelly DP, Chambers LA, Trudinger PA (1969) Cyanolysis and spectrophotometric estimation of trithionate in mixture with thiosulphate and tetrathionate. Anal Chem 41: 898–901CrossRefGoogle Scholar
  11. Kodama A, Mori T (1968) Studies on the metabolism of a sulfuroxidizing bacterium IV. Growth and oxidation of sulfur compounds in T. thiooxidans. Plant Cell Physiol 9: 709–723Google Scholar
  12. Lu WP, Kelly DP (1984) Oxidation of inorganic sulphur compounds by thiobacilli. In: Crawford RL, Hanson RS (eds) Microbial growth on C1 compounds. American Society for Microbiology, Washington DC, pp 34–41Google Scholar
  13. Lu WP, Kelly DP (1988) Kinetic and energetic aspects of inorganic sulphur compound oxidation by Thiobacillus tepidarius. J Gen Microbiol 134: 865–876Google Scholar
  14. Mason J, Kelly DP, Wood AP (1987) Chemolithotrophic and autotrophic growth of Thermotrix thiopara and some thiobacilli on thiosulphate and polythionates, a reassessment of the growth yields of T. thiopara in chemostat cultures. J Gen Microbiol 33: 1249–1256Google Scholar
  15. Naito K, Hayata H, Mochizuki M (1975) The reactions of polythionates; kinetics of the cleavage of the trithionate ion in aqueous solutions. J Inorg Nucleic Chem 37: 1453–1457CrossRefGoogle Scholar
  16. Norris PR, Marsh RM, Lindstrom EB (1986) Growth of mesophilic and thermophilic acidophilic bacteria on sulphur and tetrathionate. Biotechnol Appl Biochem 8: 313–329Google Scholar
  17. Norris PR, Kelly DP (1988) Biohydrometallurgy. Proc Int Symp Warwick 1987, 578 pp, Science and Technology Letters, Kew, 578 ppGoogle Scholar
  18. Okuzumi M (1966) studies on biochemistry of the thiobacilli. VIII. Dismutation of tetrathionate by T. thiooxidans. Agric Biol Chem 30: 313–318Google Scholar
  19. Okuzumi M, Kita Y (1965) Studies on biochemistry of the thiobacilli, part VI. Oxidation of thiosulphate to tetrathionate by T. thiooxidans. Agric Biol Chem 29: 1063–1068Google Scholar
  20. Pronk JT, Meesters PJW, vanDijken JP, Bos P, Kuenen JG (1990a) Heterotrophic growth of Thiobacillus acidophilus in batch and chemostat cultures. Arch Microbiol 153: 392–398CrossRefGoogle Scholar
  21. Pronk JT, Meulenberg R, Berg DJC van der, Batenburg-van der Vegte W, Bos P, Kuenen JG (1990b) Mixotrophic and auto-trophic growth of Thiobacillus acidophilus on glucose and thiosulfate. Appl Environ Microbiol 56: 3395–3401PubMedPubMedCentralGoogle Scholar
  22. Pronk JT, Meulenberg R, Hazeu W, Bos P, Kuenen JG (1990c) Oxidation of reduced inorganic sulphur compounds by acidophilic thiobacilli. FEMS Microbiol Rev 75: 293–306CrossRefGoogle Scholar
  23. Roy AB, Trudinger PA (1970) The biochemistry of inorganic compounds of sulphur. University Press, CambridgeGoogle Scholar
  24. Sinha DB, Walden CC (1966) Formation of polythionates and their interrelationships during oxidation of thiosulphate by T. ferrooxidans. Can J Microbiol 12: 1041–1054CrossRefGoogle Scholar
  25. Sorbö B (1957) A colorimetric method for the determination of thiosulphate. Biochim Biophys Acta 23: 412–416CrossRefGoogle Scholar
  26. Steudel R, Holdt G, Göbel T, Hazeu W (1987) Chromatographic separation of higher polythionates SnO62- (n=3 ... 22) and their detection in cultures of Thiobacillus ferrooxidans; Molecular composition of bacterial sulfur secretions. Angew Chem Int Edn Engl 26: 151–153CrossRefGoogle Scholar
  27. Steudel R, Prenzel A (1989) Raman spectroscopic discovery of the hydrogenthiosulphate anion, HSSO3-, in solid NH4HS2O3. Z Naturforsch 44b: 1499–1502CrossRefGoogle Scholar
  28. Trudinger PA (1961) Thiosulphate oxidation and cytochromes in Thiobacillus X. 2. Thiosulphate-oxidizing enzyme. Biochem J 78: 680–686CrossRefGoogle Scholar
  29. Trudinger PA (1964a) The metabolism of trithionate by Thiobacillus X. Aus J Biol Sci 17: 459–468CrossRefGoogle Scholar
  30. Trudinger PA (1964b) Products of anaerobic metabolism of tetrathionate by Thiobacillus X. Aus J Biol Sci 17: 446–458CrossRefGoogle Scholar
  31. Trüper HG, Schlegel HG (1964) Sulphur metabolism in Thiorhodaceae. I. Quantitative measurements on growing cells of Chromatium okenii. Antonie van Leeuwenhoek 30: 225–238CrossRefGoogle Scholar
  32. Wood AP, Kelly DP (1986) Chemolithotrophic metabolism of the newly-isolated moderately thermophilic, obligately autotrophic Thiobacillus tepidarius. Arch Microbiol 144: 71–77CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 1992

Authors and Affiliations

  • Rogier Meulenberg
    • 1
  • Jack T. Pronk
    • 1
  • Wim Hazeu
    • 1
  • Piet Bos
    • 1
  • J. Gijs Kuenen
    • 1
  1. 1.Department of Microbiology and Enzymology, Kluyver Laboratory of BiotechnologyDelft University of TechnologyDelftThe Netherlands

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