Skip to main content

Bacterial Sulfur Globules: Occurrence, Structure and Metabolism

  • Chapter
Inclusions in Prokaryotes

Part of the book series: Microbiology Monographs ((MICROMONO,volume 1))

Abstract

Reduced sulfur compounds such as sulfide, polysulfides, thiosulfate, polythionates, and elemental sulfur are oxidized by a large and diverse group of prokaryotes, including the phototrophic sulfur bacteria, the thiobacilli and other colorless sulfur bacteria and some thermophilic Archaea. Typically, these sulfur compounds are oxidized to sulfate but in many cases globules of polymeric, water-insoluble sulfur accumulate as a transient and sometimes as the final product. While phototrophic bacteria of the families Chlorobiaceae and Ectothiorhodospiraceae, some Rhodospirillaceae and some thiobacilli form extracellular sulfur globules, sulfur is stored intracellularly in purple sulfur bacteria of the family Chromatiaceae, in Beggiatoa species and in the “morphologically conspicuous” sulfur bacteria (e.g., Thioploca, Achromatium, Macromonas, Thiovulum). Our understanding of sulfur globule formation from sulfide, thiosulfate and tetrathionate (the latter occurs in acidophilic thiobacilli) is far from complete and suffers mainly from the uncertainties that exist about the exact chemical nature of the sulfur in the globules, the exact intracellular localization of internal sulfur deposits and the mechanisms to adhere to, attack and take up extracellular sulfur. The only fairly well described enzyme system involved in oxidative decomposition of intracellular sulfur globules is encoded by the 15 dissimilatory sulfite reductase (dsr) genes of the anoxygenic phototrophic purple sulfur bacterium Allochromatium vinosum.

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 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
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

  • Appia-Ayme C, Little PJ, Matsumoto Y, Leech AP, Berks BC (2001) Cytochrome complex essential for photosynthetic oxidation of both thiosulfate and sulfide in Rhodovulum sulfidophilum. J Bacteriol 183:6107–6118

    PubMed  CAS  Google Scholar 

  • Arndt C, Gaill F, Felbeck H (2001) Anaerobic sulfur metabolism in thiotrophic symbioses. J Exp Biol 204:741–750

    PubMed  CAS  Google Scholar 

  • Bartsch RG, Newton GL, Sherrill C, Fahey RC (1996) Glutathione amide and its perthiol in anaerobic sulfur bacteria. J Bacteriol 178:4742–4746

    PubMed  CAS  Google Scholar 

  • Bazylinski DA, Dean AJ, Williams TJ, Long LK, Middleton SL, Dubbels BL (2004) Chemolithoautotrophy in the marine, magnetotactic bacterial strains MV-1 and MV-2. Arch Microbiol 182:373–387

    PubMed  CAS  Google Scholar 

  • Beggiato FS (1838) Memoria delle terme Euganee. Padua

    Google Scholar 

  • Blais JF, Tyagi RD, Meunier N, Auclair JC (1994) The production of extracellular appendages during bacterial colonization of elemental sulphur. Process Biochem 29:475–482

    CAS  Google Scholar 

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

    Google Scholar 

  • Blazejak A, Erséus C, Amann R, Dubilier N (2005) Coexistence of bacterial sulfide oxidizers, sulfate reducers, and spirochetes in a gutless worm (Oligochaeata) from the Peru Margin. Appl Environ Microbiol 71:1553–1561

    PubMed  CAS  Google Scholar 

  • Blöthe M, Fischer U (2000) New insights in sulfur metabolism of purple and green phototrophic sulfur bacteria and their spheroplasts. In: BIOspektrum, special edition, 1st joint congress of the DGHM, ÖGHMP and VAAM: Microbiology 2000, Munich, p 62

    Google Scholar 

  • Bright M, Sorgo A (2003) Ultrastructural reinvestigation of the trophosome in adults of Riftia pachyptila (Annelida, Siboglinidae). Invertebr Biol 122:345–366

    Google Scholar 

  • Brune DC (1989) Sulfur oxidation by phototrophic bacteria. Biochim Biophys Acta 975:189–221

    PubMed  CAS  Google Scholar 

  • Brune DC (1995a) Isolation and characterization of sulfur globule proteins from Chromatium vinosum and Thiocapsa roseopersicina. Arch Microbiol 163:391–399

    PubMed  CAS  Google Scholar 

  • Brune DC (1995b) Sulfur compounds as photosynthetic electron donors. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer, Dordrecht, pp 847–870

    Google Scholar 

  • Brüser T, Lens P, Trüper HG (2000) The biological sulfur cycle. In: Lens P, Hulshoff Pol L (eds) Environmental technologies to treat sulfur pollution. IWA, London, pp 47–86

    Google Scholar 

  • Buck KR, Barry JP, Simpson AGB (2000) Monterey Bay cold seep biota: euglenoza with chemoautotrophic bacterial epibionts. Eur J Protistol 36:117–126

    Google Scholar 

  • Cavanaugh CM (1983) Symbiontic chemoautotrophic bacteria in marine invertebrates from sulfide-rich habitats. Nature 302:58–61

    CAS  Google Scholar 

  • Cavanaugh CM, Gardiner SL, Jones ML, Jannasch HW, Waterbury JB (1981) Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 213:340–342

    CAS  Google Scholar 

  • Cohn F (1865) Zwei neue Beggiatoen. Hedwigia 4:81–84

    Google Scholar 

  • Cohn F (1875) Untersuchungen über Bakterien II. Beitr Biol Pflanz 1:141–207

    Google Scholar 

  • Corsini A (1905) Über die sogenannten Schwefelkörnchen, die man bei der Familie der Beggiatoaceae antrifft. Zentralbl Bakteriol Abt II 14:272–289

    Google Scholar 

  • Dahl C (1999) Deposition and oxidation of polymeric sulfur in prokaryotes. In: Steinbüchel A (ed) Biochemical principles and mechanisms of biosynthesis and biodegradation of polymers. Wiley, Weinheim, pp 27–34

    Google Scholar 

  • Dahl C, Prange A, Steudel R (2002) Natural polymeric sulfur compounds. In: Steinbüchel A (ed) Miscellaneous bioploymers and biodegradation of synthetic polymers, vol 9. Wiley, Weinheim, pp 35–62

    Google Scholar 

  • Dahl C, Engels S, Pott-Sperling AS, Schulte A, Sander J, Lübbe Y, Deuster O, Brune DC (2005) Novel genes of the dsr gene cluster and evidence for close interaction of Dsr proteins during sulfur oxidation in the phototrophic sulfur bacterium Allochromatium vinosum. J Bacteriol 187:1392–1404

    PubMed  CAS  Google Scholar 

  • deBurgh ME, Juniper SK, Singla CL (1989) Bacterial symbiosis in northeast Pacific vestimentifera: a TEM survey. Mar Biol 101:97–105

    Google Scholar 

  • Dick WA (1992) Sulfur cycle. In: Lederberg J (ed) Encyclopedia of microbiology. Academic Press, San Diego, pp 123–133

    Google Scholar 

  • Distel DL (1998) Evolution of chemoautotrophic endosymbioses in bivalves. BioScience 48:277–286

    Google Scholar 

  • Dubilier N, Mülders C, Ferdelman T, de Beer D, Pernthaler A, Klein M, Wagner M, Erséus C, Thiermann F, Krieger J, Giere O, Amann R (2001) Endosymbiontic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm. Nature 411:298–302

    PubMed  CAS  Google Scholar 

  • Duplessis MR, Ziebis W, Gros O, Caro A, Robidart J, Felbeck H (2004) Respiration strategies utilized by the gill endosymbiont from the host lucinid Codakia orbicularis (Bivalvia: Lucinidae). Appl Environ Microbiol 70:4144–4150

    PubMed  CAS  Google Scholar 

  • Dupperon S, Nadalig T, Caprais J-C, Sibuet M, Fiala-Médioni A, Amann R, Dubilier N (2005) Dual symbiosis in a Bathymodiolus sp. mussel from a methane seep on the Gabon continental margin (southeast atlantic): 16S rRNA phylogeny and distribution of the symbionts in gills. Appl Environ Microbiol 71:1694–1700

    Google Scholar 

  • Ehrenberg CG (1838) Die Infusionsthierchen als vollkommene Organismen. Ein Blick in das tiefere organische Leben der Natur. Voss, Leipzig

    Google Scholar 

  • Eisen JA, Nelson KE, Paulsen IT, Heidelberg JF, Wu M, Dodson RJ, Deboy R, Gwinn ML, Nelson WC, Haft DH, Hickey EK, Peterson JD, Durkin AS, Kolonay JL, Yang F, Holt I, Umayam LA, Mason T, Brenner M, Shea TP, Parksey D, Nierman WC, Feldblyum TV, Hansen CL, Craven MB, Radune D, Vamathevan J, Khouri H, White O, Gruber TM, Ketchum KA, Venter JC, Tettelin H, Bryant DA, Fraser CM (2002) The complete genome sequence of Chlorobium tepidum TLS a photosynthetic, anaerobic, greensulfur bacterium. Proc Natl Acad Sci USA 99:9509–9514

    PubMed  CAS  Google Scholar 

  • Falbe J, Regitz M (1995) Römpp Chemie Lexikon, 9th edn. Thieme, Stuttgart

    Google Scholar 

  • Felbeck H (1981) Chemoautotrophic potential of the hydrothermal vent tube worm, Riftia pachyptila Jones (Vestimenifera). Science 213:336–338

    CAS  Google Scholar 

  • Fischer U (1988) Sulfur in biotechnology. In: Rehm HJ, Reed G (eds) Biotechnology, vol 6b. Wiley, Weinheim, pp 463–496

    Google Scholar 

  • Fossing H, Gallardo VA, Jorgensen BB, Hüttel M, Nielsen LP, Schulz HN, Canfield DE, Forster S, Glud RN, Gundersen JK, Küver J, Ramsing NB, Teske A, Thamdrup B, Ulloa O (1995) Concentration and transport of nitrate by the mat-forming sulphur bacterium Thioploca. Nature 374:713–715

    CAS  Google Scholar 

  • Frenkiel L, Gros O, Mouëza M (1996) Gill ultrastructure in Lucina pectinata (Bivalvia: Lucinidae) with reference to hemoglobin in bivalves with symbiotic sulphur-oxidizing bacteria. Mar Biol 125:511–524

    Google Scholar 

  • Friedrich CG (1998) Physiology and genetics of sulfur-oxidizing bacteria. Adv Microb Physiol 39:235–289

    PubMed  CAS  Google Scholar 

  • Friedrich CG, Rother D, Bardischewsky F, Quentmeier A, Fischer J (2001) Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl Environ Microbiol 67:2873–2882

    PubMed  CAS  Google Scholar 

  • Friedrich CG, Bardischewsky F, Rother D, Quentmeier A, Fischer J (2005) Prokaryotic sulfur oxidation. Curr Opin Microbiol 8:253–259

    PubMed  CAS  Google Scholar 

  • George GN, Pickering IJ, Yu EY, Prince RC (2002) X-ray absorption spectroscopy of bacterial sulfur globules. Microbiology 148:2267–2268

    PubMed  CAS  Google Scholar 

  • Gillan DC, Dubilier N (2004) Novel epibiontic Thiothrix bacterium on a marine amphipod. Appl Enivron Microbiol 70:3772–3775

    CAS  Google Scholar 

  • Goffredi SK, Barry JP (2002) Species-specific variation in sulfide physiology between closely related Vesicomyid clams. Mar Ecol Prog Ser 225:227–238

    CAS  Google Scholar 

  • Gray ND, Howarth R, Pickup RW, Jones JG, Head IM (1999) Substrate uptake by uncultured bacteria from the genus Achromatium determined by microautoradiography. Appl Environ Microbiol 65:5100–5106

    PubMed  CAS  Google Scholar 

  • Gray ND, Comaskey D, Miskin IP, Pickup RW, Suzuki K, Head IM (2004) Adaptation of sympatric Achromatium spp. to different redox conditions as a mechanism for coexistence of functionally similar sulphur bacteria. Environ Microbiol 6:669–677

    PubMed  CAS  Google Scholar 

  • Griesbeck C, Schütz M, Schödl T, Bathe S, Nausch L, Mederer N, Vielreicher M, Hauska G (2002) Mechanism of sulfide-quinone oxidoreductase investigated using site-directed mutagenesis and sulfur analysis. Biochemistry 41:11552–11565

    PubMed  CAS  Google Scholar 

  • Guerrero R, Mas J, Pedros-Alio C (1984) Boyant density changes due to intracellular content of sulfur in Chromatium warmingii and Chromatium vinosum. Arch Microbiol 137:350–356

    CAS  Google Scholar 

  • Hageage GJ Jr, Eanes ED, Gherna RL (1970) X-ray diffraction studies of the sulfur globules accumulated by Chromatium species. J Bacteriol 101:464–469

    PubMed  CAS  Google Scholar 

  • Hanson TE, Tabita FR (2003) Insights into the stress response and sulfur metabolism revealed by proteome analysis of a Chlorobium tepidum mutant lacking the Rubisco-like protein. Photosynth Res 231–248

    Google Scholar 

  • Hazeu W, Batenburg-van der Vegte WH, Bos P, van der Pas RK, Kuenen JG (1988) The production and utilization of intermediary elemental sulfur during the oxidation of reduced sulfur compounds by Thiobacillus ferrooxidans. Arch Microbiol 150:574–579

    CAS  Google Scholar 

  • Head IM, Gray ND, Clarke KJ, Pickup RW, Jones JG (1996) The phylogenetic position and ultrastructure of the uncultured bacterium Achromatium oxaliferum. Microbiology 142:2341–2354

    PubMed  CAS  Google Scholar 

  • Hipp WM, Pott AS, Thum-Schmitz N, Faath I, Dahl C, Trüper HG (1997) Towards the phylogeny of APS reductases and sirohaem sulfite reductases in sulfate-reducing and sulfur-oxidizing prokaryotes. Microbiology 143:2891–2902

    PubMed  CAS  Google Scholar 

  • Howarth R, Unz RF, Seviour EM, Seviour RJ, Blackall LL, Pickup RW, Jones JG, Yaguchi J, Head IM (1999) Phylogenetic relationships of filamentous sulfur bacteria (Thiothrix spp. and Eikelboom type 021N bacteria) isolated from wastewater-treatment plants and description of Thiothrix eikelboomii sp nov., Thiothrix unzii sp nov., Thiothrix fructosivorans sp nov and Thiothrix defluvii sp nov. Int J Syst Bacteriol 49:1817–1827

    PubMed  CAS  Google Scholar 

  • Imhoff JF, Süling J, Petri R (1998) Phylogenetic relationships among the Chromatiaceae, their taxonomic reclassification and description of the new genera Allochromatium, Halochromatium, Isochromatium, Marichromatium, Thiococcus, Thiohalocapsa, and Thermochromatium. Int J Syst Bacteriol 48:1129–1143

    PubMed  Google Scholar 

  • Kawaguchi R, Burgess JG, Matsunaga T (1992) Phylogeny and 16s rRNA sequence of Magnetospirillum sp. AMB-1, an aerobic magnetic bacterium. Nucleic Acids Res 20:1140

    PubMed  CAS  Google Scholar 

  • Kelly DP (1989) Physiology and biochemistry of unicellular sulfur bacteria. In: Schlegel HG, Bowien B (eds) Autotrophic bacteria. Science Tech, Madison, pp 193–217

    Google Scholar 

  • Kelly DP, Shergill JK, Lu WP, Wood AP (1997) Oxidative metabolism of inorganic sulfur compounds by bacteria. Antonie van Leeuwenhoek. Int J Gen Mol Microbiol 71:95–107

    CAS  Google Scholar 

  • Kleinjan WE, de Keizer A, Janssen AJH (2003) Biologically produced sulfur. In: Steudel R (ed) Elemental sulfur and sulfur-rich compounds I. Springer, Berlin Heidelberg New York, pp 167–187

    Google Scholar 

  • Kletzin A, Urich T, Müller F, Bandeiras TM, Gomes CM (2004) Dissimilatory oxidation and reduction of elemental sulfur in thermophilic archaea. J Bioenerg Biomembr 77–91

    Google Scholar 

  • Krieger J, Giere O, Dubilier N (2000) Localization of RubisCO and sulfur in endosymbiontic bacteria of the gutless marine oligochaete Inanidrilus leukodermatus (Annelida). Mar Biol 137:239–244

    CAS  Google Scholar 

  • La Riviere JWM, Schmidt K (1999) Morphologically conspicuous sulfur-oxidizing eubacteria. In: Dworkin M (ed) The prokaryotes: an evolving electronic resource for the microbiological community. Springer, Berlin Heidelberg New York. http:// 141.150.157.117:8080/prokPUB/chaprender/jsp/showchap.jsp?chapnum=218&initsec= 01_00

    Google Scholar 

  • Lane DJ, Harrison APJ, Stahl D, Pace B, Giovannoni SJ, Olsen GJ, Pace NR (1992) Evolutionary relationships among sulfur-and iron-oxidizing eubacteria. J Bacteriol 174:269–278

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Lechaire J-P, Frébourg G, Gaill F, Gros O (2006) In situ localization of sulfur in the thioautotrophic symbiontic model Lucina pectinata (Gmelin, 1791) by cryo-EFTEM microanalysis. Biol Cell 98:163–170

    PubMed  CAS  Google Scholar 

  • Maier S, Murray RG (1965) The fine structure of Thioploca ingrica and a comparison with Beggiatoa. Can J Microbiol 11:645–655

    PubMed  CAS  Google Scholar 

  • Maina JN, Maloyi GMO (1998) Adaptations of a tropical swamp worm, Alma emini, for subsistence in a H2S-rich habitat: evolution of endosymbiotnic bacteria, sulfide metabolizing bodies, and novel processes of elemination of neutralized sulfide complexes. J Struct Biol 122:257–266

    PubMed  CAS  Google Scholar 

  • Mas J, van Gemerden H (1987) Influence of sulfur accumulation and composition of sulfur globule on cell volume and bouyant density of Chromatium vinosum. Arch Microbiol 146:362–369

    CAS  Google Scholar 

  • Mas J, van Gemerden H (1995) Storage products in purple and green sulfur bacteria. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer, Dordrecht, pp 973–990

    Google Scholar 

  • Mas J, Pedros-Alio C, Guerrero R (1985) Mathematical model for determining the effects of intracytoplasmic inclusions on volume and density of microorganisms. J Bacteriol 164:749–756

    PubMed  CAS  Google Scholar 

  • Middelburg JJ (2000) The geochemical sulfur cycle. In: Lens P, Hulshoff Pol L (eds) Environmental technologies to treat sulfur pollution. IWA, London, pp 33–46

    Google Scholar 

  • Müller A, Krebs B (1984) Sulfur—its significance for chemistry, for the geo-, bio-and cosmosphere and technology. Elsevier, Amsterdam

    Google Scholar 

  • Müller C (1870) Chemisch-physikalische Beschreibung der Thermen von Baden in der Schweiz (Canton Aargau). Zehnder, Baden

    Google Scholar 

  • Müller OF (1786) Animacula infusoria fluviatilia et marina, quae detexit, systematice descripsit et ad vivum delineari curavit. Mölleri, Hauniae

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Nelson DC, Fisher CR (1995) Chemoautotrophic and methanoautotrophic endosymbiontic bacteria at deep-sea vents and seeps. In: Karl DM (ed) Deep-sea hydrothermal vents. CRC, Boca Raton, pp 125–167

    Google Scholar 

  • Nelson DC, Hagen KD (1995) Physiology and biochemistry of symbiotic and free-living chemoautotrophic sulfur bacteria. Am Zool 35:91–101

    CAS  Google Scholar 

  • Nickless G (1968) Inorganic sulphur chemistry. Elsevier, Amsterdam

    Google Scholar 

  • Nicolson GL, Schmidt GL (1971) Structure of the Chromatium sulfur particle and its protein membrane. J Bacteriol 105:1142–1148

    PubMed  CAS  Google Scholar 

  • Odintsova EV, Wood AP, Kelly DP (1993) Chemolithoautotrophic growth of Thiotrix ramosa. Arch Microbiol 160:152–157

    CAS  Google Scholar 

  • Odintsova EV, Jannasch H, Mamone JA, Langworthy TA (1996) Thermothrix azorensis sp. nov., an obligately chemolithoautotrophic, sulfur-oxidizing, thermophilic bacterium. Int J Syst Bacteriol 46:422–428

    PubMed  CAS  Google Scholar 

  • Ohmura N, Tsugita K, Koizumi J, Saiki H (1996) Sulfur-binding protein of flagella of Thiobacillus ferrooxidans. J Bacteriol 178:5776–5780

    PubMed  CAS  Google Scholar 

  • Otte S, Kuenen JG, Nielsen LP, Pearl HW, Zopfi J, Schulz HN, Teske A, Strotmann B, Gallardo VA, Jørgensen BB (1999) Nitrogen, carbon, and sulfur metabolism in natural Thioploca samples. Appl Environ Microbiol 65:3148–3157

    PubMed  CAS  Google Scholar 

  • Overmann J (1997) Mahoney Lake: A case study of the ecological significance of phototrophic sulfur bacteria. Adv Microb Ecol 15:251–288

    CAS  Google Scholar 

  • Pasteris JD, Freeman JJ, Goffredi SK, Buck KR (2001) Raman spectroscopic and laser confocal microscopic analysis of sulfur in living sulfur-precipitating marine bacteria. Chem Geol 180:3–18

    CAS  Google Scholar 

  • Pattaragulwanit K, Dahl C (1995) Development of a genetic system for a purple sulfur bacterium: conjugative plasmid transfer in Chromatium vinosum. Arch Microbiol 164:217–222

    CAS  Google Scholar 

  • Pattaragulwanit K, Brune DC, Trüper HG, Dahl C (1998) Molecular genetic evidence for extracytoplasmic localization of sulfur globules in Chromatium vinosum. Arch Microbiol 169:434–444

    PubMed  CAS  Google Scholar 

  • Perty M (1852) Zur Kenntnis kleinster Lebensformen nach Bau, Funktionen, Systematik, mit Spezialverzeichnis der in der Schweiz beobachteten. Jent and Reinert, Bern

    Google Scholar 

  • Pfennig N, Trüper HG (1992) The family Chromatiaceae. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H (eds) The Prokaryotes. A handbook on the biology of bacteria: ecophysiology, isolation, identification, applications. Springer, Berlin Heidelberg New York, pp 3200–3221

    Google Scholar 

  • Pibernat IV, Abella CA (1996) Sulfide pulsing as the controlling factor of spinae production in Chlorobium limicola strain UdG 6038. Arch Microbiol 165:272–278

    PubMed  CAS  Google Scholar 

  • Pickering IJ, George GN, Yu EY, Brune DC, Tuschak C, Overmann J, Beatty JT, Prince RC (2001) Analysis of sulfur biochemistry of sulfur bacteria using X-ray absorption spectroscopy. Biochemistry 40:8138–8145

    PubMed  CAS  Google Scholar 

  • Polz MF, Distel DL, Zarda B, Amann R, Felbeck H, Ott JA, Cavanaugh CM (1994) Phylogenetic analysis of a highly specific association between ectosymbiotic, sulfur-oxidizing bacteria and a marine nematode. Appl Environ Microbiol 60:4461–4467

    PubMed  CAS  Google Scholar 

  • Postgate JR (1968) The sulphur cycle. In: Nickless G (ed) Inorganic sulphur chemistry. Elsevier, Amsterdam, pp 259–279

    Google Scholar 

  • Pott AS, Dahl C (1998) Sirohaem-sulfite reductase and other proteins encoded in the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur. Microbiology 144:1881–1894

    PubMed  CAS  Google Scholar 

  • Prange A (2001) Molekulargenetische und physikalisch-chemische Untersuchungen an den Schwefelkugeln photo-und chemotropher Schwefelbakterien. PhD thesis, University of Bonn

    Google Scholar 

  • Prange A, Modrow H (2002) X-ray absorption spectroscopy and its application in biological, agricultural and environmental research. Rev Environ Sci Biotechnol 1:259–276

    CAS  Google Scholar 

  • Prange A, Arzberger I, Engemann C, Modrow H, Schumann O, Trüper HG, Steudel R, Dahl C, Hormes J (1999) In situ analysis of sulfur in the sulfur globules of phototrophic sulfur bacteria by X-ray absorption near edge spectroscopy. Biochim Biophys Acta 1428:446–454

    PubMed  CAS  Google Scholar 

  • Prange A, Chauvistré R, Modrow H, Hormes J, Trüper HG, Dahl C (2002a) Quantitative speciation of sulfur in bacterial sulfur globules: X-ray absorption spectroscopy reveals at least three different speciations of sulfur. Microbiology 148:267–276

    PubMed  CAS  Google Scholar 

  • Prange A, Dahl C, Trüper HG, Behnke M, Hahn J, Modrow H, Hormes J (2002b) Investigation of S — H bonds in biologically important compounds by sulfur K-edge X-ray absorption spectroscopy. Eur Phys J D 20:589–596

    CAS  Google Scholar 

  • Prange A, Dahl C, Trüper HG, Chauvistré R, Modrow H, Hormes J (2002c) X-ray absorption spectroscopy of bacterial sulfur globules: a detailed reply. Microbiology 148:2268–2270

    CAS  Google Scholar 

  • Prange A, Engelhardt H, Trüper HG, Dahl C (2004) The role of the sulfur globule proteins of Allochromatium vinosum: mutagenesis of the sulfur globule protein genes and expression studies by Real-time RT PCR. Arch Microbiol 182:165–174

    PubMed  CAS  Google Scholar 

  • Pronk JT, Meulenberg R, Hazeu W, Bos P, Kuenen JG (1990) Oxidation of reduced inorganic sulphur compounds by acidophilic thiobacilli. FEMS Microbiol Rev 75:293–306

    CAS  Google Scholar 

  • Reinartz M, Tschäpe J, Brüser T, Trüper HG, Dahl C (1998) Sulfide oxidation in the phototrophic sulfur bacterium Chromatium vinosum. Arch Microbiol 170:59–68

    PubMed  CAS  Google Scholar 

  • Remsen CC (1978) Comparative subcellular architecture of photosynthetic bacteria. In: Clayton RK, Sistrom WR (eds) The photosynthetic bacteria. Plenum, New York, pp 31–62

    Google Scholar 

  • Remsen CC, Trüper HG (1973) The fine structure of Chromatium buderi. Arch Mikrobiol 90:269–280

    PubMed  CAS  Google Scholar 

  • Robertson LA, Kuenen GJ (1999) The colorless sulfur bacteria. In: Dworkin M (ed) The prokaryotes: an evolving electronic resource for the microbiological community. Springer, Berlin Heidelberg New York. http://141.150.157.117:8080/prokPUB/chapren der/jsp/showchap.jsp?chapnum=016&initsec=01_00

    Google Scholar 

  • Roy AB, Trudinger PA (1970) The biochemistry of inorganic compounds of sulfur. Cambridge University Press, London

    Google Scholar 

  • Schedel M, Trüper HG (1980) Anaerobic oxidation of thiosulfate and elemental sulfur in Thiobacillus denitrificans. Arch Microbiol 124:205–210

    CAS  Google Scholar 

  • Schmidt GL, Nicolson GL, Kamen MD (1971) Composition of the sulfur particle of Chromatium vinosum. J Bacteriol 105:1137–1141

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Schmidt TM, Vinci VA, Strohl WR (1986) Protein synthesis by Beggiatoa alba B18LD in the presence and absence of sulfide. Arch Microbiol 144:158–162

    CAS  Google Scholar 

  • Schulz HN, Jørgensen BB (2001) Big bacteria. Annu Rev Microbiol 55:105–137

    PubMed  CAS  Google Scholar 

  • Schulz HN, Brinkhoff T, Ferdelman TG, Hernández Mariné M, Teske A, Jørgensen BB (1999) Dense populations of a giant sulfur bacterium in Namibian shelf sediments. Science 284:493–495

    PubMed  CAS  Google Scholar 

  • Shively JM, Bryant DA, Fuller RC, Konopka AE, Stevens SE Jr, Strohl WR (1989) Functional inclusions in prokaryotic cells. Int Rev Cytol 113:35–100

    Google Scholar 

  • Sorokin DY, Lysenko AM, Mityushina LL, Tourova TP, Jones BE, Rainey FA, Robertson LA, Kuenen GJ (2001) Thioalkalimicrobium aerophilum gen. nov., sp. nov. and Thioalkalimicrobium sibericum sp. nov., and Thioalkalivibrio versutus gen. nov., sp. nov., Thioalkalivibrio nitratis sp. nov. and Thioalkalivibrio denitrificans sp. nov., novel obligately alkaliphilic and obligately chemolithoautotrophic sulfur-oxidizing bacteria from soda lakes. Int J Syst Evol Microbiol 51:565–580

    PubMed  CAS  Google Scholar 

  • Spring S, Bazylinski DA (2000) Magnetotactic bacteria. In: Dworkin M (ed) The prokaryotes: an evolving electronic resource for the microbiological community. Springer, Berlin Heidelberg New York. http://141.150.157.117:8080/prokPUB/chaprender/jsp/showchap.jsp?chapnum=281&initsec=01_00

    Google Scholar 

  • Steudel R (1982) Homocyclic sulfur molecules. Top Curr Chem 102:149–176

    CAS  Google Scholar 

  • Steudel R (1985) Neue Entwicklungen in der Chemie des Schwefels und des Selens. Nova Acta Leopold 264:231–246

    Google Scholar 

  • Steudel R (1987) Sulfur homocycles. In: Haiduc I, Sowerby DB (eds) The chemistry of inorganic homo-and heterocycles. Academic, London, pp 737–768

    Google Scholar 

  • Steudel R (1989) On the nature of the “elemental sulfur” (S0) produced by sulfur-oxidizing bacteria—a model for S0 globules. In: Schlegel HG, Bowien B (eds) Autotrophic bacteria. Science Tech, Madison, pp 289–303

    Google Scholar 

  • Steudel R (1996a) Das gelbe Element und seine erstaunliche Vielseitigkeit. Chem Unserer Zeit 30:226–234

    CAS  Google Scholar 

  • Steudel R (1996b) Mechanism for the formation of elemental sulfur from aqueous sulfide in chemical and microbiological desulfurization processes. Ind Eng Chem Res 35:1417–1423

    CAS  Google Scholar 

  • Steudel R (1998) Chemie der Nichtmetalle, 2 edn. W. de Gruyter, Berlin

    Google Scholar 

  • Steudel R (2000) The chemical sulfur cycle. In: Lens P, Hulshoff Pol L (eds) Environmental technologies to treat sulfur pollution. IWA, London, pp 1–31

    Google Scholar 

  • Steudel R (2003a) Aqueous sulfur sols. In: Steudel R (ed) Elemental sulfur and sulfur-rich compounds I. Springer, Berlin Heidelberg New York, pp 153–166

    Google Scholar 

  • Steudel R (2003b) Elemental sulfur and sulfur-rich compounds I. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Steudel R (2003c) Elemental sulfur and sulfur-rich compounds II. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Steudel R, 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. Wiley, Weinheim, pp 17–26

    Google Scholar 

  • Steudel R, Eckert B (2003) Solid sulfur allotropes. In: Steudel R (ed) Elemental sulfur and sulfur-rich compounds. Springer, Berlin Heidelberg New York, pp 1–79

    Google Scholar 

  • Steudel R, 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 43:581–589

    CAS  Google Scholar 

  • Steudel R, Kustos M (1994) Organic polysulfanes. In: King RB (ed) Encyclopedia of inorganic chemistry. Wiley, Chichester, pp 4009–4038

    Google Scholar 

  • Steudel R, Holdt G, Nagorka R (1986) On the autoxidation of aqueous sodium polysulfide. Z Naturforsch 41b:1519–1522

    CAS  Google Scholar 

  • Steudel R, Göbel T, Holdt G (1987a) The molecular composition of hydrophilic sulfur sols prepared by acid decomposition of thiosulfate. Z Naturforsch 43b:203–218

    Google Scholar 

  • Steudel R, Holdt G, Göbel T, Hazeu W (1987b) Chromatographic separation of higher polythionates SnO2−6 (n = 3...22) and their detection in cultures of Thiobacillus ferrooxidans; molecular composition of bacterial sulfur secretions. Angew Chem Int Ed Engl 26:151–153

    Google Scholar 

  • Steudel R, Holdt G, Visscher PT, van Gemerden H (1990) Search for polythionates in cultures of Chromatium vinosum after sulfide incubation. Arch Microbiol 155:432–437

    Google Scholar 

  • Strohl WR, Geffers I, Larkin JM (1981) Structure of the sulfur inclusion envelopes from four Beggiatoas. Curr Microbiol 6:75–79

    Google Scholar 

  • Strohl WR, Howard KS, Larkin JM (1982) Ultrastructure of Beggiatoa alba strain B15LD. J Gen Microbiol 128:73–84

    Google Scholar 

  • Takakuwa S (1992) Biochemical aspects of microbial oxidation of inorganic sulfur compounds In: Oae S, Okuyama T (eds) Organic sulfur chemistry: biochemical aspects. CRC, Boca Raton, pp 1–43

    Google Scholar 

  • Teske A, Nelson DC (2004) The genera Beggiatoa and Thioploca. In: Dworkin M (ed) The prokaryotes: An evolving electronic resource for the microbiological community. Springer, Berlin Heidelberg New York. http://141.150.157.117:8080/prokPUB/chaprender/jsp/showchap.jsp?chapnum=432&initsec=01_00

    Google Scholar 

  • Teske AP, Ramsing NB, Kuever J, Fossing H (1995) Phylogeny of Thioploca and related filamentous sulfide-oxidizing bacteria. Syst Appl Microbiol 18:517–526

    Google Scholar 

  • Then J (1984) Beiträge zur Sulfidoxidation durch Ectothiorhodospira abdelmalekii und Ectothiorhodospira halochloris. PhD thesis, University of Bonn

    Google Scholar 

  • Then J, Trüper HG (1983) Sulfide oxidation in Ectothiorhodospira abdelmalekii. Evidence for the catalytic role of cytochrome c-551. Arch Microbiol 135:254–258

    CAS  Google Scholar 

  • Then J, Trüper HG (1984) Utilization of sulfide and elemental sulfur by Ectothiorhodospira halochloris. Arch Microbiol 139:295–298

    CAS  Google Scholar 

  • Trevisan V (1842) Prospetto della Flora Euganea. In: Coi Tipi del Seminario, Padua, pp 1–68

    Google Scholar 

  • Trüper HG (1978) Sulfur metabolism. In: Clayton RK, Sistrom WR (eds) The photosynthetic bacteria. Plenum, New York, pp 677–690

    Google Scholar 

  • Trüper HG (1984) Microorganisms and the sulfur cycle. In: Müller A, Krebs B (eds) Sulfur, its significance for chemistry, for the geo-, bio-, and cosmosphere and technology. Elsevier, Amsterdam, pp 351–365

    Google Scholar 

  • Trüper HG, Hathaway JC (1967) Orthorombic sulfur formed by photosynthetic sulphur bacteria. Nature 215:435–436

    PubMed  Google Scholar 

  • van Gemerden H (1968) On the ATP generation by Chromatium in the dark. Arch Mikrobiol 64:118–124

    PubMed  Google Scholar 

  • van Niel BC (1936) On the metabolism of the Thiorhodaceae. Arch Mikrobiol 7:323–358

    Google Scholar 

  • van Niel CB (1931) On the morphology and physiology of the purple and green sulfur bacteria. Arch Mikrobiol 3:1–112

    Google Scholar 

  • Verte F, Kostanjevecki V, de Smet L, Meyer TE, Cusanovich MA, van Beeumen JJ (2002) Identification of a thiosulfate utilization gene cluster from the green phototrophic bacterium Chlorobium limicola. Biochemistry 41:2932–2945

    PubMed  CAS  Google Scholar 

  • Vetter RD (1985) Elemental sulfur in the gills of three species of clams containing chemoautotrophic symbiontic bacteria: a possible inorganic energy storage compound. Mar Biol 88:33–42

    CAS  Google Scholar 

  • Visser JM, de Jong GAH, Robertson LA, Kuenen JG (1997) A novel membrane-bound flavocytochrome c sulfide dehydrogenase from the colourless sulfur bacterium Thiobacillus sp. W5. Arch Microbiol 167:295–301

    PubMed  CAS  Google Scholar 

  • Warming E (1875) Om nogle ved Danmarks kyster levede bakterier. Vidensk Medd Dan Naturhist Foren Khobenhavn 20–28:3–116

    Google Scholar 

  • Williams TM, Unz RF, Doman T (1987) Ultrastructure of Thiothrix and “Type 012N” bacteria. Appl Enivron Microbiol 53:1560–1570

    Google Scholar 

  • Winogradsky SN (1887) Über Schwefelbakterien. Bot Ztg 45:489–508

    Google Scholar 

  • Winogradsky SN (1889) Recherches physiologiques sur le sulfobactéries. Ann Inst Pasteur 3:49–60

    Google Scholar 

  • Wirsen CO, Jannasch HW (1978) Physiological and morphological observations on Thiovulum sp. J Bacteriol 136:765–774

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Additional information

Dedicated to our esteemed academic teacher Prof. Dr. rer. nat. Dr. phil. Dr. rer. nat. h.c. Hans G. Trüper, Bonn, on the occasion of his 70th birthday on March 16th, 2006, for his fundamental work on microbial sulfur metabolism and encouraging support of his students.

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Dahl, C., Prange, A. (2006). Bacterial Sulfur Globules: Occurrence, Structure and Metabolism. In: Shively, J.M. (eds) Inclusions in Prokaryotes. Microbiology Monographs, vol 1. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-33774-1_2

Download citation

Publish with us

Policies and ethics