Introduction to Sulfur Metabolism in Phototrophic Organisms

  • Christiane Dahl
  • Rüdiger Hell
  • Thomas Leustek
  • David Knaff
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 27)

Sulfur is one of the most versatile elements in life due to its reactivity in different oxidation and reduction states. In phototrophic organisms, the redox properties of sulfur in proteins and of sulfur-containing metabolites are particularly important for the mediation between the reductive assimilation processes of photosynthesis and reactive oxygen species that arise as by-products of electron transport chains in chloroplasts and mitochondria. Further, reduced sulfur compounds play a prominent role as electron donors for photosynthetic carbon dioxide fixation in anoxygenic phototrophic sulfur bacteria. The assimilatory process is part of the biological sulfur cycle that is completed by dissimilation of reduced sulfur compounds. In contrast to the assimilatory provision of sulfur-containing cell constituents that is found in most taxonomic groups, dissimilation is restricted to prokaryotes and serves energy-yielding processes where sulfur compounds are donors or acceptors of electrons. Interest in the investigation of the multiple functions of sulfur-related processes has exponentially increased in recent years, especially in molecular and cellular biology, biochemistry, agrobiotechnology and ecology.

Keywords

Phytoplankton Assimilation Taurin Thiophene Rhizobium 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abrams WR and Schiff JA (1973) Studies on sulfate utilization by algae. 11. An enzyme-bound intermediate in the reduction of adenosine-5′-phosphosulfate (APS) by cell-free extracts of wild-type Chlorella and mutants blocked for sulfate reduction. Arch Microbiol 94: 1–10Google Scholar
  2. Abrol YP and Ahmad A (2005) Sulphur in Plants. Kluwer Academic Publishers, LondonGoogle Scholar
  3. Barbosa-Jefferson VL, Zhao FJ, Mcgrath SP and Magan N (1998) Thiosulphate and tetrathionate oxidation in arable soils. Soil Biol Biochem 30: 553–559CrossRefGoogle Scholar
  4. Barrett EL and Clark MA (1987) Tetrathionate reduction and production of hydrogen sulfide from thiosulfate. Microbiol Rev 51: 192–205PubMedGoogle Scholar
  5. Bavendamm W (1924) Die farblosen und roten Schwefelbakterien des Süß- und Salzwassers. In: Kolkwitz R (ed) Pflanzenforschung (2), pp 1–156. Verlag G. Fischer, JenaGoogle Scholar
  6. Beer-Romero P and Gest H (1987) Heliobacillus mobilis, a peritrichously flagellated anoxyphototroph containing bacteriochlorophyll g. FEMS Microbiol Lett 41: 109–114CrossRefGoogle Scholar
  7. Beinert H (2000) A tribute to sulfur. Eur J Biochem 267: 5657–5664PubMedCrossRefGoogle Scholar
  8. Berendt U, Haverkamp T and Schwenn JD (1995) Reaction mechanism of thioredoxin: 3′-phospho-adenylylsulfate reductase investigated by site-directed mutagenesis. Eur J Biochem 233: 347–356PubMedCrossRefGoogle Scholar
  9. Berndt C, Lillig CH, Wollenberg M, Bill E, Mansilla MC, de Mendoza D, Seidler A and Schwenn JD (2004) Characterization and reconstitution of a 4Fe–4S adenylyl sulfate/phosphoadenylyl sulfate reductase from Bacillus subtilis. J Biol Chem 279: 7850–7855PubMedCrossRefGoogle Scholar
  10. Bick JA, Aslund F, Chen YC and Leustek T (1998) Glutaredoxin function for the carboxyl-terminal domain of the plant-type 5′-adenylylsulfate reductase. Proc Natl Acad Sci USA 95: 8404–8409PubMedCrossRefGoogle Scholar
  11. Bick JA, Dennis JJ, Zylstra GJ, Nowack J and Leustek T (2000) Identification of a new class of 5′-adenylylsulfate (APS) reductases from sulfate-assimilating bacteria. J Bacteriol 182: 135–142PubMedCrossRefGoogle Scholar
  12. Brown KA (1982) Sulfur in the environment: a review. Environ Pollut 3B: 47–80Google Scholar
  13. Brune DC (1989) Sulfur oxidation by phototrophic bacteria. Biochim Biophys Acta 975: 189–221PubMedCrossRefGoogle Scholar
  14. Brune DC (1995) Sulfur compounds as photosynthetic electron donors. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, (Advances in Photosynthesis, Vol.2) pp 847–870. Kluwer Academic Publishers, DordrechtGoogle Scholar
  15. Brunold C and Schiff JA (1976) Studies of sulfate utilization by algae. 15. Enzymes of assimilatory sulfate reduction in Euglena and their cellular localization. Plant Physiol 57: 430–436PubMedCrossRefGoogle Scholar
  16. Brüser T, Lens P and Trüper HG (2000) The biological sulfur cycle. In: Lens P and Pol LH (eds) Environmental Technologies to Treat Sulfur Pollution, pp 47–86. IWA Publishing, LondonGoogle Scholar
  17. Bryantseva IA, Gorlenko VM, Kompantseva EI, Tourova TP, Kuznetsov B and Osipov GA (2000) Alkaliphilic heliobacterium Heliorestis baculata sp. nov. and emended description of the genus Heliorestis. Arch Microbiol 174: 283–291PubMedCrossRefGoogle Scholar
  18. Buder J (1915) Zur Kenntnis des Thiospirillum jenense und seine Reaktionen auf Lichtreize. Jahrb f wiss Bot 56: 529–584Google Scholar
  19. Buder J (1919) Zur Biologie des Bakteriopurpurins und der Purpurbakterien. Jahrb f wiss Bot 58: 525–628Google Scholar
  20. Bunker HJ (1936) A Review of the Physiology and Biochemistry of the Sulfur Bacteria. HM Stationery Office, LondonGoogle Scholar
  21. Cohen Y, Padan E and Shilo M (1975) Facultative anoxygenic photosynthesis in the cyanobacterium Oscillatoria limnetica. J Bacteriol 123: 855–861PubMedGoogle Scholar
  22. Cohn F (1875) Untersuchungen über Bakterien II. Beitr z Biol d Pflanzen 1: 141–207Google Scholar
  23. Cooper RM, Resende MLV, Flood J, Rowan MG, Beale MH and Potter U (1996) Detection and cellular localization of elemental sulphur in disease-resistant genotypes of Theobroma cacao. Nature 379: 159–162CrossRefGoogle Scholar
  24. Cooper RM and Williams JS (2004) Elemental sulphur as an induced antifungal substance in plant defence. J Exp Bot 55: 1947–1953PubMedCrossRefGoogle Scholar
  25. Dahl C and Friedrich CG (2007) Microbial Sulfur Metabolism. Springer, Berlin, Heidelberg, New YorkGoogle Scholar
  26. Dahl C and Prange A (2006) Bacterial sulfur globules: occurrence, structure and metabolism. In: Shively JM (ed) Inclusions in Prokaryotes, pp 21–51. Springer, HeidelbergCrossRefGoogle Scholar
  27. Dahl C, Prange A and Steudel R (2002) Natural polymeric sulfur compounds. In: Steinbüchel A (ed) Miscellaneous Biopolymers and Biodegradation of Synthetic Polymers, pp 35–62. Wiley-VCH, WeinheimGoogle Scholar
  28. De Kok LJ and Schnug E (2005) Proceedings of the 1st Sino-German workshop on aspects of sulfur nutrition in plants. Landbauforschung Völkenrode–FAL Agricult Res special issue No 283Google Scholar
  29. de Wit R and van Gemerden H (1987) Oxidation of sulfide to thiosulfate by Microcoleus chtonoplastes. FEMS Microbiol Ecol 45: 7–13CrossRefGoogle Scholar
  30. Denger K, Laue H and Cook AM (1997) Thiosulfate as a metabolic product: the bacterial fermentation of taurine. Arch Microbiol 168: 297–301PubMedCrossRefGoogle Scholar
  31. Dick WA (1992) Sulfur cycle. In: Lederberg J (ed) Encyclopedia of Microbiology, pp 123–133. Academic, San DiegoGoogle Scholar
  32. Ehrenberg CG (1838) Die Infusionsthierchen als vollkommene Organismen. Ein Blick in das tiefere organische Leben der Natur. Leopold Voss-Verlag, LeipzigGoogle Scholar
  33. Engelmann TW (1882) Ueber Licht- und Farbenperception niederster Organismen. E Pflüger Arch f Physiol 29: 387–400CrossRefGoogle Scholar
  34. Falbe J and Regitz M (1995) Römpp Chemie Lexikon, 9th edn. Thieme, StuttgartGoogle Scholar
  35. Falkowski PG (2006) Evolution: tracing oxygen’s imprint on Earth’s metabolic evolution. Science 311: 1724–1725PubMedCrossRefGoogle Scholar
  36. Friedrich CG (1998) Physiology and genetics of sulfur-oxidizing bacteria. Adv Microb Physiol 39: 235–289PubMedCrossRefGoogle Scholar
  37. Friedrich CG, Bardischewsky F, Rother D, Quentmeier A and Fischer J (2005) Prokaryotic sulfur oxidation. Curr Opin Microbiol 8: 253–259PubMedCrossRefGoogle Scholar
  38. Friedrich CG, Rother D, Bardischewsky F, Quentmeier A and Fischer J (2001) Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl Environ Microbiol 67: 2873–2882PubMedCrossRefGoogle Scholar
  39. Gao Y, Schofield OME and Leustek T (2000) Characterization of sulfate assimilation in marine algae focusing on the enzyme 5′-adenylylsulfate reductase. Plant Physiol 123: 1087–1096PubMedCrossRefGoogle Scholar
  40. Giordano M, Norici A and Hell R (2005) Sulfur and phytoplankton: acquisition, metabolism and impact on the environment. New Phytologist 166: 371–382PubMedCrossRefGoogle Scholar
  41. Grieshaber MK and Völkel S (1998) Animal adaptations for tolerance and exploitation of poisonous sulfide. Ann Rev Physiol 60: 33–53CrossRefGoogle Scholar
  42. Gutierrez-Marcos JF, Roberts MA, Campbell EI and Wray JL (1996) Three members of a novel small gene-family from Arabidopsis thaliana able to complement functionally an Escherichia coli mutant defective in PAPS reductase activity encode proteins with a thioredoxin-like domain and “APS reductase” activity. Proc Natl Acad Sci USA 93: 13377–13382PubMedCrossRefGoogle Scholar
  43. Harborne JB (1988) Introduction to Ecological Biochemistry. Academic, LondonGoogle Scholar
  44. Haverkamp T and Schwenn JD (1999) Structure and function of a cysBJIH gene cluster in the purple sulfur bacterium Thiocapsa roseopersicina. Microbiology 145: 115–125PubMedCrossRefGoogle Scholar
  45. Hawkesford M (2004) Sulphur metabolism in plants. J Exp Bot 55: (404) special issueGoogle Scholar
  46. Hawkesford M and De Kok LJ (2007) Sulfur in Plants. An Ecological Perspective. Springer, LondonCrossRefGoogle Scholar
  47. Heidelberg JF, Seshadri R, Haveman SA, Hemme CL, Paulsen IT, Kolonay JF, Eisen JA, Ward N, Methe B, Brinkac LM, Daugherty SC, Deboy RT, Dodson RJ, Durkin AS, Madupu R, Nelson WC, Sullivan SA, Fouts D, Haft DH, Selengut J, Peterson JD, Davidsen TM, Zafar N, Zhou L, Radune D, Dimitrov G, Hance M, Tran K, Khouri H, Gill J, Utterback TR, Feldblyum TV, Wall JD, Voordouw G and Fraser CM (2004) The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat Biotechnol 22: 554–559PubMedCrossRefGoogle Scholar
  48. Hell R (1997) Molecular physiology of plant sulfur metabolism. Planta 202: 138–148PubMedCrossRefGoogle Scholar
  49. Hell R and Kruse C (2007) Sulfur in biotic interactions of plants. In: Hawkesford M and De Kok LJ (eds) Sulfur in Plants. An Ecological Perspective, pp 197–224. Springer, LondonCrossRefGoogle Scholar
  50. Hell R and Leustek T (2005) Sulfur metabolism in plants and algae–a case study for an integrative scientific approach. Photosyn Res 86: 297–298PubMedCrossRefGoogle Scholar
  51. Hesse H and Hoefgen R (2003) Molecular aspects of methionine biosynthesis. Trends Plant Sci 8: 259–262PubMedCrossRefGoogle Scholar
  52. Houba VJG and Uittenbogaard J (1994) Chemical Composition of Various Plant Species. Wageningen University, The NetherlandsGoogle Scholar
  53. Imai S, Tsuge N, Tomotake M, Nagatome Y, Sawada H, Nagata T and Kumagai H (2002) An onion enzyme that makes the eyes water–A flavoursome, user-friendly bulb would give no cause for tears when chopped up. Nature 419: 685PubMedCrossRefGoogle Scholar
  54. Kanno N, Nagahisa E, Sato M and Sato Y (1996) Adenosine 5′-phosphosulfate sulfotransferase from the marine macroalga Porphyra yezoensis Ueda (Rhodophyta): Stabilization, purification, and properties. Planta 198: 440–446CrossRefGoogle Scholar
  55. Kelly DP and Smith NA (1990) Organic sulfur compounds in the environment. Adv Microb Ecol 11: 345–385Google Scholar
  56. Kim SO, Merchant K, Nudelman R, Beyer WF, Keng T, DeAngelo J, Hausladen A and Stamler JS (2002) OxyR: a molecular code for redox-related signaling. Cell 109: 383–396PubMedCrossRefGoogle Scholar
  57. Kopriva S, Fritzemeier K, Wiedemann G and Reski R (2007) The putative moss 3′-phosphoadenosine phosphosulfate reductase is a novel form of adenosine 5′-phosphosulfate reductase without iron sulfur cluster. J Biol Chem 282: 22930–22938PubMedCrossRefGoogle Scholar
  58. Kredich NM (1987) Biosynthesis of cysteine. In: Neidhardt FC, Ingraham TL, Low KB, Magasanik B, Schaechter M and Umbarger HE (eds) Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, pp 419–428. American Society of Microbiology, Washington, DCGoogle Scholar
  59. Lens PNL and Kuenen JG (2001) The biological sulfur cycle: novel opportunities for environmental biotechnology. Water Sci Technol 44: 57–66PubMedGoogle Scholar
  60. Leustek T, Martin MN, Bick JA and Davies JP (2000) Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu Rev Plant Physiol Plant Mol Biol 51: 141–165PubMedCrossRefGoogle Scholar
  61. Li J and Schiff JA (1991) Purification and properties of adenosine 5′-phophosulfate sulfotransferase from Euglena. Biochem J 274: 355–360PubMedGoogle Scholar
  62. Luther GW, Church TM, Scudlark JR and Cosman M (1986) Inorganic and organic sulfur cycling in salt-marsh pore waters. Science 232: 746–749PubMedCrossRefGoogle Scholar
  63. Madigan MT and Ormerod JG (1995) Taxonomy, physiology and ecology of heliobacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, (In Advances in Photosynthesis, Vol. 2) pp 17–30. Kluwer Academic Publishers, DordrechtGoogle Scholar
  64. Matias PM, Pereira IAC, Soares CM and Carrondo MA (2005) Sulphate respiration from hydrogen in Desulfovibrio bacteria: a structural biology overview. Prog Biophys Molec Biol 89: 292–329CrossRefGoogle Scholar
  65. Middelburg J (2000) The geochemical sulfur cycle. In: Lens P and Hulshoff Pol W (eds) Environmental Technologies to Treat Sulfur Pollution, pp 33–46. IWA Publishing, LondonGoogle Scholar
  66. Mitchell SC (1996) Biological Interactions of Sulfur Compounds. Taylor and Francis, LondonGoogle Scholar
  67. Mothes K and Specht W (1934) Über den Schwefeltoffwechsel der Pflanzen. Planta 22: 800–803CrossRefGoogle Scholar
  68. Müller A and Krebs B (1984) Sulfur – Its Significance for Chemistry, for the Geo-, Bio- and Cosmosphere and Technology. Elsevier, AmsterdamGoogle Scholar
  69. Müller C (1870) Chemisch-Physikalische Beschreibung der Thermen von Baden in der Schweiz (Canton Aargau). Zehnder, BadenGoogle Scholar
  70. Müller OF (1786) Animalcula Infusoria Fluviatilia Et Marina, Quae Detexit, Systematice Descripsit Et Ad Vivum Delineari Curavit. Mölleri, HauniaeGoogle Scholar
  71. Nadson GA (1906) The morphology of the lower algae. III Chlorobium limicola Nads., the green chlorophyll bearing microbe (in Russian). Bull Jard Bot St Petersb 6: 190–194Google Scholar
  72. Nelson DC and Fisher CR (1995) Chemoautotrophic and methanoautotrophic endosymbiontic bacteria at deep-sea vents and seeps. In: Karl DM (ed) Deep-Sea Hydrothermal Vents, pp 125–167. CRC Press, Boca Raton, FLGoogle Scholar
  73. Neumann S, Wynen A, Trüper HG and Dahl C (2000) Characterization of the cys gene locus from Allochromatium vinosum indicates an unusual sulfate assimilation pathway. Mol Biol Reports 27: 27–33CrossRefGoogle Scholar
  74. Norici A, Hell R and Giordano M (2005) Sulfur and primary production in aquatic environments: an ecological perspective. Photosyn Res 86: 409–417PubMedCrossRefGoogle Scholar
  75. Perty M (1852) Zur Kenntnis kleinster Lebensformen nach Bau, Funktionen, Systematik, mit Spezialverzeichnis der in der Schweiz Beobachteten. Jent und Reinert, BernGoogle Scholar
  76. Philips D and Philips SL (2000) High temperature dissociation constants of HS and the standard thermodynamic values for S2−. J Chem Eng Data 45: 981–987CrossRefGoogle Scholar
  77. Postgate JR (1968) The sulphur cycle. In: Nickless G (ed) Inorganic Sulphur Chemistry, pp 259–279. Elsevier, AmsterdamGoogle Scholar
  78. Prange A, Chauvistré R, Modrow H, Hormes J, Trüper HG and Dahl C (2002) Quantitative speciation of sulfur in bacterial sulfur globules: X-ray absorption spectroscopy reveals at least three different speciations of sulfur. Microbiology 148: 267–276PubMedGoogle Scholar
  79. Rabenstein A, Rethmeier J and Fischer U (1995) Sulphite as intermediate sulphur compound in anaerobic sulphide oxidation to thiosulphate by marine cyanobacteria. Z Naturforsch 50c: 769–774Google Scholar
  80. Rausch T and Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10: 503–509PubMedCrossRefGoogle Scholar
  81. Roche P, Debelle F, Maillet F, Lerouge P, Faucher C, Truchet G, Denarie J and Prome JC (1991) Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell 67: 1131–1143PubMedCrossRefGoogle Scholar
  82. Roy AB and Trudinger PA (1970) The Biochemistry of Inorganic Compounds of Sulfur. Cambridge University Press, LondonGoogle Scholar
  83. Saito K, De Kok LJ, Stulen I, Hawkesford MJ, Schnug E and Sirko A (2005) Sulfur Transport and Assimilation in the Postgenomic Era. Backhuys Publishers, LeidenGoogle Scholar
  84. Schippers A and Sand W (1999) Bacterial leaching of metal sulfides proceeds by two indirect mechanisms via thiosulfate or via polysulfides and sulfur. Appl Environ Microbiol 65: 319–321PubMedGoogle Scholar
  85. Schmidt A (1973) Sulfate reduction in a cell-free system of Chlorella. The ferredoxin-dependent reduction of a protein-bound intermediate by a thiosulfonate reductase. Arch Microbiol 93: 29–52Google Scholar
  86. Schmidt A and Jäger K (1992) Open questions about sulfur metabolism in plants. Annu Rev Plant Physiol Plant Mol Biol 43: 325–349CrossRefGoogle Scholar
  87. Schnug E (1998) Sulfur in Agroecosystems. Series: Nutrients in Ecosystems, Vol. 2. Springer, New YorkGoogle Scholar
  88. Schwenn JD (1989) Sulphate assimilation in higher plants–a thioredoxin-dependent PAPS-reductase from spinach leaves. Z Naturforsch C 42: 93–102Google Scholar
  89. Setya A, Murillo M and Leustek T (1996) Sulfate reduction in higher plants: Molecular evidence for a novel 5′-adenylylsulfate reductase. Proc Natl Acad Sci USA 93: 13383–13388PubMedCrossRefGoogle Scholar
  90. Stetter KO (1996) Hyperthermophilic prokaryotes. FEMS Microbiol Rev 18: 149–158CrossRefGoogle Scholar
  91. Steudel R (1982) Homocyclic sulfur molecules. Topics Curr Chem 102: 149–176Google Scholar
  92. Steudel R (1985) Neue Entwicklungen in der Chemie des Schwefels und des Selens. Nova Acta Leopoldina 264: 231–246Google Scholar
  93. Steudel R (1987) Sulfur homocycles. In: Haiduc I and Sowerby DB (eds) The Chemistry of Inorganic Homo- and Heterocycles, pp 737–768. Academic Press, LondonGoogle Scholar
  94. Steudel, R (1996a) Das gelbe Element und seine erstaunliche Vielseitigkeit. Chemie in unserer Zeit 30: 226–234CrossRefGoogle Scholar
  95. Steudel R (1996b) Mechanism for the formation of elemental sulfur from aqueous sulfide in chemical and microbiological desulfurization processes. Ind Eng Chem Res 35: 1417–1423CrossRefGoogle Scholar
  96. Steudel R (1998) Chemie der Nichtmetalle, 2nd edn. W. de Gruyter, BerlinGoogle Scholar
  97. Steudel R (2000) The chemical sulfur cycle. In: Lens P and Hulshoff Pol W (eds) Environmental Technologies to Treat Sulfur Pollution, pp 1–31. IWA Publishing, LondonGoogle Scholar
  98. Steudel R (2003a) Elemental Sulfur and Sulfur-Rich Compounds I. Springer, BerlinGoogle Scholar
  99. Steudel R (2003b) Elemental Sulfur and Sulfur-Rich Compounds II. Springer, BerlinGoogle Scholar
  100. Steudel R and Albertsen A (1999) The chemistry of aqueous sulfur sols – models for bacterial sulfur globules? In: Steinbüchel A (ed) Biochemical Principles and Mechanisms of Biosynthesis and Biodegradation of Polymers, pp 17–26. Wiley-VCH, WeinheimGoogle Scholar
  101. Steudel R and Eckert B (2003) Solid sulfur allotropes. In: Steudel R (ed) Elemental Sulfur and Sulfur-Rich Compounds, pp 1–79. Springer, BerlinGoogle Scholar
  102. Steudel R and Holz B (1988) Detection of reactive sulfur molecules (S6, S7, S9, Sµ), in commercial sulfur, in sulfur minerals, and in sulfur metals slowly cooled to 20 °C. Z Naturforsch B 43: 581–589Google Scholar
  103. Steudel R and Kustos M (1994) Organic polysulfanes. In: King RB (ed) Encyclopedia of Inorganic Chemistry, pp 4009–4038. Wiley, SussexGoogle Scholar
  104. Steudel R, Holdt G and Nagorka R (1986) On the autoxidation of aqueous sodium polysulfide. Z Naturforsch 41b: 1519–1522Google Scholar
  105. Suter M, von Ballmoos P, Kopriva S, den Camp RO, Schaller J, Kuhlemeier C, Schürmann P and Brunold C (2000) Adenosine 5′-phosphosulfate sulfotransferase and adenosine 5′-phosphosulfate reductase are identical enzymes. J Biol Chem 275: 930–936PubMedCrossRefGoogle Scholar
  106. Takano B and Watanuki K (1988) Quenching and liquid chromatographic determination of polythionates in natural water. Talanta 35: 847–854PubMedCrossRefGoogle Scholar
  107. Trüper HG (1984a) Microorganisms and the sulfur cycle. In: Müller A and Krebs B (eds) Sulfur, Its Significance for Chemistry, for the Geo-, Bio-, and Cosmosphere and Technology, pp 351–365. Elsevier Science Publishers B.V., AmsterdamGoogle Scholar
  108. Trüper HG (1984b) Phototrophic bacteria and their sulfur metabolism. In: Müller A and Krebs B (eds) Sulfur, Its Significance for Chemistry, for the Geo-, Bio-, and Cosmosphere and Technology, pp 367–382. Elsevier Science Publishers B.V., AmsterdamGoogle Scholar
  109. Trüper HG (1989) Physiology and biochemistry of phototrophic bacteria. In: Schlegel HG and Bowien B (eds) Autotrophic Bacteria, pp 267–281. Science Tech Publishers, MadisonGoogle Scholar
  110. Trüper HG and Fischer U (1982) Anaerobic oxidation of sulphur compounds as electron donors for bacterial photosynthesis. Phil Trans R Soc Lond B 298: 529–542CrossRefGoogle Scholar
  111. van Niel BC (1936) On the metabolism of the Thiorho-daceae. Arch Microbiol 7: 323–358Google Scholar
  112. van Niel CB (1931) On the morphology and physiology of the purple and green sulfur bacteria. Arch Microbiol 3: 1–112Google Scholar
  113. Varin L, Chamberland H, Lafontaine JG and Richard M (1997) The enzyme involved in sulfation of the turgorin, gallic acid 4-O-(β-D-glucopyranosyl-6′-sulfate) is pulvini-localized in Mimosa pudica. Plant J 12: 831–837PubMedCrossRefGoogle Scholar
  114. Warming E (1875) Om nogle ved Danmarks kyster levede bakterier. Vidensk Medd Dan Naturhist Foren Khobenhavn 20–28: 3–116Google Scholar
  115. Winogradsky SN (1887) Über Schwefelbakterien. Bot Ztg 45: 489–508Google Scholar
  116. Woese CR, Stackebrandt E, Macke TJ and Fox GE (1985) The phylogenetic definition of the major eubacterial taxa. Syst Appl Microbiol 5: 327–336Google Scholar

Copyright information

© Springer Science + Business Media B.V 2008

Authors and Affiliations

  • Christiane Dahl
    • 1
  • Rüdiger Hell
    • 2
  • Thomas Leustek
    • 3
  • David Knaff
    • 4
  1. 1.Institute of Microbiology & BiotechnologyUniversity of BonnGermany
  2. 2.Heidelberg Institute of Plant SciencesUniversity of HeidelbergGermany
  3. 3.Department of Plant Biology and PathologyRutgers UniversityNew BrunswickUSA
  4. 4.Center for Biotechnology and GenomicsTexas Tech UniversityLubbockUSA

Personalised recommendations