Inorganic Sulfur Compounds as Electron Donors in Purple Sulfur Bacteria

  • Christiane Dahl
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 27)

Most anoxygenic phototrophic bacteria can use inorganic sulfur compounds (e.g. sulfide, elemental sulfur, polysulfides, thiosulfate, or sulfide) as electron donors for reductive carbon dioxide fixation during photolithoautotrophic growth. In these organisms, light energy is used to transfer electrons from sulfur compounds to the level of the more highly reducing electron carriers NAD(P)+ and ferredoxin. In this chapter the sulfur oxidizing capabilities of the different groups of anoxygenic phototrophic bacteria are briefly summarized. This chapter then focuses on the pathways of sulfur compound oxidation in purple sulfur bacteria of the families Chromatiaceae and Ectothiorhodospiraceae. A variety of enzymes catalyzing sulfur oxidation reactions have been isolated from members of this group and Allochromatium vinosum, a representative of the Chromatiaceae, has been especially well characterized also on a molecular genetic level. In this organism intracellular sulfur globules are an obligate intermediate during the oxidation of thiosulfate and sulfide to sulfate. Thiosulfate oxidation is strictly dependent on the presence of three periplasmic Sox proteins encoded by the soxBXA and soxYZ genes. Sulfide oxidation does not appear to require the presence of Sox proteins. Flavocytochrome c is also not essential leaving sulfide:quinone oxidoreductase as the probably most important sulfide-oxidizing enzyme. Polysulfides are intermediates en route of sulfide to stored sulfur. Sulfur is deposited in the periplasm and present as long chains probably terminated by organic residues at one or both ends. The oxidation of stored sulfur is completely dependent on the proteins encoded in the dsr operon. These include siroamide-containing sulfite reductase (DsrAB), a transmembrane electrontransporting complex (DsrMKJOP) and a iron–sulfur flavoprotein with NADH:acceptor oxidoreductase activity (DsrL). The last step of reduced sulfur compound oxidation in purple sulfur bacteria is the oxidation of sulfite. This can occur either via the enzymes adenosine 5'-phosphosulfate (APS) reductase and ATP sulfurylase which are non-essential in Alc. vinsoum or via direct oxidation to sulfate. The nature of the enzyme catalyzing the latter step is still unresolved in purple sulfur bacteria.

Keywords

Glutathione Photosynthesis Carotenoid Desulfurization Rotenone 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Altschul SF, Gish W, Miller W, Myers EW and Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410PubMedGoogle Scholar
  2. Appia-Ayme C, Little PJ, Matsumoto Y, Leech AP and Berks BC (2001) Cytochrome complex essential for photosynthetic oxidation of both thiosulfate and sulfide in Rhodovulum sulfidophilum. J Bacteriol 183: 6107–6118PubMedCrossRefGoogle Scholar
  3. Arieli B, Shahak Y, Taglicht D, Hauska G and Padan E (1994) Purification and characterization of sulfide-quinone reductase, a novel enzyme driving anoxygenic photosynthesis in Oscillatoria limnetica. J Biol Chem 269: 5705–5711PubMedGoogle Scholar
  4. Arunasri K, Sasikala C, Ramana CV, Sűling J and Imhoff JF (2005) Marichromatium indicum sp. nov., a novel purple sulfur gammaproteobacterium from mangrove soil of Goa, India. Int J Syst Evol Microbiol 55: 673–679PubMedCrossRefGoogle Scholar
  5. Bardischewsky F, Quentmeier A and Friedrich CG (2006) The flavoprotein SoxF functions in chemotrophic thiosulfate oxidation of Paracoccus pantotrophus in vivo and in vitro. FEMS Microbiol Lett 258: 121–126PubMedCrossRefGoogle Scholar
  6. Bartsch RG (1978) Cytochromes. In: Clayton RK and Sistrom WR (eds) The Photosynthetic Bacteria, pp 249–279. Plenum, New YorkGoogle Scholar
  7. Bartsch RG, Newton GL, Sherrill C and Fahey RC (1996) Glutathione amide and its perthiol in anaerobic sulfur bacteria. J Bacteriol 178: 4742–4746PubMedGoogle Scholar
  8. Beynon JD, MacRae IJ, Huston SL, Nelson DC, Segel IH and Fisher AJ (2001) Crystal structure of ATP sulfurylase from the bacterial symbiont of the hydrothermal vent tubeworm Riftia pachyptila. Biochemistry 40: 14509–14517PubMedCrossRefGoogle Scholar
  9. 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
  10. Blöthe, M and Fischer, U (2000) New insights in sulfur metabolism of purple and green phototrophic sulfur bacteria and their spheroplasts. BIOspektrum, Special edition 1st Joint Congress of DGHM, ÖGHMP and VAAM: “Microbiology 2000”, Munidi, p. 62Google Scholar
  11. Brune DC (1989) Sulfur oxidation by phototrophic bacteria. Biochim Biophys Acta 975: 189–221PubMedCrossRefGoogle Scholar
  12. Brune DC (1995a) Isolation and characterization of sulfur globule proteins from Chromatium vinosum and Thiocapsa roseopersicina. Arch Microbiol 163: 391–399PubMedCrossRefGoogle Scholar
  13. Brune DC (1995b) Sulfur compounds as photosynthetic electron donors. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 847–870, Vol 2 of Advances in Photosnythesis (Govindjee ed.). Kluwer Academic Publishers (now Springer), DordrechtCrossRefGoogle Scholar
  14. Brune DC and Trüper HG (1986) Noncyclic electron transport in chromatophores from photolithoautotrophically grown Rhodobacter sulfidophilus. Arch Microbiol 145: 295–301CrossRefGoogle Scholar
  15. Brüser T, Selmer T and Dahl C (2000) “ADP sulfurylase” from Thiobacillus denitrificans is an adenylylsulfate:phosphate adenylyltransferase and belongs to a new family of nucleotidyltransferases. J Biol Chem 275: 1691–1698PubMedCrossRefGoogle Scholar
  16. Brüser T, Trüper HG and Dahl C (1997) Cloning and sequencing of the gene encoding the high potential iron–sulfur protein (HiPIP) from the purple sulfur bacterium Chromatium vinosum. Biochim Biophys Acta 1352: 18–22PubMedGoogle Scholar
  17. Bryantseva IA, Gorlenko VM, Kompantseva EI, Imhoff JF, Süling J and Mityushina L (1999) Thiorhodospira sibirica gen. nov., sp. nov., a new alkaliphilic purple sulfur bacterium from a Siberian Soda lake. Int J Syst Bacteriol 49: 697–703PubMedCrossRefGoogle Scholar
  18. 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
  19. Dahl C (1996) Insertional gene inactivation in a phototrophic sulphur bacterium: APS-reductase-deficient mutants of Chromatium vinosum. Microbiology 142: 3363–3372PubMedCrossRefGoogle Scholar
  20. 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, pp 27–34. Wiley, WeinheimGoogle Scholar
  21. 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
  22. Dahl C and Trüper HG (1989) Comparative enzymology of sulfite oxidation in Thiocapsa roseopersicina strains 6311, M1 and BBS under chemotrophic and phototrophic conditions. Z Naturforsch 44c: 617–622Google Scholar
  23. Dahl C, Engels S, Pott-Sperling AS, Schulte A, Sander J, Lübbe Y, Deuster O and 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: 1392–1404PubMedCrossRefGoogle Scholar
  24. Davidson MW, Gray GO and Knaff DB (1985) Interaction of Chromatium vinosum flavocytochrome c-552 with cytochromes c studied by affinity chromatography. FEBS Lett 187: 155–159CrossRefGoogle Scholar
  25. de Jong GAH, Hazeu W, Bos P and Kuenen JG (1997) Isolation of the tetrathionate hydrolase from Thiobacillus acidophilus. Eur J Biochem 243: 678–683PubMedCrossRefGoogle Scholar
  26. de Jong GAH, Tang JA, Bos P, de Vries S and Kuenen GJ (2000) Purification and characterization of a sulfite:cytochrome c oxidoreductase from Thiobacillus acidophilus. J Mol Catal B 8: 61–67CrossRefGoogle Scholar
  27. Dolata MM, van Beeumen JJ, Ambler RP, Meyer TE and Cusanovich MA (1993) Nucleotide sequence of the heme subunit of flavocytochrome c from the purple phototrophic bacterium, Chromatium vinosum. A 2.6-kilobase pair DNA fragment contains two multiheme cytochromes, a flavoprotein, and a homolog of human ankyrin. J Biol Chem 268: 14426–14431PubMedGoogle Scholar
  28. Doonan CJ, Kappler U and George GN (2006) Structure of the active site of sulfite dehydrogenase from Starkeya novella. Inorg Chem 45: 7488–7492PubMedCrossRefGoogle Scholar
  29. Drepper F and Mathis P (1997) Structure and function of cytochrome c(2) in electron transfer complexes with the photosynthetic reaction center of Rhodobacter sphaeroides: Optical linear dichroism and EPR. Biochemistry 36: 1428–1440PubMedCrossRefGoogle Scholar
  30. Feng C, Kappler U, Tollin G and Enemark JH (2003) Intramolecular electron transfer in a bacterial sulfite dehydrogenase. J Am Chem Soc 125: 14696–14697PubMedCrossRefGoogle Scholar
  31. Fischer U (1984) Cytochromes and iron sulfur proteins in sulfur metabolism of phototrophic sulfur bacteria. In: Müller A and Krebs B (eds) Sulfur, Its Significance for Chemistry, for the Geo-, Bio- and Cosmosphere and Technology, pp 383–407. Elsevier Science, AmsterdamGoogle Scholar
  32. Franz B, Lichtenberg H, Hormes J, Modrow H, Dahl C and Prange A (2006) Utilization of solid “elemental” sulfur by the phototrophic purple sulfur bacterium Allochromatium vinosum: a sulfur K-edge XANES spectroscopy study. Microbiology 153: 1268–1274CrossRefGoogle Scholar
  33. 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
  34. Frigaard NU and Bryant DA (2008) Genomic insights into the sulfur metabolism of phototrophic green sulfur bacteria. In: Hell R, Dahl C, Knaff DB and Leustek T (eds), Sulfur Metabolism in Phototrophic Organisms, (Advances in Photosynthesis and Respiration, Vol 27), pp 337–355. Springer, New YorkCrossRefGoogle Scholar
  35. Fritz G, Buchert T, Huber H, Stetter KO and Kroneck PMH (2000) Adenylylsulfate reductases from archaea and bacteria are 1: 1 alpha beta-heterodimeric iron–sulfur flavoenzymes – high similarity of molecular properties emphasizes their central role in sulfur metabolism. FEBS Lett 473: 63–66PubMedCrossRefGoogle Scholar
  36. Fukumori Y and Yamanaka T (1979) A high-potential nonheme iron protein (HiPIP)-linked, thiosulfate-oxidizing enzyme derived from Chromatium vinosum. Curr Microbiol 3: 117–120CrossRefGoogle Scholar
  37. Garrity GM and Holt G (2001) Chlorobi phy. nov. In: Boone, DR, Castenholz, RW and Garrity GM (eds) Bergey’s Manual of Systematic Bacteriology, Vol 1, pp 601–623. Springer, New YorkGoogle Scholar
  38. Gavel OY, Bursakov SA, Calvete JJ, George GN, Moura JJG and Moura I (1998) ATP sulfurylases from sulfate-reducing bacteria of the genus Desulfovibrio. A novel metalloprotein containing cobalt and zinc. Biochemistry 37: 16225–16232PubMedCrossRefGoogle Scholar
  39. Gehrke T, Telegdi J, Thierry D and Sand W (1998) Importance of extracellular polymeric substances from Thiobacillus ferrooxidans for bioleaching. Appl Environ Microbiol 64: 2743–2747PubMedGoogle Scholar
  40. George, GN, Pickering, IJ, Yu, EY and Prince, RC (2002) X-ray absorption spectroscopy of bacterial sulfur globules. Microbiology 148: 2267–2268PubMedGoogle Scholar
  41. Gorlenko VM, Bryantseva IA, Panteleeva EE, Tourova TP, Kolganova TV, Makhneva ZK and Moskalenko AA (2004) Ectothiorhodosinus mongolicum gen. nov., sp. nov., a new purple bacterium from a soda lake in Mongolia. Microbiology 73: 66–73CrossRefGoogle Scholar
  42. Griesbeck C, Schütz M, Schödl T, Bathe S, Nausch L, Mederer N, Vielreicher M and Hauska G (2002) Mechanism of sulfide-quinone oxidoreductase investigated using site-directed mutagenesis and sulfur analysis. Biochemistry 41: 11552–11565PubMedCrossRefGoogle Scholar
  43. Hageage GJ, Jr., Eanes ED and Gherna RL (1970) X-ray diffraction studies of the sulfur globules accumulated by Chromatium species. J Bacteriol 101: 464–469PubMedGoogle Scholar
  44. Hagen KD and Nelson DC (1997) Use of reduced sulfur compounds by Beggiatoa spp.: Enzymology and physiology of marine and freshwater strains in homogeneous and gradient cultures. Appl Environ Microbiol 63: 3957–3964PubMedGoogle Scholar
  45. Hanada S and Pierson BK (2002) The family Chloroflexaceae. In: Dworkin M (ed) The Prokaryotes: an Evolving Electronic Resource for the Microbiological Community, http://link.springer-ny.com/link/service/books/10125/. Springer, Berlin, Heidelberg, New York
  46. Hensen D, Sperling D, Trüper HG, Brune DC and Dahl C (2006) Thiosulfate oxidation in the phototrophic sulfur bacterium Allochromatium vinosum. Mol Microbiol 62: 794–810PubMedCrossRefGoogle Scholar
  47. Hille R (1996) The mononuclear molybdenum enzymes. Chem Rev 96: 2757–2816PubMedCrossRefGoogle Scholar
  48. Hipp WM, Pott AS, Thum-Schmitz N, Faath I, Dahl C and Trüper HG (1997) Towards the phylogeny of APS reductases and sirohaem sulfite reductases in sulfate-reducing and sulfur-oxidizing prokaryotes. Microbiology 143: 2891–2902PubMedCrossRefGoogle Scholar
  49. Hiraishi A and Shimada K (2001) Aerobic anoxygenic photosynthetic bacteria with zinc-bacteriochlorophyll. J Gen Appl Microbiol 47: 161–180PubMedCrossRefGoogle Scholar
  50. Hiraishi A, Nagashima KVP, Matsuura K, Shimada K, Takaichi S, Wakao N and Katayama Y (1998) Phylogeny and photosynthetic features of Thiobacillus acidophilus and related acidophilic bacteria: its transfer to the genus Acidiphilium as Acidiphilium acidophilum comb. nov. Int J Syst Bacteriol 48: 1389–1398PubMedCrossRefGoogle Scholar
  51. Hirschler-Rea A, Matheron R, Riffaud C, Moune S, Eatock C, Herbert RA, Willison JC and Caumette P (2003) Isolation and characterization of spirilloid purple phototrophic bacteria forming red layers in microbial mats of Mediterranean salterns: description of Halorhodospira neutriphila sp. nov. and emendation of the genus Halorhodospira. Int J Syst Evol Microbiol 53: 153–163PubMedCrossRefGoogle Scholar
  52. Ikeuchi Y, Shigi N, Kato J, Nishimura A and Suzuki T (2006) Mechanistic insights into sulfur relay by multiple sulfur mediators involved in thiouridine biosynthesis at tRNA wobble positions. Mol Cell 21: 97–108PubMedCrossRefGoogle Scholar
  53. Imhoff JF (2003) Phylogenetic taxonomy of the family Chlorobiaceae on the basis of 16S rRNA and fmo (Fenna–Matthews–Olson protein) gene sequences. Int J Syst Evol Microbiol 53: 941–951PubMedCrossRefGoogle Scholar
  54. Imhoff JF (2005a) Family I. Chromatiaceae Bavendamm 1924, 125AL emend. Imhoff 1984b, 339. In: Brenner, DJ, Krieg NR, Staley JT and Garrity GM (eds) Bergey’s Manual of Systematic Bacteriology, Vol 2, part B, pp 3–40. Springer, New YorkGoogle Scholar
  55. Imhoff JF (2005b) Family II. Ectothiorhodospiraceae Imhoff 1984b, 339VP. In: Brenner DJ, Krieg NR, Staley JT and Garrity GM (eds) Bergey’s Manual of Systematic Bacteriology, Vol 2, Part B, pp 41–57. Springer, New YorkGoogle Scholar
  56. Imhoff JF and Hiraishi A (2005) Aerobic bacteria containing bacteriochlorophyll and belonging to the Alphaproteobacteria. In: Brenner DJ, Krieg NR, Staley JT and Garrity GM (eds) Bergey’s Manual of Systematic Bacteriology, Vol 2, part A, pp 135. Springer, New YorkGoogle Scholar
  57. Imhoff JF, Hiraishi A and Süling J (2005) Anoxygenic phototrophic purple bacteria. In: Brenner DJ, Krieg NR, Staley JT and Garrity GM (eds) Bergey’s Manual of Systematic Bacteriology, Vol 2, part A, pp 119–132. Springer, New YorkCrossRefGoogle Scholar
  58. Jenney FE, Prince RC and Daldal F (1994) Roles of soluble cytochrome c(2) and membrane-associated cytochrome c(y) of Rhodobacter capsulatus in photosynthetic electron transfer. Biochemistry 33: 2496–2502PubMedCrossRefGoogle Scholar
  59. Jørgensen BB (1990) The sulfur cycle of freshwater sediments: Role of thiosulfate. Limnol Oceanogr 35: 1329–1342CrossRefGoogle Scholar
  60. Kappler U (2007) Bacterial sulfite-oxidizing enzymes – enzymes for chemolithotrophy only? In: Dahl C and Friedrich CG (eds) Microbial Sulfur Metabolism, pp 151–169. Springer, HeidelbergGoogle Scholar
  61. Kappler, U and Bailey, S (2005) Molecular basis of intramolecular electron transfer in sulfite-oxidizing enzymes is revealed by high resolution structure of a heterodimeric complex of the catalytic molybdopterin subunit and a c-type cytochrome subunit. J Biol Chem 280: 24999–245007PubMedCrossRefGoogle Scholar
  62. Kappler U and Dahl C (2001) Enzymology and molecular biology of prokaryotic sulfite oxidation (minireview). FEMS Microbiol Lett 203: 1–9PubMedGoogle Scholar
  63. Kappler U, Bennett B, Rethmeier J, Schwarz G, Deutzmann R, McEwan AG and Dahl C (2000) Sulfite: cytochrome c oxidoreductase from Thiobacillus novellus – Purification, characterization, and molecular biology of a heterodimeric member of the sulfite oxidase family. J Biol Chem 275: 13202–13212PubMedCrossRefGoogle Scholar
  64. Keppen OI, Baulina OI, Lysenko AM and Kondrateva EN (1993) A new green bacterium belonging to the Chloroflexaceae family. Microbiology 62: 179–185Google Scholar
  65. Kerfeld CA, Chan C, Hirasawa M, Kleis-SanFrancisco S, Yeates TO and Knaff DB (1996) Isolation and characterization of soluble electron transfer proteins from Chromatium purpuratum. Biochemistry 35: 7812–7818PubMedCrossRefGoogle Scholar
  66. Khanna S and Nicholas DJD (1982) Utilization of tetrathionate and 35S-labelled thiosulphate by washed cells of Chlorobium vibrioforme f. sp. thiosulfatophilum. J Gen Microbiol 128: 1027–1034Google Scholar
  67. Kisker C, Schindelin H and Rees DC (1997) Molybdenum-cofactor-containing enzymes: Structure and mechanism. Ann Rev Biochem 66: 233–267PubMedCrossRefGoogle Scholar
  68. Kleinjan WE, de Keizer A and Janssen AJH (2003) Biologically produced sulfur. In: Steudel R (ed) Elemental Sulfur and Sulfur-Rich Compounds I., pp 167–187. Springer, BerlinGoogle Scholar
  69. Knobloch K, Schmitt W, Schleifer G, Appelt N and Müller H (1981) On the enzymatic system thiosulfate-cytochrome c-oxidoreductase. In: Bothe H and Trebst A (eds) Biology of Inorganic Nitrogen and Sulfur, pp 359–365. Springer, BerlinGoogle Scholar
  70. Kondratieva EN, Zhukov VG, Ivanovskii RN, Petushkova YP and Monosov EZ (1981) Light and dark metabolism in purple sulfur bacteria. Sov Sci Rev 2: 325–364Google Scholar
  71. Kopriva S, Büchert T, Fritz G, Suter M, Weber M, Benda R, Schaller J, Feller U, Schürmann P, Schünemann V, Trautwein AX, Kroneck PMH and Brunold C (2001) Plant adenosine 5′-phosphosulfate reductase is a novel iron–sulfur protein. J Biol Chem 276: 42881–42886PubMedCrossRefGoogle Scholar
  72. Krafft T, Bokranz M, Klimmek O, Schröder I, Fahrenholz F, Kojro E and Kröger A (1992) Cloning and nucleotide sequence of the psrA gene of Wolinella succinogenes polysulphide reductase. Eur J Biochem 206: 503–510PubMedCrossRefGoogle Scholar
  73. Kusai K and Yamanaka T (1973) The oxidation mechanisms of thiosulphate and sulphide in Chlorobium thiosulphatophilum: roles of cytochrome c-551 and cytochrome c-553. Biochim Biophys Acta 325: 304–314PubMedCrossRefGoogle Scholar
  74. Larsen H (1952) On the culture and general physiology of the green sulfur bacteria. J Bacteriol 64: 187–196PubMedCrossRefGoogle Scholar
  75. Leguijt T (1993) Photosynthetic electron transfer in Ectothiorhodospira. PhD Dissertation, University of AmsterdamGoogle Scholar
  76. Leyh TS (1993) The physical biochemistry and molecular genetics of sulfate activation. Crit Rev Biochem Mol Biol 28: 515–542PubMedCrossRefGoogle Scholar
  77. Lübbe YJ, Youn H-S, Timkovich R and Dahl C (2006) Siro(haem) amide in Allochromatium vinosum and relevance of DsrL and DsrN, a homolog of cobyrinic acid a, c diamide synthase for sulfur oxidation. FEMS Microbiol Lett 261: 194–202PubMedCrossRefGoogle Scholar
  78. Madigan MT (2001a) Family VI. “Heliobacteriaceae” Beer-Romero and Gest 1987, 113. In: Garrity G (ed) Bergey’s Manual of Systematic Bacteriology, Vol 1, pp 625–630. Springer, New YorkGoogle Scholar
  79. Madigan MT (2001b) The Family Heliobacteriaceae. In: Dworkin M (ed) The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community, http://link.springer-ny.com/link/service/books/10125/. Springer, New York
  80. Madigan MT and Brock TD (1977) CO2 fixation in photosynthetically-grown Chloroflexus auranticus. FEMS Microbiol Lett 1: 301–304CrossRefGoogle Scholar
  81. Menin L, Gaillard J, Parot P, Schoepp B, Nitschke W and Verméglio A (1998) Role of HiPIP as electron donor to the RC-bound cytochrome in photosynthetic purple bacteria. Photosyn Res 55: 343–348CrossRefGoogle Scholar
  82. Meulenberg R, Pronk JT, Frank J, Hazeu W, Bos P and Kuenen JG (1992a) Purification and partial characterization of a thermostable trithionate hydrolase from the acidophilic sulphur oxidizer Thiobacillus acidophilus. Eur J Biochem 209: 367–374PubMedCrossRefGoogle Scholar
  83. Meulenberg R, Pronk JT, Hazeu W, van Dijken JP, Frank J, Bos P and Kuenen JG (1993) Purification and partial characterization of thiosulphate dehydrogenase from Thiobacillus acidophilus. J Gen Microbiol 139: 2033–2039Google Scholar
  84. Meulenberg R, Pronk JT, Hazeu W, Bos P and Kuenen JG (1992b) Oxidation of reduced sulphur compounds by intact cells of Thiobacillus acidophilus. Arch Microbiol 157: 161–168Google Scholar
  85. Myers JD and Kelly DJ (2005) A sulphite respiration system in the chemoheterotrophic human pathogen Campylobacter jejuni. Microbiology151: 233–242PubMedCrossRefGoogle Scholar
  86. Myers JM and Myers CR (2001) Role for outer membrane cytochromes OmcA and OmcB of Shewanella putrefaciens MR-1 in reduction of manganese dioxide. Appl Environ Microbiol 67: 260–269PubMedCrossRefGoogle Scholar
  87. Nakamura K, Nakamura M, Yoshikawa H and Amano Y (2001) Purification and properties of thiosulfate dehydrogenase from Acidithiobacillus thiooxidans JCM7814. Biosci Biotechnol Biochem 65: 102–108PubMedCrossRefGoogle Scholar
  88. Nitschke W, Jubault-Bregler M and Rutherford AW (1993) The reaction center associated tetraheme cytochrome subunit from Chromatium vinosum revisited: a reexamination of its EPR properties. Biochemistry 32: 8871–8879PubMedCrossRefGoogle Scholar
  89. Numata T, Fukai S, Ikeuchi Y, Suzuki T and Nureki O (2006) Structural basis for sulfur relay to RNA mediated by heterohexameric TusBCD complex. Structure 14: 357–366PubMedCrossRefGoogle Scholar
  90. Overmann J, Fischer U and Pfennig N (1992) A new purple sulfur bacterium from saline littoral sediments, Thiorhodovibrio winogradskyi gen. nov. and sp. nov. Arch Microbiol 157: 329–335CrossRefGoogle Scholar
  91. Pattaragulwanit K and Dahl C (1995) Development of a genetic system for a purple sulfur bacterium: conjugative plasmid transfer in Chromatium vinosum. Arch Microbiol 164: 217–222CrossRefGoogle Scholar
  92. Pattaragulwanit K, Brune DC, Trüper HG and Dahl C (1998) Molecular genetic evidence for extracytoplasmic localization of sulfur globules in Chromatium vinosum. Arch Microbiol 169: 434–444PubMedCrossRefGoogle Scholar
  93. Peck HD, Jr. (1968) Energy-coupling mechanisms in chemolithotrophic bacteria. Annu Rev Microbiol 22: 489–518PubMedCrossRefGoogle Scholar
  94. Pibernat IV and Abella CA (1996) Sulfide pulsing as the controlling factor of spinae production in Chlorobium limicola strain UdG 6038. Arch Microbiol 165: 272–278PubMedCrossRefGoogle Scholar
  95. Pickering IJ, George GN, Yu EY, Brune DC, Tuschak C, Overmann J, Beatty JT and Prince RC (2001) Analysis of sulfur biochemistry of sulfur bacteria using x-ray absorption spectroscopy. Biochemistry 40: 8138–8145PubMedCrossRefGoogle Scholar
  96. Pires RH, Lourenco AI, Morais F, Teixeira M, Xavier AV, Saraiva LM and Pereira IAC (2003) A novel membrane-bound respiratory complex from Desulfovibrio desulfuricans ATCC 27774. Biochim Biophys Acta 1605: 67–82PubMedCrossRefGoogle Scholar
  97. Pires, RH, Venceslau, SS, Morais, F, Teixeira, M, Xavier, AV and Pereira, IAC (2006) Characterization of the Desulfovibrio desulfuricans ATCC 27774 DsrMKJOP complex – a membrane-bound redox complex involved in the sulfate respiratory pathway. Biochemistry 45: 249–262PubMedCrossRefGoogle Scholar
  98. Pittman MS, Robinson HC and Poole RK (2005) A bacterial glutathione transporter (Escherichia coli CydDC) exports reductant to the periplasm. J Biol Chem 280: 32254–32261PubMedCrossRefGoogle Scholar
  99. Podgorsek L and Imhoff JF (1999) Tetrathionate production by sulfur oxidizing bacteria and the role of tetrathionate in the sulfur cycle of Baltic Sea sediments. Aquat Microb Ecol 17: 255–265CrossRefGoogle Scholar
  100. Pott AS and 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: 1881–1894PubMedCrossRefGoogle Scholar
  101. Prange A, Arzberger I, Engemann C, Modrow H, Schumann O, Trüper HG, Steudel R, Dahl C and 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: 446–454PubMedGoogle Scholar
  102. Prange A, Chauvistre R, Modrow H, Hormes J, Trüper HG and 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: 267–276PubMedGoogle Scholar
  103. Prange A, Dahl C, Trüper HG, Behnke M, Hahn J, Modrow H and 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: 589–596CrossRefGoogle Scholar
  104. Prange A, Dahl C, Trüper HG, Chauvistre R, Modrow H and Hormes J (2002c) X-ray absorption spectroscopy of bacterial sulfur globules: a detailed reply. Microbiology 148: 2268–2270Google Scholar
  105. Prange A, Engelhardt H, Trüper HG and 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: 165–174PubMedCrossRefGoogle Scholar
  106. Pronk JT, Meulenberg R, Hazeu W, Bos P and Kuenen JG (1990) Oxidation of reduced inorganic sulphur compounds by acidophilic thiobacilli. FEMS Microbiol Rev 75: 293–306CrossRefGoogle Scholar
  107. Raitsimring AM, Kappler U, Feng CJ, Astashkin AV and Enemark JH (2005) Pulsed EPR studies of a bacterial sulfite-oxidizing enzyme with pH-invariant hyperfine interactions from exchangeable protons. Inorg Chem 44: 7283–7285PubMedCrossRefGoogle Scholar
  108. Ramírez, P, Guiliani, N, Valenzuela, L, Beard, S and Jerez, CA (2004) Differential protein expression during growth of Acidithiobacillus ferrooxidans on ferrous iron, sulfur compounds, or metal sulfides. Appl Enivron Microbiol 70: 4491–4498CrossRefGoogle Scholar
  109. Raymond JC and Sistrom WR (1969) Ectothiorhodospira halophila – a new species of the genus Ectothiorhodospira. Arch Mikrobiol 69: 121–126PubMedCrossRefGoogle Scholar
  110. Rees GN, Harfoot CG, Janssen PH, Schoenborn L, Kuever J and Lunsdorf H (2002) Thiobaca trueperi gen. nov., sp. nov., a phototrophic purple sulfur bacterium isolated from freshwater lake sediment. Int J Syst Evol Microbiol 52: 671–678PubMedGoogle Scholar
  111. Reinartz M, Tschäpe J, Brüser T, Trüper HG and Dahl C (1998) Sulfide oxidation in the phototrophic sulfur bacterium Chromatium vinosum. Arch Microbiol 170: 59–68PubMedCrossRefGoogle Scholar
  112. Renosto F, Martin RL, Borrell JL, Nelson DC and Segel IH (1991) ATP sulfurylase from trophosome tissue of Riftia pachyptila (hydrothermal vent tube worm). Arch Biochem Biophys 290: 66–78PubMedCrossRefGoogle Scholar
  113. Rohwerder T and Sand W (2003) The sulfane sulfur of persulfides is the actual substrate of the sulfur-oxidizing enzymes from Acidithiobacillus and Acidiphilium spp. Microbiology 149: 1699–1709PubMedCrossRefGoogle Scholar
  114. Rother D, Heinrich HJ, Quentmeier A, Bardischewsky F and Friedrich CG (2001) Novel genes of the sox gene cluster, mutagenesis of the flavoprotein SoxF, and evidence for a general sulfur-oxidizing system in Paracoccus pantotrophus GB17. J Bacteriol 183: 4499–4508PubMedCrossRefGoogle Scholar
  115. Samyn B, DeSmet L, van Driessche G, Meyer TE, Bartsch RG, Cusanovich MA and van Beeumen JJ (1996) A high-potential soluble cytochrome c-551 from the purple phototrophic bacterium Chromatium vinosum is homologous to cytochrome c(8) from denitrifying pseudomonads. Eur J Biochem 236: 689–696PubMedCrossRefGoogle Scholar
  116. Sanchez O, Ferrera I, Dahl C and Mas J (2001) In vivo role of APS reductase in the purple sulfur bacterium Allochromatium vinosum. Arch Microbiol 176: 301–305PubMedCrossRefGoogle Scholar
  117. Sander J and Dahl C (2008) Metabolism of inorganic sulfur compounds in purple bacteria. In: Hunter CN, Daldal, F, Thurnauer, MC and Beatty, JT (eds) Purple Bacteria (Advances in Photosynthesis and Respiration), in press. Springer, New YorkGoogle Scholar
  118. Sander J, Engels-Schwarzlose S and Dahl C (2006) Importance of the DsrMKJOP complex for sulfur oxidation in Allochromatium vinosum and phylogenetic analysis of related complexes in other prokaryotes. Arch Microbiol 186: 357–366PubMedCrossRefGoogle Scholar
  119. Schedel M and Trüper HG (1980) Anaerobic oxidation of thiosulfate and elemental sulfur in Thiobacillus denitrificans. Arch Microbiol 124: 205–210CrossRefGoogle Scholar
  120. Schedel M, Vanselow M and Trüper HG (1979) Siroheme sulfite reductase from Chromatium vinosum. Purification and investigation of some of its molecular and catalytic properties. Arch Microbiol 121: 29–36CrossRefGoogle Scholar
  121. Schmidt GL, Nicolson GL and Kamen MD (1971) Composition of the sulfur particle of Chromatium vinosum. J Bacteriol 105: 1137–1141PubMedGoogle Scholar
  122. Schmitt W, Schleifer G and Knobloch K (1981) The enzymatic system thiosulfate: cytochrome c oxidoreductase from photolithoautotrophically grown Chromatium vinosum. Arch Microbiol 130: 334–338CrossRefGoogle Scholar
  123. Schütz M, Maldener I, Griesbeck C and Hauska G (1999) Sulfide-quinone reductase from Rhodobacter capsulatus: requirement for growth, periplasmic localization, and extension of gene sequence analysis. J Bacteriol 181: 6516–6523PubMedGoogle Scholar
  124. Schütz M, Shahak Y, Padan E and Hauska G (1997) Sulfide-quinone reductase from Rhodobacter capsulatus. J Biol Chem 272: 9890–9894PubMedCrossRefGoogle Scholar
  125. Segel IH (1993) Enzyme kinetics: behaviour and analysis of rapid equilibrium and steady-state enzyme systems. Wiley-Interscience, New YorkGoogle Scholar
  126. Shahak Y, Arieli B, Padan E and Hauska G (1992) Sulfide quinone reductase (SQR) activity in Chlorobium. FEBS Lett 299: 127–130PubMedCrossRefGoogle Scholar
  127. Shively JM, Bryant DA, Fuller RC, Konopka AE, Stevens SE and Strohl WR (1989) Functional inclusions in prokaryotic cells. Int Rev Cytol 113: 35–100CrossRefGoogle Scholar
  128. Smith AJ (1966) The role of tetrathionate in the oxidation of thiosulphate by Chromatium sp. strain D. J Gen Microbiol 42: 371–380PubMedGoogle Scholar
  129. Smith AJ and Lascelles J (1966) Thiosulphate metabolism and rhodanese in Chromatium sp. strain D. J Gen Microbiol 42: 357–370PubMedGoogle Scholar
  130. Sorokin DY, Teske A, Robertson LA and Kuenen JG (1999) Anaerobic oxidation of thiosulfate to tetrathionate by obligately heterotrophic bacteria, belonging to the Pseudomonas stutzeri group. FEMS Microbiol Ecol 30: 113–123PubMedCrossRefGoogle Scholar
  131. Sorokin DY, Tourova TP, Kuznetsov BB, Bryantseva IA and Gorlenko VM (2000) Roseinatronobacter thiooxidans gen. nov., sp. nov., a new alkaliphilic aerobic bacteriochlorophyll a–containing bacterium isolated from a soda lake. Microbiology 69: 75–82Google Scholar
  132. Sperling D, Kappler U, Wynen A, Dahl C and Trüper HG (1998) Dissimilatory ATP sulfurylase from the hyperthermophilic sulfate reducer Archaeoglobus fulgidus belongs to the group of homo-oligomeric ATP sulfurylases. FEMS Microbiol Lett 162: 257–264PubMedCrossRefGoogle Scholar
  133. Steinmetz MA and Fischer U (1982) Cytochromes of the green sulfur bacterium Chlorobium vibrioforme f. thiosulfatophilum. Purification, characterization and sulfur metabolism. Arch Microbiol 19: 19–26CrossRefGoogle Scholar
  134. Steudel R (1989) On the nature of the “elemental sulfur” (S0) produced by sulfur-oxidizing bacteria- a model for S0 globules. In: Schlegel HG and Bowien B (eds) Autotrophic Bacteria, pp 289–303. Science Tech Publishers, Madison, WIGoogle Scholar
  135. Steudel R (1996) Mechanism for the formation of elemental sulfur from aqueous sulfide in chemical and microbiological desulfurization processes. Ind Eng Chem Res 35: 1417–1423CrossRefGoogle Scholar
  136. 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
  137. 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
  138. Steudel R, Holdt G, Visscher PT and van Gemerden H (1990) Search for polythionates in cultures of Chromatium vinosum after sulfide incubation. Arch Microbiol 155: 432–437CrossRefGoogle Scholar
  139. Suzuki H, Koyanagi T, Izuka S, Onishi A and Kumagai H (2005) The yliA, -B, -C, and -D genes of Escherichia coli K-12 encode a novel glutathione importer with an ATP-binding cassette. J Bacteriol 187: 5861–5867PubMedCrossRefGoogle Scholar
  140. Taylor BF (1994) Adenylylsulfate reductases from thiobacilli. Meth Enzymol 243: 393–400CrossRefGoogle Scholar
  141. Then J and Trüper HG (1981) The role of thiosulfate in sulfur metabolism of Rhodopseudomonas globiformis. Arch Microbiol 130: 143–146CrossRefGoogle Scholar
  142. Then J and Trüper HG (1983) Sulfide oxidation in Ectothiorhodospira abdelmalekii. Evidence for the catalytic role of cytochrome c-551. Arch Microbiol 135: 254–258CrossRefGoogle Scholar
  143. Then J and Trüper HG (1984) Utilization of sulfide and elemental sulfur by Ectothiorhodospira halochloris. Arch Microbiol 139: 295–298CrossRefGoogle Scholar
  144. Trüper HG (1978) Sulfur metabolism. In: Clayton RK and Sistrom WR (eds) The Photosynthetic Bacteria, pp 677–690. Plenum, New YorkGoogle Scholar
  145. 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
  146. Trüper HG and Pfennig N (1966) Sulphur metabolism in Thiorhodaceae. III. Storage and turnover of thiosulphate sulphur in Thiocapsa floridana and Chromatium species. Antonie van Leeuwenhoek Int J Gen Mol Microbiol 32: 261–276CrossRefGoogle Scholar
  147. Trüper HG and Rogers LA (1971) Purification and properties of adenylyl sulfate reductase from the phototrophic sulfur bacterium, Thiocapsa roseopersicina. J Bacteriol 108: 1112–1121PubMedGoogle Scholar
  148. van Beeumen JJ, Demol H, Samyn B, Bartsch RG, Meyer TE, Dolata MM and Cusanovich MA (1991) Covalent structure of the diheme cytochrome subunit and amino-terminal sequence of the flavoprotein subunit of flavocytochrome c from Chromatium vinosum. J Biol Chem 266: 12921–12931PubMedGoogle Scholar
  149. van Driessche G, Vandenberghe I, Devreese B, Samyn B, Meyer TE, Leigh R, Cusanovich MA, Bartsch RG, Fischer U and van Beeumen JJ (2003) Amino acid sequences and distribution of high-potential iron–sulfur proteins that donate electrons to the photosynthetic reaction center in phototropic proteobacteria. J Mol Evol 57: 181–199PubMedCrossRefGoogle Scholar
  150. van Gemerden H (1968) On the ATP generation by Chromatium in the dark. Arch Mikrobiol 64: 118–124PubMedCrossRefGoogle Scholar
  151. van Gemerden H (1987) Competition between purple sulfur bacteria and green sulfur bacteria: role of sulfide, sulfur and polysulfides. In: Lindholm T (ed) Ecology of Photosynthetic Prokaryotes with Special Reference to Meromictic Lakes and Coastal Lagoons, pp 13–27. Abo Academy, AboGoogle Scholar
  152. Vermeglio A, Li J, Schoepp-Cothenet B, Pratt N and Knaff DB (2002) The role of high-potential iron protein and cytochrome c(8) as alternative electron donors to the reaction center of Chromatium vinosum. Biochemistry 41: 8868–8875PubMedCrossRefGoogle Scholar
  153. Visscher PT, Nijburg JW and van Gemerden H (1990) Polysulfide utilization by Thiocapsa roseopersicina. Arch Microbiol 155: 75–81CrossRefGoogle Scholar
  154. Visscher PT and Taylor BF (1993) Organic thiols as organolithotrophic substrates for growth of phototrophic bacteria. Appl Environ Microbiol 59: 93–96PubMedGoogle Scholar
  155. Visscher PT and van Gemerden H (1991) Photoautotrophic growth of Thiocapsa roseopersicina on dimethyl sulfide. FEMS Microbiol Lett 81: 247–250CrossRefGoogle Scholar
  156. Visser JM, de Jong GAH, Robertson LA and Kuenen JG (1996) Purification and characterization of a periplasmic thiosulfate dehydrogenase from the obligately autotrophic Thiobacillus sp. W5. Arch Microbiol 166: 372–378PubMedCrossRefGoogle Scholar
  157. Williams TJ, Zhang CL, Scott JH and Bazylinski DA (2006) Evidence for autotrophy via the reverse tricarboxylic acid cycle in the marine magnetotactic coccus strain MC-1. Appl Environ Microbiol 72: 1322–1329PubMedCrossRefGoogle Scholar
  158. Yu Z, Lansdon EB, Segel IH and Fisher AJ (2007) Crystal structure of the bifunctional ATP sulfurylase – APS kinase from the chemolithotrophic thermophile Aquifex aeolicus. J Mol Biol 365: 732–743PubMedCrossRefGoogle Scholar
  159. Yurkov VV (2006) Aerobic phototrophic proteobacteria. In: Dworkin M, Falkow, S, Rosenberg, E, Schleifer, K-H and Stackebrandt, E (eds) The Prokaryotes, Vol 5, pp 562–584. Springer, New YorkCrossRefGoogle Scholar
  160. Yurkov VV, Krasil’nikova EN and Gorlenko VM (1994) Thiosulfate metabolism in the aerobic bacteriochloro-phyll-a-containing bacteria Erythromicrobium hydrolyticum and Roseococcus thiosulfatophilus. Microbiology 63: 91–94Google Scholar
  161. Zaar A, Fuchs G, Golecki JR and Overmann J (2003) A new purple sulfur bacterium isolated from a littoral microbial mat, Thiorhodococcus drewsii sp. nov. Arch Microbiol 179: 174–183PubMedGoogle Scholar

Copyright information

© Springer Science + Business Media B.V 2008

Authors and Affiliations

  • Christiane Dahl
    • 1
  1. 1.Institute of Microbiology & BiotechnologyUniversity of BonnGermany

Personalised recommendations