Skip to main content
SpringerLink
Log in

Oxidation of Inorganic Sulfur Compounds by Obligately Organotrophic Bacteria

  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

New data obtained by the author and other researchers on two different groups of obligately heterotrophic bacteria capable of inorganic sulfur oxidation are reviewed. Among culturable marine and (halo)alkaliphilic heterotrophs oxidizing sulfur compounds (thiosulfate and, much less actively, elemental sulfur and sulfide) incompletely to tetrathionate, representatives of the gammaproteobacteria, especially from the Halomonas group, dominate. Some denitrifying species from this group are able to carry out anaerobic oxidation of thiosulfate and sulfide using nitrogen oxides as electron acceptors. Despite the low energy output of the reaction of thiosulfate oxidation to tetrathionate, it can be utilized for ATP synthesis by some tetrathionate-producing heterotrophs; however, this potential is not always realized during their growth. Another group of marine and (halo)alkaliphilic heterotrophic bacteria capable of complete oxidation of sulfur compounds to sulfate mostly includes representatives of the alphaproteobacteria which are most closely related to nonsulfur purple bacteria. They can oxidize sulfide (polysulfide), thiosulfate, and elemental sulfur via sulfite to sulfate but neither produce nor oxidize tetrathionate. All of the investigated sulfate-forming heterotrophic bacteria belong to lithoheterotrophs, being able to gain additional energy from the oxidation of sulfur compounds during heterotrophic growth on organic substrates. Some doubtful cases of heterotrophic sulfur oxidation described in the literature are also discussed.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  1. Sorokin, D.Yu., Oxidation of Sulfur Compounds by Heterotrophic Microorganisms, Izv. Akad. Nauk SSSR, Ser. Biol., 1991, pp. 558-569.

  2. Mason, J. and Kelly, D.P., Thiosulfate Oxidation by Obligately Heterotrophic Bacteria, Microb. Ecol., 1988, vol. 15, pp. 123-134.

    Google Scholar 

  3. Gommers, P.J.F. and Kuenen, J.G., Thiobacillus Q—a Chemolithoheterotrophic Sulfur Bacterium, Arch. Microbiol., 1988, vol. 150, pp. 117-125.

    Google Scholar 

  4. Springs, S., Kampfer, P., and Schleifer, K.H., Limnobacter thiooxidans gen. nov., sp. nov., a Novel Thiosulfate-Oxidizing Bacterium Isolated from Freshwater Lake Sediments, Int. J. Syst. Evol. Microbiol., 2001, vol. 51, pp. 1463-1470.

    Google Scholar 

  5. Gonzales, J.M., Kiene, R.P., Joye, S.B., Sorokin, D.Yu., and Moran, M.A., Oxidation of Organic and Inorganic Sulfur Compounds by Aerobic Heterotrophic Marine Bacteria, Biotransformations: Bioremediation Technology for Health and Environmental Protection, Singh, V.P. and Stapleton, R.D., Eds., Elsevier, pp. 291-310.

  6. Tuttle, J.H. and Jannasch, H.W., Occurrence and Types of Thiobacillus-like Bacteria in the Sea, Limnol. Oceanogr., 1972, vol. 18, pp. 532-543.

    Google Scholar 

  7. Tuttle, J.H. and Jannasch, H.W., Sulfide and Thiosulfate-Oxidizing Bacteria in Anoxic Marine Basins, Mar. Biol., 1973, vol. 20, pp. 64-70.

    Google Scholar 

  8. Tuttle, J.H., Holmes, P.E., and Jannasch, H.W., Growth Rate Stimulation of Marine Pseudomonads by Thiosulfate, Arch. Microbiol., 1974, vol. 99, pp. 1-14.

    Google Scholar 

  9. Tuttle, J.H., Organic Carbon Utilization by Resting Cells of Thiosulfate-Oxidizing Marine Heterotrophs, Appl. Environ. Microbiol., 1980, vol. 40, pp. 516-521.

    Google Scholar 

  10. Tuttle, J.H., Schwartz, J.H., and Whiled, G.M., Some Properties of Thiosulfate-Oxidizing Enzyme from Marine Heterotroph 16 B, Appl. Environ. Microbiol., 1983, vol. 46, pp. 438-445.

    Google Scholar 

  11. Podgorsek, L. and Imhoff, J.F., Tetrathionate Production by Sulfur-Oxidizing Bacteria and the Role of Tetrathionate in the Sulfur Cycle of Baltic Sea Sediments, Aquatic Microb. Ecol., 1999, vol. 17, pp. 255-263.

    Google Scholar 

  12. Sorokin, D.Yu., Bacterial Thiosulfate Oxidation in the Black Sea, Izv. Akad. Nauk SSSR, Ser. Biol., 1991, pp. 255-266.

  13. Sorokin, D.Yu., Oxidation of Thiosulfate and Elemental Sulfur in the Redox Layer of the Black Sea during Winter-Spring Period, Okeanologiya, 1992, vol. 32, pp. 873-880.

    Google Scholar 

  14. Pimenov, N.V., Rusanov, I.I., Poglazova, M.N., Mityushina, L.L., Sorokin, D.Yu., Khmelenina, V.N., and Trotsenko, Yu.A., Bacterial Mats on the Coral-like Structures at Methane Seeps in the Black Sea, Mikrobiologiya, 1997, vol. 66, pp. 421-428.

    Google Scholar 

  15. Sorokin, D.Yu., Oxidation of Reduced Sulfur Compounds in Volcanically Active Regions of the Plenty Bay (New Zealand) and Matupy Harbour (Papua-New Guinea), Izv. Akad. Nauk SSSR, Ser. Biol., 1991, pp. 376-387.

  16. Sorokin, D.Yu., Lysenko, A.M., and Mityushina, L.L., Isolation and Characterization of Alkaliphilic Chemoorganoheterotrophic Bacteria Oxidizing Reduced Inorganic Sulfur Compounds to Tetrathionate, Mikrobiologiya, 1996, vol. 65, pp. 370-383.

    Google Scholar 

  17. Tesku, A., Brinkhoff, T., Muyzer, G., Moser, D.P., Rethmeier, J., and Jannasch, H.W., Diversity of Thiosulfate-Oxidizing Bacteria from Marine Sediments and Hydrothermal Vents, Appl. Environ. Microbiol., vol. 66, pp. 3125-3133.

  18. Sorokin, D.Yu., Catenococcus thiocyclus gen. nov. sp. nov.—a New Facultatively Anaerobic Bacterium from Nearshore Sulphidic Hydrothermal Waters, J. Gen. Microbiol., 1992, vol. 138, pp. 2287-2292.

    Google Scholar 

  19. Sorokin, D.Yu., Tesku, A., Robertson, B.A., and Kuenen, J.G., Anaerobic Oxidation of Thiosulfate by Obligately Heterotrophic Bacteria, FEMS Microbiol. Ecol., 1999, vol. 30, pp. 113-123.

    Google Scholar 

  20. Sorokin, D.Yu. and Mityushina, L.L., Ultrastructure of Alkaliphilic Heterotrophic Bacteria Oxidizing Sulfur Compounds to Tetrathionate, Mikrobiologiya, 1998, vol. 67, pp. 93-101.

    Google Scholar 

  21. Berendes, F., Gottschalk, G., Heine-Dokbernack, E., Moore, E.P.B., and Tindall, B.J., Halomonas desiderata sp. nov., a New Alkaliphilic, Halotolerant and Denitrifying Bacterium Isolated from a Municipal Sewage Works, Syst. Appl. Microbiol., 1996, vol. 19, pp. 158-167.

    Google Scholar 

  22. Duckworth, A.W., Grant, W.D., Jones, B.E., Meijer, D., Marquez, M.C., and Ventosa, A., Halomonas magadii sp. nov., a New Member of the Genus Halomonas, Isolated from a Soda Lake of the East African Rift Valley, Extremophiles, 2000, vol. 4, pp. 53-60.

    Google Scholar 

  23. Arahal, D.R., Ludwig, W., Schleifer, K.H., and Ventosa, A., Phylogeny of the Family Halomonadaceae Based on 23S and 16S rDNA Sequence Analysis, Int. J. Syst. Evol. Microbiol., 2002, vol. 52, pp. 241-249.

    Google Scholar 

  24. Ventosa, A., Nieto, J.J., and Oren, A., Biology of Moderately Halophilic Aerobic Bacteria, Microbiol. Mol. Biol. Rev., 1998, vol. 62, pp. 504-544.

    Google Scholar 

  25. Fendrich, C., Halovibrio variabilis gen. nov. sp. nov., Pseudomonas halophila sp. nov. and a New Halophilic Aerobic Coccoid Eubacterium from Great Salt Lake, Utah, USA, Syst. Appl. Microbiol., 1988, vol. 11, pp. 36-43.

    Google Scholar 

  26. Sorokin, D.Yu., Thiosulfate Oxidation to Tetrathionate by Heterotrophic Bacteria from Aquatic Habitats, Mikrobiologiya, 1992, vol. 61, pp. 756-763.

    Google Scholar 

  27. Kurtenaker, A. and Kaufmann, M., Die Einwirkung von Lauge auf die Polythionate, Z. Anorg. Allgem. Chem, 1925, vol. 148, pp. 369-380.

    Google Scholar 

  28. Sorokin, D.Yu., Oxidation of Thiosulfate to Tetrathionate by Marine Pseudomonad Strain ChG 7-3: Influence on Growth and the Properties of the Oxidation System, Mikrobiologiya, 1993, vol. 62, pp. 223-231.

    Google Scholar 

  29. Sorokin, D.Yu., Robertson, L.A., and Kuenen, J.G., Sulphur Metabolism of Catenococcus thiocyclus, FEMS Microbiol. Ecol., 1996, vol. 19, pp. 117-125.

    Google Scholar 

  30. Sorokin, D.Yu., Influence of Thiosulfate on Dark Carbon Dioxide Assimilation by Marine Heterotrophic Sulfur-Oxidizing Bacteria, Mikrobiologiya, 1993, vol. 62, pp. 816-824.

    Google Scholar 

  31. Whited, G.M. and Tuttle, J.H., Separation and Distribution of Thiosulfate-Oxidizing Enzyme, Tetrathionate Reductase, and Thiosulfate Reductase in Extracts of Marine Heterotroph Strain 16 B, J. Bacteriol., 1983, vol. 156, pp. 600-610.

    Google Scholar 

  32. Vedenina, I.Ya. and Sorokin, D.Yu., ATP Synthesis during Oxidation of Thiosulfate to Tetrathionate by Heterotrophic Bacteria, Mikrobiologiya, 1992, vol. 61, pp. 764-769.

    Google Scholar 

  33. Sorokin, D.Yu., Oxidation of Sulfide and Elemental Sulfur to Tetrathionate by Chemoorganoheterotrophic Bacteria, Mikrobiologiya, 1996, vol. 65, pp. 5-9.

    Google Scholar 

  34. Sorokin, D.Yu., Combined Microbial-Chemical Processes in the Transformation of Inorganic Compounds: Role in natural Systems and Possible Applications in Biotechnology, Mikrobiologiya, 1997, vol. 66, pp. 293-301.

    Google Scholar 

  35. Buisman, C.J.N., Sorokin, D.Yu., Kuenen, J.G., Janssen, A.J.H., and Robertson, L.A., Process for the Conversion of Thiosulfate and Process for the Purification of Gases Containing Hydrogen Sulfide, International Patent Application no. 97/43033, 1997.

  36. Sorokin, D.Yu. and Lysenko, A.M., Characterization of Heterotrophic Bacteria from the Black Sea Able To Oxidize Sulfur Compounds to Sulfate, Mikrobiologiya, 1993, vol. 62, pp. 1018-1031.

    Google Scholar 

  37. Sorokin, D.Yu., Sulfitobacter pontiacus gen. nov. sp. nov.—a New Heterotrophic Bacterium from the Black Sea, Specialized on Sulfite Oxidation, Mikrobiologiya, 1995, vol. 64, pp. 354-365.

    Google Scholar 

  38. Yurkov, V.V. and Beaty, T., Aerobic Anoxygenic Phototrophic Bacteria, Microbiol. Mol. Biol. Rev., 1998, vol. 62, pp. 695-724.

    Google Scholar 

  39. Sorokin, D.Yu., Tourova, T.P., Kuznetsov, B.B., Bryantseva, I.A., and Gorlenko, V.M., Roseinatronobacter thiooxidans gen. nov., sp. nov., a New Alkaliphilic Aerobic Bacteriochlorophyll a-Containing Bacterium Isolated from a Soda Lake, Mikrobiologiya, 2000, vol. 69, pp. 89-97.

    Google Scholar 

  40. Das, S.K., Mishra, A.K., Tindall, B.J., Rainey, F.A., and Stackebrandt, E., Oxidation of Thiosulfate by a New Bacterium Bosea thiooxidans gen. nov., sp. nov.: Analysis of Phylogeny Based on Chemotaxonomy and 16S Ribosomal DNA Sequencing, Int. J. Syst. Bacteriol., 1996, vol. 46, pp. 981-987.

    Google Scholar 

  41. Moreira, C., Rainey, F.A., Nobre, M.F., Da Silva, M.T., and Da Costa, M.S., Tepidomonas ignava gen. nov., sp. nov., a New Chemolithoheterotrophic and Thermophilic Member of the β-Proteobacteria, Int. J. Syst. Evol. Microbiol., 2000, vol. 50, pp. 735-742.

    Google Scholar 

  42. Sorokin, D.Yu., Influence of Thiosulfate on the Growth of Sulfate-Producing Heterotrophic Bacteria from the Black Sea in Continuous Culture, Mikrobiologiya, 1994, vol. 63, pp. 457-465.

    Google Scholar 

  43. Kelly, D.P., Physiology and Biochemistry of Unicellular Sulfur Bacteria, Autotrophic Bacteria, Schlegel, H.G. and Bowien, B., Eds., Berlin: Springer, 1989, pp. 193-217.

    Google Scholar 

  44. Sorokin, D.Yu., Vedenina, I.Ya., and Grabovich, M.Yu., Influence of Sulfite on Acetate Metabolism Sulfitobacter pontiacus Growing in Continuous Culture of, Mikrobiologiya, 1999, vol. 68, pp. 19-26.

    Google Scholar 

  45. Vairavamurthy, A., Zhou, W., Eglinton, T., and Manowitz, B., Sulfonates: a Novel Class of Organic Sulfur Compounds in Marine Sediments, Geochim. Cosmochim. Acta, 1994, vol. 58, pp. 4681-4687.

    Google Scholar 

  46. Tan, N.C.G. and Field, J.A., Biodegradation of sulfonated aromatic compounds, Environmental Technologies To Treat Sulfur Pollution, Lens, P. and Hulshoff, P.L., Eds., London: IWA, 2000, pp. 377-392.

    Google Scholar 

  47. Kertesz, M.A., Riding the Sulfur Cycle—Metabolism of Sulfonates and Sulfur Esters in Gram-Negative Bacteria, FEMS Microbiol. Rev., 1999, vol. 24, pp. 135-175.

    Google Scholar 

  48. Denger, K. and Cook, A.M., Ethanedisulfonate Is Degraded via Sulfoacetaldehyde in Ralstonia sp. Strain EDS 1, Arch. Microbiol., 2001, vol. 176, pp. 89-95.

    Google Scholar 

  49. Reichenbecher, W. and Murell, J.C., Desulfonation of Propanesulfonic Acid by Comamonas acidovorans Strain P53: Evidence for An Alkane Sulfonatase and an Atypical Sulfite Dehydrogenase, Arch. Microbiol., 1999, vol. 172, pp. 387-392.

    Google Scholar 

  50. Kelly, D.P. and Murrell, J.C., Microbial Metabolism of Methanesulfonic Acid, Arch. Microbiol., 1999, vol. 172, pp. 341-348.

    Google Scholar 

  51. Gonzalez, J.M. and Moran, M.A., Numerical Dominance of a Group of Marine Bacteria in the α-Subclass of the Proteobacteria in Coastal Seawaters, Appl. Environ. Microbiol., 1997, vol. 63, pp. 4237-4242.

    Google Scholar 

  52. Pukall, R., Buntefuss, D., Frühling, A., Rohde, M., Kroppenstedt, R.M., Burghardt, J., Lebaron, P., Bernard, L., and Stackebrandt, E., Sulfitobacter mediterraneus sp. nov., a New Sulfite-Oxidizing Member of the α-Proteobacteria, Int. J. Syst. Bacteriol., 1999, vol. 49, pp. 513-519.

    Google Scholar 

  53. Labrenz, M., Tindall, B.J., Lawson, P.A., Collins, M.D., Schuman, P., and Hirsch, P., Staleya guttiformis gen. nov., sp. nov., and Sulfitobacter brevis sp. nov., α-3-Proteobacteria from Hypersaline, Heliothermal and Meromictic Antarctic Ekho Lake, Int. J. Syst. Evol. Microbiol., 2000, vol. 50, pp. 303-313.

    Google Scholar 

  54. Yagi, S., Kitai, S., and Kimura, T., Oxidation of Elemental Sulfur to Thiosulfate by Streptomycetes, Appl. Microbiol., 1971, vol. 22, pp. 157-162.

    Google Scholar 

  55. Wainwright, M., Sulfur Oxidation in Soils, Adv. Agronomy, 1985, vol. 37, pp. 349-396.

    Google Scholar 

  56. Sorokin, D.Yu., Aerobic Sulfur Reduction by Gram-Positive Bacteria and Yeasts Results in Thiosulfate Production from Elemental Sulfur, Mikrobiologiya, 1993, vol. 62, pp. 604-615.

    Google Scholar 

  57. Grayston, S.J., Nevel, W., and Wainwright, M., Sulfur Oxidation by Fungi, Trans. Brit. Mycol. Soc., 1986, vol. 87, pp. 193-198.

    Google Scholar 

  58. Grayston, S.J. and Wainwright, M., Fungal Sulfur Oxidation: Effect of Carbon Source and Growth Stimulation by Thiosulfate, Trans. Brit. Mycol. Soc., 1987, vol. 88, pp. 213-219.

    Google Scholar 

  59. Wainwright, M. and Grayston, S.J., Fungal Growth Stimulation by Thiosulfate under Oligotrophic Conditions, Trans. Brit. Mycol. Soc., 1988, vol. 91, pp. 149-156.

    Google Scholar 

  60. Jones, R., Parkinson, S.M., Wainwright, M., and Killham, K., Oxidation of Thiosulfate by Fusarium oxysporum Grown under Oligotrophic Conditions, Mycol. Res., 1991, vol. 95, pp. 1169-1174.

    Google Scholar 

  61. Golovacheva, R.S. and Karavaiko, G.I., Sulfobacillus, a New Genus of Thermophilic Spore-Forming Bacteria, Mikrobiologiya, 1978, vol. 47, pp. 815-822.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Microbiology, Russian Academy of Sciences, pr. 60-letiya Oktyabrya 7, k. 2, Moscow, 117312, Russia

    D. Yu. Sorokin

Authors
  1. D. Yu. Sorokin
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sorokin, D.Y. Oxidation of Inorganic Sulfur Compounds by Obligately Organotrophic Bacteria. Microbiology 72, 641–653 (2003). https://doi.org/10.1023/B:MICI.0000008363.24128.e5

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:MICI.0000008363.24128.e5

Search

Navigation