Skip to main content

Sulfide-Dependent Anoxygenic Photosynthesis in Prokaryotes

Sulfide-Quinone Reductase (SQR), the Initial Step

  • Chapter
The Phototrophic Prokaryotes

Abstract

Anoxygenic photosynthesis with sulfide serving as the electron donor is a property unique to prokaryotes. Most photosynthetic bacteria can grow photoautotrophically using sulfide (as well as few other inorganic sulfur compounds) as electron donors for CO2 fixation (see ref. 1 for recent review). Cyanobacteria are exceptional in the world of phototrophic prokaryotes. With the closely related prochlorophytes, they are the only eubacteria that can perform plant-type oxygenic photosynthesis, using two photosystems in series and water as the electron donor. However, some species of cyanobacteria can facultatively shift to anoxygenic, sulfide-dependent photosynthesis in which only PS I is involved2-5. This unique capacity to shift between anoxygenic and oxygenic photosynthesis was discovered in various strains of cyanobacteria, evolutionarily distant from each other3. It was considered to represent a primitive relic of the evolution of photosynthesis6. Of these strains, the filamentous cyanobacterium Oscillatoria limnetica has been studied most extensively. O. limnetica shifts to anoxygenic photosynthesis 2—3 hours after incubation in the presence of sulfide and light, in an inducible process specific to sulfide7, 8. Depending on the growth conditions, the induced cells perform several sulfide-dependent reactions: CO2 fixation, 3, 7-9 H2 evolution10 or N2 fixation. 11

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Brune, D. C. (1995) Sulfur compounds as photosynthetic electron donors. In: Anoxygenic Photosynthetic Bacteria (Blankenship, R. E., Madigan, M. T. and Bauer, C. E., eds.) pp. 847–870, Kluwer Academic Publishers, The Netherlands.

    Google Scholar 

  2. Padan, E. (1979) Facultative anoxygenic photosynthesis in cyanobacteria. Annu. Rev. Plant Physiol. 30, 27–40.

    Article  CAS  Google Scholar 

  3. Garlick S., Oren, A. and Padan, E. (1977) Occurrence of facultative anoxygenic photosynthesis among filamentous unicellular cyanobacteria. J. Bacteriol. 129, 623–629.

    PubMed  CAS  Google Scholar 

  4. Belkin S., Shahak, Y. and Padan, E. (1988) Anoxygenic photosynthetic electron transport. In: Methods in Enzymology. (Packer, L. and Glazer A. N., eds.) Vol. 167, pp. 380–386, Academic Press, San Diego.

    Google Scholar 

  5. Stal, J. L. (1995) Physiological ecology of cyanobacteria in microbial mats and other communities. New Phytol. 131, 1–32.

    Article  CAS  Google Scholar 

  6. Padan, E. (1989) Combined molecular and physiological approach to anoxygenic photosynthesis of cyanobacteria. In: Microbial Mats, Physiological Ecology of Benthic Microbial Communities (Cohen, Y. and Rosenberg E., eds.) pp. 277–282.

    Google Scholar 

  7. Cohen, Y, Padan, E and Shilo, M. (1975) Facultative anoxygenic photosynthesis in the cyanobacterium Oscillatoria limnetica. J. Bacteriol. 123, 855–861.

    PubMed  CAS  Google Scholar 

  8. Oren, A. and Padan, E. (1978) Induction of anaerobic photoautotrophic growth in the cyanobacterium Oscillatoria limnetica. J. Bacteriol. 133, 558–563.

    PubMed  CAS  Google Scholar 

  9. Cohen Y., Jorgensen, B. B., Padan, E and Shilo, M. (1975) Sulfide-dependent anoxygenic photosynthesis in the cyanobacterium Oscillatoria limnetica Nature (London) 257, 489–492.

    Article  CAS  Google Scholar 

  10. Belkin, S. and Padan, E. (1978) Sulfide-dependent hydrogen evolution in the cyanobacterium Oscillatoria limnetica. FEBS Lett. 94, 291–294.

    Article  CAS  Google Scholar 

  11. Belkin S., Arieli, B. and Padan E. (1982) Sulfide-dependent electron transport in Oscillatoria limnetica. Isr. J. Botany 31, 199–200.

    CAS  Google Scholar 

  12. Knaff, D. B. and Kampf, C. (1987) in: New Comprehensive Biochemistry (Ametz, J. ed.) Vol. 15, pp. 199–211, Elsevier, Amsterdam.

    Google Scholar 

  13. Chen Z., Koh ML, van Dreissche G., van Beeumen J. J., Bartsch R. G., Meyer T. E., Cusanovich M. A. and Mathews F. S. (1994) The structure of flavocytochrome c sulfide dehydrogenase from a purple phototrophic bacterium. Science 266, 430–432.

    Article  PubMed  CAS  Google Scholar 

  14. Steinmetz, M. A., Trüper H. G. and Fischer, U. (1983) Cytochrome c-555 and iron-sulfur proteins of the non-thiosulfate-utilizing green sulfur bacterium Chlorobium vibrioforme. Arch. Microbiol. 135, 186–190.

    Article  CAS  Google Scholar 

  15. Brune, D. C., and Trüper, H. G. (1986) Noncyclic electron transport in chromatophores of photolithotrophy-cally grown Rhodobacter sulfidophilus. Arch. Microbiol. 145, 295–301.

    Article  CAS  Google Scholar 

  16. Trumpower B. L. 1990 Cytochrome bc1 complexes of microorganisms. Microbiol. Rev. 54] 101–129

    Google Scholar 

  17. Shahak Y., Arieli B., Binder, B. and Padan, E. (1987) Sulfide-dependent photosynthetic electron flow coupled to proton translocation in thylakoids of the cyanobacterium Oscillatoria limnetica. Arch. Biochem. Biophys. 259, 605–615.

    Article  PubMed  CAS  Google Scholar 

  18. Slooten L., deSmet, M. and Sybesma, C. (1989) Sulfide-dependent electron transport in thylakoids from the cyanobacterium Oscillatoria limnetica. Biochim. Biophys. Acta 973, 272–280.

    Article  CAS  Google Scholar 

  19. Arieli B., Padan, E. and Shahak, Y. (1991) Sulfide induced sulfide-quinone reductase activity in thylakoids of Oscillatoria limnetica. J. Biol. Chem. 266, 104–111.

    PubMed  CAS  Google Scholar 

  20. Shahak, Y, Arieli B., Hauska G., Herrmann, I. and Padan, E. (1992) Isolation of sulfide-quinone reductase (SQR) from prokaryotes. Phyton 32, 133–137.

    CAS  Google Scholar 

  21. Arieli B., Shahak, Y, Taglicht D., Hauska, G. and Padan, E. (1994) Purification and characterization of sulfide-quinone reductase (SQR), a novel enzyme driving anoxygenic photosynthesis in Oscillatoria limnetica. J. Biol. Chem., 269, 5705–5711.

    PubMed  CAS  Google Scholar 

  22. Arieli, B, Binder B., Shahak, Y. and Padan, E. (1989) Sulfide induces the synthesis of a periplasmic protein in the cyanobacterium Oscillatoria limnetica. J. Bacteriol. 171: 699–702.

    PubMed  CAS  Google Scholar 

  23. Shahak, Y, Hauska G., Herrmann I., Arieli B., Taglicht, D. and Padan, E. (1992) Sulfide-quinone reductase (SQR) drives anoxygenic photosynthesis in prokaryotes. In: Research in Photosynthes is (Murata N., ed.), Vol. II, pp 483–486 Kluwer Academic Publishers,The Netherland

    Google Scholar 

  24. Yamanaka, T. and Kusai, A. (1976) In Flavins and Flavoproteins (Singer T. P., ed) pp. 292–301, Elsevier, Amsterdam.

    Google Scholar 

  25. Wierenga, R. K., Terpstra P., and Hol, W. G. J. (1986) Prediction of the occurrence of the ADP-binding βαβ-fold in proteins, using an amino acid sequence fingerprint. J. Mol. Biol. 187, 101–107.

    Article  PubMed  CAS  Google Scholar 

  26. Eggink G., Engel H., Vriend G., Terpstra, P. and Witholt, B. (1990) Ruberdoxin reductase of Pseudo-monas oleovorans. Structural relationship to other flavoprotein oxidoreductases based on one NAD and two FAD fingerprints. J. Mol. Biol. 212, 135–142.

    Article  PubMed  CAS  Google Scholar 

  27. Feiler, U. and Hauska, G. (1995) The reaction center from green sulfur bacteria. In: Anoxygenic Photosynthetic Bacteria (Blankenship, R. E., Madigan, M. T. and Bauer, C. E., eds.) pp. 665–685, Kluwer Academic Publishers, Dordrecht, Holland.

    Google Scholar 

  28. Buchanan, S. K., Fritzsch G., Ermler, U. and Michel, H. (1993) New crystal form of the photosynthetic reaction center from Rhodobacter spheroides of improved diffraction quality. J. Mol. Biol. 230, 1311–1314.

    Article  PubMed  CAS  Google Scholar 

  29. Shahak, Y, Arieli B., Padan, E. and Hauska, G. (1992) Sulfide-quinone reductase (SQR) activity in Chlorobium. FEBS Lett. 299, 127–130.

    Article  PubMed  CAS  Google Scholar 

  30. Shahak, Y, Klughammer C., Schreiber U., Padan E., Herrmann, I. and Hauska, G. (1994) Sulfide-quinone and sulfide-cytochrome reduction in Rhodobacter capsulatus. Photosynt. Res. 39, 175–181.

    Article  CAS  Google Scholar 

  31. Klughammer C., Hager C., Padan E., Schütz M., Schreiber U., Shahak, Y and Hauska, G. (1995) Reduction of cytochromes with menaquinol and sulfide in membranes from green sulfur bacteria. Photosynt. Res. 43, 27–34.

    Article  CAS  Google Scholar 

  32. Schütz M., Shahak Y., Padan, E. and Hauska, G. (1996) Purification and characterization of the sulfide-quinone reductase (SQR) of Rhodobacter capsulatus DSM 155. Proc. Xth International Congress of Photosynthesis, Montpellier, France (Mathis P., ed.) Vol II, pp 673–676, Kluwer Academic Publishers.

    Google Scholar 

  33. Schütz M., Shahak, Y, Padan, E. and Hauska, G. (1997) Sulfide-quinone reductase from Rhodobacter capsulatus: purification, cloning and expression. J. Biol. Chem., 272, 9890–9894.

    Article  PubMed  Google Scholar 

  34. Hansen, T, and van Gemerden, H. (1972) Sulfide utilization by purple nonsulfur bacteria. Arch. Microbiol. 86, 49–56.

    CAS  Google Scholar 

  35. Alberti M., Burke, D. H. and Hearst, J. E. (1995) Structure and sequence of the photosynthesis gene cluster. In: Anoxygenic Photosynthetic Bacteria (Blankenship, R. E., Madigan, M. T., and Bauer, C. E., eds) pp. 1083–1106, Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Google Scholar 

  36. Karplus, P. A. and Schulz, G. E. (1987) Refined Structure of Glutathion Reductase at 1, 54A Resolution. J. Mol. Biol. 195, 701–729.

    Article  PubMed  CAS  Google Scholar 

  37. Krauth-Siegel, R. L., Blatterspiel R., Saleh M., Schiltz E., Schirmer, R. H. and Untucht-Grau, R. (1982) Glutathion Reductase from Human Erythrocytes. Eur. J. Biochem. 121, 259–267.

    Article  PubMed  CAS  Google Scholar 

  38. Schierbeck, A. J., Swarte, M. B. A., Dijkstra, B. W., Vriend G., Read, R. J., Hol, W. G. J., Drenth, J. and Betzel, C. (1989) X-ray Structure of Lipoamide Dehydrogenase from Azotobacter vinelandii determined by a Combination of Molecular and Isomorphous Replacement Techniques. J. Mol. Biol. 206, 365–379.

    Article  Google Scholar 

  39. Woese CR (1987) Bacterial evolution. Microbiol. Reviews 51: 221–271.

    CAS  Google Scholar 

  40. Fenchel, T. M. and Riedl, R. J. (1970) The sulfide system. A new biotic community underneath the oxidised layer of marine sand bottom. Mar. Biol. 7, 255–268.

    Article  CAS  Google Scholar 

  41. Fenchel, T. and Bernar, C. (1995) Mats of colourless sulphur bacteria. I. Major microbial processes. Mar. Ecol. Prog. Ser. 128, 161–170.

    Article  Google Scholar 

  42. Schiemer F., Novak, R. and Ott, J. (1990) Metabolic studies on thiobiotic free-living nematodes and their symbiotic microorganisms. Mar. Biol. 106, 129–137.

    Article  CAS  Google Scholar 

  43. Völkel, S. and Grieshaber, M. K. (1996) Mitochondrial sulphide oxidation in the lugworm Arenicola marina. Evidence for alternative electron pathways. Eur. J. Biochem. 235: 231–377.

    Article  PubMed  Google Scholar 

  44. Kelly, D. P., Shergill, J. K., Lu, W-P. and Wood, A. P. (1997) Oxidative metabolism of inorganic sulfur compounds by bacteria. Antonie van Leeuwenhock 71, 95–107.

    Article  CAS  Google Scholar 

  45. Burggraf S., Olsen, G. J., Stetter, K. O. and Woese, C. R. (1992) A phylogenetic analysis of A quifex pyrophilus. Syst. Appl. Microb. 15, 352–356

    Article  CAS  Google Scholar 

  46. Völkel, S. and Grieshaber, M. K. (1997) Sulphide oxidation and oxidative phosphorylation in the mitochondria of the lugworm Arenicola marina. J. Exp. Biol. 200, 83–92.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1999 Springer Science+Business Media New York

About this chapter

Cite this chapter

Shahak, Y., Schütz, M., Bronstein, M., Griesbeck, C., Hauska, G., Padan, E. (1999). Sulfide-Dependent Anoxygenic Photosynthesis in Prokaryotes. In: Peschek, G.A., Löffelhardt, W., Schmetterer, G. (eds) The Phototrophic Prokaryotes. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-4827-0_26

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-4827-0_26

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-7188-5

  • Online ISBN: 978-1-4615-4827-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics