Skip to main content
Log in

Chemolithoutotrophic growth of Thiothrix ramosa

  • Original Papers
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Thiothrix has been shown for the first time to be able to grow chemolithoautotrophically with thiosulphate or carbon disulphide as sole energy substrate. Thiosulphate served as the growth-limiting substrate for Thiothrix ramosa in chemostat culture. Maximum growth yield (Ymax) from yields at growth rates between 0.029–0.075 h-1 was 4.0 g protein/mol thiosulphate oxidized. The key enzyme of the Calvin cycle, ribulose 1,5-bisphosphate carboxylase, was present in these cells, as were rhodanese, adenylyl sulphate (APS) reductase and ‘sulphur-oxidizing enzyme’. Thiosulphate-grown cells oxidized thiosulphate, sulphide, tetrathionate and carbon disulphide. Oxidation kinetics for sulphide, thiosulphate and tetrathionate were biphasic: oxygen consumption during the fast first phase of oxidation indicated oxidation of sulphide, and the sulphane moieties of thiosulphate and tetrathionate, to elemental sulphur, before further oxidation to sulphate. Kinetic constants for these four substrates were determined. T. ramosa also grew mixotrophically in batch culture on lactate with a number of organic sulphur compounds: carbon disulphide, methanethiol and diethyl sulphide. Substituted thiophenes were also used as sole substrates. The metabolic versatility of T. ramosa is thus much greater than previously realised.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bland JA, Staley JT (1978) Observations on the biology of Thiothrix. Arch Microbiol 117: 79–87

    Google Scholar 

  • Bowen TJ, Butler PJ, Happold FC (1965) Some properties of the rhodanese system of Thiobacillus denitrificans. Biochem J 97: 651–657

    Google Scholar 

  • Bowen TJ, Happold FC, Taylor BF (1966) Studies on adenosine 5′-phosphosulfate reductase from Thiobacillus denitrificans. Biochim Biophys Acta 118: 566–576

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Chem 72: 248–254

    Google Scholar 

  • Charles AM, Suzuki I (1966) Mechanism of thiosulfate oxidation by Thiobacillus novellus. Biochim Biophys Acta 128: 510–521

    Google Scholar 

  • Kanagawa T, Kelly DP (1987) Degradation of substituted thiophenes by bacteria isolated from activated sludge. Microb Ecol 13: 47–57

    Google Scholar 

  • Kanagawa T, Dazai M, Fukuoka S (1982) Degradation of 0,0-dimethyl-phosphorodithioate by Thiobacillus thioparus TK-1 and Pseudomonas AK-2. Agric Biol Chem 46: 2571–2578

    Google Scholar 

  • Keil F (1912) Beiträge zur Physiologie der farblosen Schwefelbakterien. Beitr Biol Pflanz 11: 335–372

    Google Scholar 

  • Kelly DP, Smith NA (1990) Organic sulfur compounds in the environment. Biogeochemistry, microbiology, and ecological aspects. Adv Microb Ecol 11: 345–385

    Google Scholar 

  • Kelly DP, Chambers LA, Trudinger PA (1969) Cyanolysis and spectrophotometric estimation of trithionate in mixture with thiosulphate and tetrathionate. Anal Chem 41: 898–901

    Google Scholar 

  • Kelly DP, Mason J, Wood AP (1987) Energy metabolism in chemolithotrophs. In: Verseveld HWvan, Duine JA (eds) Microbial growth on C1 compounds. Martinus Nijhoff, Dordrecht, pp 186–194

    Google Scholar 

  • Kelly DP, Malin G, Wood AP (1993) Microbial transformations and biogeochemical cycling of one-carbon substrates containing sulphur, nitrogen or halogens. In: Murrell JC, Kelly DP (eds) Microbial metabolism of C1 compounds. Intercept, Andover, UK, pp 47–63

    Google Scholar 

  • Kondratieva EN, Zhukov VG, Ivanovsky RN, Petushkova YP, Monosov EZ (1976) The capacity of phototrophic sulfur bacterium Thiocapsa roseopersicina for chemosynthesis. Arch Microbiol 108: 287–292

    Google Scholar 

  • Larkin JM (1989) Genus II. Thiothrix Winogradsky 1888. In: Staley JT, Bryant MP, Pfennig N, Holt JG (eds) Bergey's manual of systernatic bacteriology, vol 3. Williams and Wilkins, Baltimore, pp 2098–2101

    Google Scholar 

  • Larkin JM, Shinabarger DL (1983) Characterization of Thiothrix nivea. Int J Syst Bacteriol 33: 841–846

    Google Scholar 

  • Larkin JM, Strohl WR (1983) Beggiatoa, Thiothrix, and Thioploca. Annu Rev Microbiol 37: 341–367

    Google Scholar 

  • Morita RY, Burton SD (1965) Filamentous appendages of Thiothrix. Z Allg Mikrobiol 5: 177–179

    Google Scholar 

  • Nelson DC (1989) Physiology and biochemistry of filamentous sulfur bacteria. In: Schlegel HG, Bowien B (eds) Autotrophic bacteria. Science Tech/Springer, Madison Berlin, pp 219–238

    Google Scholar 

  • Nelson DC, Castenholz RW (1981) Use of reduced sulfur compounds by Beggiatoa sp. J Bacteriol 147: 140–154

    Google Scholar 

  • Nelson DC, Jannasch HW (1983) Chemoautotrophic growth of a marine Beggiatoa in sulfide-gradient cultures. Arch Microbiol 136: 262–269

    Google Scholar 

  • Nelson DC, Jorgensen BB, Revsbech NP (1986) Growth pattern and yield of a chemoautotrophic Beggiatoa sp. in oxygen-sulfide microgradients. Appl Environ Microbiol 52: 225–233

    Google Scholar 

  • Nelson DC, Williams CA, Farah BA, Shively JM (1989) Occurrence and regulation of Calvin cycle enzymes in non-autotrophic Beggiatoa strains. Arch Microbiol 151: 15–19

    Google Scholar 

  • Odintsova EV (1991) Characterization of Thiothrix ramosa nov. sp. PhD thesis, Moscow (Academy of Sciences, Institute of Microbiology)

  • Odintsova EV, Dubinina GA (1990) New filamentous colourless sulphur bacteria Thiothrix ramosa nov. sp. Mikrobiologiia 59: 637–644

    Google Scholar 

  • Odintsova EV, Dubinina GA (1991) The growth cycle, reproduction and ultrastructure of Thiothrix ramosa. Mikrobiologiia 60: 314–320

    Google Scholar 

  • Odintsova EV, Dubinina GA (1993) The role of reduced sulphur compounds in the metabolism of Thiothrix ramosa. Mikrobiologiia 62: 213–222

    Google Scholar 

  • Overmann J, Pfennig N (1992) Continuous chemotrophic growth and respiration of Chromatiaceae species at low oxygen concentrations. Arch Microbiol 158: 59–67

    Google Scholar 

  • Pringsheim EG (1967) Die Mixotrophie von Beggiatoa. Arch Microbiol 59: 247–254

    Google Scholar 

  • Rabenhorst L (1865) Flora europaea algarum aquae dulcis submarinae, section II. Kummer, Leipzig, p 94

    Google Scholar 

  • Schmidt TM, Arieli B, Cohen Y, Padan E, Strohl WR (1987) Sulfur metabolism in Beggiatoa alba. J Bacteriol 169: 5466–5472

    Google Scholar 

  • Shively JM, Devore W, Stratford L, Porter L, Medlin L, Stevens SEJr (1986) Molecular evolution of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO). FEMS Microbiol Lett 37: 251–257

    Google Scholar 

  • Smith AJ, Lascelles J (1966) Thiosulphate metabolism and rhodanese in Chromatium sp. strain D. J Gen Microbiol 42: 357–370

    Google Scholar 

  • Smith DW, Strohl WR (1991) Sulfur-oxidizing bacteria. In: Shively JM, Barton LL (eds) Variations in autotrophic life. Academic Press, London, pp 121–146

    Google Scholar 

  • Smith NA, Kelly DP (1988) Oxidation of carbon disulphide as the sole cource of energy for the autotrophic growth of Thiobacillus thioparus strain TK-m. J Gen Microbiol 134: 3041–3048

    Google Scholar 

  • Sörbo B (1953) Crystalline rhodanese. I. Purification and physicochemical examination. Acta Chem Scand 7: 1129–1136

    Google Scholar 

  • Strohl WR, Schmidt TM (1984) Mixotrophy of colorless, sulfideoxidizing gliding bacteria Beggiatoa and Thiothrix. In: Strohl WR, Tuovinen OH (eds) Microbial chemoautotrophy. Ohio State University Press, Columbus, Ohio, USA, pp 79–95

    Google Scholar 

  • Suzuki I (1965) Oxidation of elemental sulfur by an enzyme system of Thiobacillus thiooxidans. Biochim Biophys Acta 104: 359–371

    Google Scholar 

  • Suzuki I, Silver M (1966) The initial product and properties of the sulfur-oxidizing enzyme of thiobacilli. Biochim Biophys Acta 122: 22–33

    Google Scholar 

  • Taylor BF (1968) Oxidation of elemental sulfur by an enzyme system from Thiobacillus neapolitanus. Biochim Biophys Acta 170: 112–122

    Google Scholar 

  • Trüper HG, Pfennig N (1966) Sulphur metabolism in Thiorhodaceae. III. Storage and turnover of thiosulphate sulphur in Thiocapsa floridana and Chromatium species. Antonie van Leeuwenhoek. J Microbiol Serol 32: 261–276

    Google Scholar 

  • Tuovinen OH, Kelly DP (1973) Studies on the growth of Thiobacillus ferrooxidans. Arch Microbiol 88: 285–298

    Google Scholar 

  • VanGemerden H (1986) Production of elemental sulfur by green and purple sulfur bacteria. Arch Microbiol 146: 52–56

    Google Scholar 

  • Williams TM, Unz RF (1985) Filamentous sulfur bacteria of activated sludge: characterization of Thiothrix, Beggiatoa and Eikelboom type 021N strains. Appl Environ Microbiol 49: 887–898

    Google Scholar 

  • Winogradsky S (1888) Beiträge zur Morphologie und Physiologie der Bakterien. I. Zur Morphologie und Physiologie der Schwefelbakterien. Felix, Leipzig. Republished as: Contribution à la morphologie et physiologie des sulfobactéries. In: Winogradsky S (ed) Microbiologie du sol Masson, Paris, pp 83–126

    Google Scholar 

  • Wood AP, Kelly DP (1986) Chemolithotrophic metabolism of the newly-isolated moderately thermophilic, obligately autotrophic Thiobacillus tepidarius. Arch Microbiol 144: 71–77

    Google Scholar 

  • Wood AP, Kelly DP (1989) Isolation and physiological characterisation of Thiobacillus thyasiris sp. nov., a novel marine facultative autotroph and the putative symbiont of Thyasira flexuosa. Arch Microbiol 152: 160–166

    Google Scholar 

  • Zavarzin GA (1989) Sergei N Winogradsky and the discovery of chemo-synthesis. In: Schlegel HG, Bowien B (eds) Autotrophic bacteria. Science Tech/Springer, Madison Berlin, pp 17–32

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Odintsova, E.V., Wood, A.P. & Kelly, D.P. Chemolithoutotrophic growth of Thiothrix ramosa . Arch. Microbiol. 160, 152–157 (1993). https://doi.org/10.1007/BF00288718

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00288718

Key words

Navigation