Transformation of Sulfur Species by Phototrophic and Chemotrophic Microbes

  • J. Bauld
Part of the Dahlem Workshop Reports book series (DAHLEM, volume 33)

Abstract

Transformations between the various oxidation states of sulfur occurring within the biosphere are dominantly microbially mediated. Species transformations may occur during the biosynthesis of cell biomass (e.g., the assimilatory reduction of sulfate) or its subsequent decomposition. Dissimilatory processes may be oxidative or reductive in character. The former commonly provide a source of electrons for energy-generating metabolism and/or a source of reducing power for autotrophic CO2 fixation. The latter employs oxidized S species as terminal electron acceptors for anaerobic respirations. In contrast to the diversity of microbes which selectively assimilate species, dissimilatory processes are mediated by distinct and specialized physiological groups having widely differing responses to parameters such as oxygen, light, and sulfide. These restrictions effectively partition certain sulfur species transformations into separate, though often adjacent, habitats. Some species transformations can only proceed at the interface between mutually exclusive habitats. Under anoxic conditions dissimilatory sulfur species transformations are exclusively microbial.

Recent investigations have been marked by an increasing awareness of the quantitative importance of certain organic S species in aquatic sediments and the wide variation of spatial and temporal scales across oxicanoxic interfaces. The ability of microbially mediated oxidations to compete with abiotic reactions under oxic conditions appears to be variable and habitat-dependent. Under anoxic conditions iron may act as a significant, though possibly transitory, sink for sulfide produced during dissimilatory sulfate reduction.

Keywords

Phytoplankton Cysteine Assimilation Photosynthesis Disulfide 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Almgren T, Hagström I (1974) The oxidation rate of sulfide in seawater. Water Res 8: 395–400CrossRefGoogle Scholar
  2. Anderson JW (1978) Sulphur in biology. Edward Arnold, LondonGoogle Scholar
  3. Andreae MO (1980) The production of methylated sulfur compounds by marine phytoplankton. In: Trudinger PA, Walter MR, Ralph BJ (eds) Biogeochemistry of ancient and modern environments. Australian Academy of Science, Canberra, pp 253–259Google Scholar
  4. Bechard MJ, Rayburn WR (1979) Volatile organic sulfides from freshwater algae. J Phycol 15: 379–383Google Scholar
  5. Berner RA (1971) Principles of chemical sedimentology. McGraw-Hill, New YorkGoogle Scholar
  6. Biebl H, Pfennig N (1978) Growth yields of green sulfur bacteria in mixed cultures with sulfur- and sulfate-reducing bacteria. Arch Microbiol 117: 9–16CrossRefGoogle Scholar
  7. Boulege J, Michard G (1973) Formation de polysulfures dans les conditions physicochimiques de l’eau de mer. CR Acad Sci (Paris) 277: 2613–2616Google Scholar
  8. Bremner JM, Steele CG (1978) Role of microorganisms in the atmospheric sulfur cycle. In: Alexander M (ed) Advances in microbial ecology. Plenum Press, New York, pp 155–201Google Scholar
  9. Cavanaugh CM (1983) Symbiotic chemoautotrophic bacteria in marine invertebrates from sulphide-rich habitats. Nature 302: 58–61CrossRefGoogle Scholar
  10. Chambers LA (1982) Sulfur isotope study of a modern intertidal environment and interpretation of ancient sulfides. Geochim Cosmochim Acta 46: 721–728CrossRefGoogle Scholar
  11. Ehrlich HL (1981) Geomicrobiology. Marcel Dekker, New YorkGoogle Scholar
  12. Fitzgerald JW (1976) Sulfate ester formation and hydrolysis: a potentially important yet often ignored aspect of the sulfur cycle of aerobic soils. Bacteriol Rev 40: 698–721PubMedGoogle Scholar
  13. Fitzgerald JW (1978) Naturally occurring organosulfur compounds in soil. In: Nriagu JO (ed) Sulfur in the environment. II. Ecological impacts. John Wiley, New York, pp 391–43Google Scholar
  14. Freney JR, Melville GE, Williams CH (1971) Organic sulphur fractions labelled by addition of 35S-sulphate to soil. Soil Biol Biochem 3: 133–141CrossRefGoogle Scholar
  15. Hageage GJ, Eanes ED, Gherna RL (1970) X-ray diffraction studies of the sulfur globules accumulated by Chromatium species. J Bacteriol 101: 464–469PubMedGoogle Scholar
  16. Hansen TA (1983) Electron donor metabolism in phototrophic bacteria. In: Ormerod JG (ed) The phototrophic bacteria: anaerobic life in the light. Black well Scientific Publications, Oxford, pp 76–99Google Scholar
  17. Hashwa F (1975) Thiosulfate metabolism in some red phototrophic bacteria. PI Soil 43: 41–47CrossRefGoogle Scholar
  18. Howarth RW (1979) Pyrite: its rapid formation in a salt marsh and its importance in ecosystem metabolism. Science 203: 49–51PubMedCrossRefGoogle Scholar
  19. Howarth RW, Jorgensen BB (1984) Formation of 35S-labelled elemental sulfur and pyrite in coastal marine sediments (Limfjorden and Kysing Fjord, Denmark) during short-term 35S02–-reduction measurements. Geochim Cosmochim. Acta 48: 1807–1818Google Scholar
  20. Howarth RW, Merkel S (1984) Pyrite formation and the measurement of sulfate reduction in salt marsh sediments. Limnol Oceanog 29: 598–608CrossRefGoogle Scholar
  21. Hurlbert RE (1967) Effect of oxygen on viability and substrate utilization in Chromatium. J Bacteriol 93: 1346–1352PubMedGoogle Scholar
  22. Jannasch HW, Nelson DC (1984) Recent progress in the microbiology of hydro thermal vents. In: Klug MJ, Reddy CA (eds) Current perspectives in microbial ecology. American Society for Microbiology, Washington, DC, pp 170–176Google Scholar
  23. Jannasch HW, Wirsen CO (1979) Chemosynthetic primary production at East Pacific sea floor spreading centers. Bioscience 29: 592–598CrossRefGoogle Scholar
  24. Jørgensen BB (1977) The sulfur cycle of a coastal marine sediment (Limfjorden, Denmark). Limnol Oceanog 22: 814–832CrossRefGoogle Scholar
  25. Jørgensen BB (1982) Ecology of the bacteria of the sulphur cycle with special reference to anoxic-oxic interface environments. Phil Trans Roy Soc Lond B 298: 543–561CrossRefGoogle Scholar
  26. Jørgensen BB (1983) The microbial sulfur cycle. In: Krumbein WE (ed) Microbial geochemistry. Blackwell, Oxford, pp 91–124Google Scholar
  27. Kämpf C, Pfennig N (1980) Capacity of Chromatiaceae for chemotrophic growth. Specific respiration rates of Thiocystis violacea and Chromatium vinosum. Arch Microbiol 127: 125–137Google Scholar
  28. Kelly DP (1982) Biochemistry of the chemolithotrophic oxidation of inorganic sulphur. Phil Trans Roy Soc Lond B 298: 499–528CrossRefGoogle Scholar
  29. Kelly DP, Kuenen JG (1985) Ecology of the colourless sulfur bacteria. In: Codd GA (ed) Aspects of microbial metabolism and ecology. Academic Press, San Diego, pp 211–240Google Scholar
  30. King GM (1983) Sulfate reduction in Georgia salt marsh soils: an evaluation of pyrite formation by use of 35S and 55Fe tracers. Limnol Oceanog 28: 987–995CrossRefGoogle Scholar
  31. King GM, Klug MJ (1980) Sulfhydrolase activity in sediments of Wintergreen Lake, Kalamazoo County, Michigan. Appl Envir Microbiol 39: 950–956Google Scholar
  32. King GM, Klug MJ (1982) Comparative aspects of sulfur mineralization in sediments of a eutrophic lake basin. Appl Envir Microbiol 43: 1406–1412Google Scholar
  33. Kuenen JG, Beudeker RF (1982) Microbiology of thiobacilli and other sulphur-oxidizing autotrophs, mixotrophs, and heterotrophs. Phil Trans Roy Soc Lond B 298: 473–497CrossRefGoogle Scholar
  34. McCandless EL, Craigie JS (1979) Sulfated polysaccharides in red and brown algae. Ann Rev Plant Physiol 30: 41–53CrossRefGoogle Scholar
  35. Nriagu JO, Coker RD, Kemp ALW (1979) Thiosulfate, polythionates, and rhodanese activity in Lake Erie and Ontario sediments. Limnol Oceanog 24: 383–389CrossRefGoogle Scholar
  36. Nriagu JO, Hem JD (1978) Chemistry of pollutant sulfur in natural waters. In: Nriagu JO (ed) Sulfur in the environment. II. Ecological impacts. John Wiley, New York, pp 211–270Google Scholar
  37. Oshrain RL, Wiebe WJ (1979) Arylsulfatase activity in salt marsh soils. Appl Envir Microbiol 38: 337–340Google Scholar
  38. Padan E (1979) Impact of facultatively anaerobic photoautotrophic metabolism on ecology of cyanobacteria (blue-green algae). Adv Microb Ecol 3: 1–48Google Scholar
  39. Peck HD, LeGall J (1982) Biochemistry of dissimilatory sulphate reduction. Phil Trans Roy Soc Lond B 298: 443–466CrossRefGoogle Scholar
  40. Percival E, McDowell RH (1967) Chemistry and enzymology of marine algal polysaccharides. Academic Press, LondonGoogle Scholar
  41. Pfennig N (1978) General physiology and ecology of photosynthetic bacteria. In: Clayton RK, Sistrom WR (eds) The photosynthetic bacteria. Plenum Press, New York, pp 3–18Google Scholar
  42. Pfennig N, Biebl H (1976) De sulfur omonas acetoxidans gen. nov. and sp. nov., a new anaerobic,sulfur-reducing, acetate-oxidizing bacterium. Arch Microbiol 110: 3–12PubMedCrossRefGoogle Scholar
  43. Pfennig N, Widdel F (1981) Ecology and physiology of some anaerobic bacteria from the microbial sulfur cycle. In: Bothe H, Trebst A (eds) Biology of inorganic nitrogen and sulfur. Springer-Verlag, Heidelberg, pp 169–177CrossRefGoogle Scholar
  44. Pfennig N, Widdel F (1982) The bacteria of the sulphur cycle. Phil Trans Roy Soc Lond B 298:433–41Google Scholar
  45. Pfennig N, Widdel F, Trüper HG (1981) The dissimilatory sulfate-reducing bacteria. In: Starr MP, Stolp H, Trüper HG, Balows A, Schlegel HG (eds) The prokaryotes. Springer-Verlag, New York, pp 926–940Google Scholar
  46. Postgate JR (1968) The sulfur cycle. In: Nickless G (ed) Inorganic sulfur chemistry. Elsevier, Amsterdam, pp 259–279Google Scholar
  47. Postgate JR (1982) Economic importance of sulphur bacteria. Phil Trans Roy Soc Lond B 298: 583–600CrossRefGoogle Scholar
  48. Postgate JR (1984) The sulphate-reducing bacteria. Cambridge University Press, CambridgeGoogle Scholar
  49. Rolls JP, Lindstrom ES (1967) Effect of thiosulfate on the photosynthetic growth of Rhodopseudomonas palustris. J Bacteriol 94: 860–866PubMedGoogle Scholar
  50. Roy AB, Trudinger PA (1970) The biochemistry of inorganic compounds of sulfur. Cambridge University Press, LondonGoogle Scholar
  51. Ruby EG, Wirsen CO, Jannasch HW (1981) Chemolithotrophic sulfur-oxidizing bacteria from the Galapagos Rift hydrothermal vents. Appl Envir Microbiol 42: 317–324Google Scholar
  52. Schlegel HG (1981) Microorganisms involved in the nitrogen and sulfur cycles. In Bothe H, Trebst A (eds) Biology of inorganic nitrogen and sulfur. Springer-Verlag, Berlin, pp 3–12CrossRefGoogle Scholar
  53. Siegel LM (1975) Biochemistry of the sulfur cycle. In: Greenberg DM (ed) Metabolic pathways. Metabolism of sulfur compounds. Academic Press, New York, pp 217–286Google Scholar
  54. Skyring GW, Chambers LA, Bauld J (1983) Sulfate reduction in sediments colonized by cyanobacteria, Spencer Gulf, South Australia. Aust J Mar Freshw Res 34: 359–374Google Scholar
  55. Steinitz YL (1981) Microbial desulfonation of lignosulfonate - a new approach. Eur J Appl Microbiol Biotechnol 13: 216–221CrossRefGoogle Scholar
  56. Swank WT, Fitzgerald JW, Ash JT (1984) Microbial transformation of sulfate in forest soils. Science 223: 182–184PubMedCrossRefGoogle Scholar
  57. Trudinger PA (1982) Geological significance of sulphur oxidoreduction by bacteria. Phil Trans Roy Soc Lond B 298: 563–581CrossRefGoogle Scholar
  58. Trudinger PA, Loughlin RE (1981) Metabolism of simple sulfur compounds. In: Florkin M, Neuberger A, van Deemem LLM (eds) Comprehensive biochemistry. 19A. Amino acid metabolism and sulfur metabolism. Elsevier, Amsterdam, pp 165–256Google Scholar
  59. Trüper HG (1978) Sulfur metabolism. In: Clayton RK, Sistrom WR (eds) The photosynthetic bacteria. Plenum Press, New York, pp 677–690Google Scholar
  60. Trüper HG (1981) Photolithotrophic sulfur oxidation. In: Bothe H, Trebst A (eds) Biology in inorganic nitrogen and sulfur. Springer-Verlag, Berlin, pp 199–211Google Scholar
  61. Trüper HG (1982) Microbial processes in the sulfur cycle through time. In: Holland HD, Schidlowski M (eds) Mineral deposits and the evolution of the biosphere. Dahlem Konferenzen. Springer-Verlag, Berlin Heidelberg New YorkGoogle Scholar
  62. Trüper HG, Fischer U (1982) Anaerobic oxidation of sulphur compounds as electron donors for bacterial photosynthesis. Phil Trans Roy Soc Lond B 298: 529–542CrossRefGoogle Scholar
  63. Tuttle JH, Wirsen CO, Jannasch HW (1983) Microbial activities in the emitted hydrothermal waters of the Galapagos Rift vents. Mar Biol 73: 293–299CrossRefGoogle Scholar
  64. van Gemerden H, Beeftink HH (1983) Ecology of phototrophic bacteria: In: Ormerod JG (ed) The phototrophic bacteria: anaerobic life in the light. Blackwell Scientific Publications, Oxford, pp 146–185Google Scholar
  65. Wetzel RG (1983) Limnology. Saunders College Publishing, PhiladelphiaGoogle Scholar
  66. Wood JM, Wang HK (1983) Microbial resistance to heavy metals. Envir Sci Technol 17: 582A–590ACrossRefGoogle Scholar
  67. Zinder SH, Brock TD (1978a) Dimethyl sulfoxide as an electron acceptor for an aerobic growth. Arch Microbiol 116:35–40Google Scholar
  68. Zinder SH, Brock TD (1978b) Methane, carbon dioxide and hydrogen sulfide production from the terminal methiol group of methionine by anaerobic lake sediments. Appl Envir Microbiol 35:344–352Google Scholar
  69. Zinder SH, Brock TD (1978c) Production of methane and carbon dioxide from metane thiol and dimethyl sulfide by anaerobic lake sediments. Nature 273:226–228Google Scholar

Copyright information

© Dr. S. Bernhard, Dahlem Konferenzen 1986

Authors and Affiliations

  • J. Bauld
    • 1
  1. 1.Baas Becking Geobiological LaboratoryCanberra CityAustralia

Personalised recommendations