1887

Abstract

In phototrophic sulfur bacteria, sulfite is a well-established intermediate during reduced sulfur compound oxidation. Sulfite is generated in the cytoplasm by the reverse-acting dissimilatory sulfite reductase DsrAB. Many purple sulfur bacteria can even use externally available sulfite as a photosynthetic electron donor. Nevertheless, the exact mode of sulfite oxidation in these organisms is a long-standing enigma. Indirect oxidation in the cytoplasm via adenosine-5′-phosphosulfate (APS) catalysed by APS reductase and ATP sulfurylase is neither generally present nor essential. The inhibition of sulfite oxidation by tungstate in the model organism indicated the involvement of a molybdoenzyme, but homologues of the periplasmic molybdopterin-containing SorAB or SorT sulfite dehydrogenases are not encoded in genome-sequenced purple or green sulfur bacteria. However, genes for a membrane-bound polysulfide reductase-like iron–sulfur molybdoprotein (SoeABC) are universally present. The catalytic subunit of the protein is predicted to be oriented towards the cytoplasm. We compared the sulfide- and sulfite-oxidizing capabilities of WT with single mutants deficient in SoeABC or APS reductase and the respective double mutant, and were thus able to prove that SoeABC is the major sulfite-oxidizing enzyme in and probably also in other phototrophic sulfur bacteria. The genes also occur in a large number of chemotrophs, indicating a general importance of SoeABC for sulfite oxidation in the cytoplasm. Furthermore, we showed that the periplasmic sulfur substrate-binding protein SoxYZ is needed in parallel to the cytoplasmic enzymes for effective sulfite oxidation in and provided a model for the interplay between these systems despite their localization in different cellular compartments.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.071019-0
2013-12-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/12/2626.html?itemId=/content/journal/micro/10.1099/mic.0.071019-0&mimeType=html&fmt=ahah

References

  1. Bartlett J. K., Skoog D. A.( 1954). Colorimetric determination of elemental sulfur in hydrocarbons. Anal Chem 26:1008–1011 [View Article]
    [Google Scholar]
  2. Bazaral M., Helinski D. R.( 1968). Circular DNA forms of colicinogenic factors E1, E2 and E3 from Escherichia coli. J Mol Biol 36:185–194 [View Article][PubMed]
    [Google Scholar]
  3. Bryantseva I. A., Gorlenko V. M., Kompantseva E. I., Imhoff J. F., Süling J., Mityushina L.( 1999). Thiorhodospira sibirica gen. nov., sp. nov., a new alkaliphilic purple sulfur bacterium from a Siberian soda lake. Int J Syst Bacteriol 49:697–703 [View Article][PubMed]
    [Google Scholar]
  4. Caumette P., Guyoneaud R., Imhoff J. F., Süling J., Gorlenko V.( 2004). Thiocapsa marina sp. nov., a novel, okenone-containing, purple sulfur bacterium isolated from brackish coastal and marine environments. Int J Syst Evol Microbiol 54:1031–1036 [View Article][PubMed]
    [Google Scholar]
  5. D’Errico G., Di Salle A., La Cara F., Rossi M., Cannio R.( 2006). Identification and characterization of a novel bacterial sulfite oxidase with no heme binding domain from Deinococcus radiodurans. J Bacteriol 188:694–701 [View Article][PubMed]
    [Google Scholar]
  6. Dahl C.( 1996). Insertional gene inactivation in a phototrophic sulphur bacterium: APS-reductase-deficient mutants of Chromatium vinosum. Microbiology 142:3363–3372 [View Article][PubMed]
    [Google Scholar]
  7. Dahl C.( 2008). Inorganic sulfur compounds as electron donors in purple sulfur bacteria. Sulfur in Phototrophic Organisms289–317 Hell R., Dahl C., Knaff D. B., Leustek T. Dordrecht: Springer; [View Article]
    [Google Scholar]
  8. Dahl C., Engels S., Pott-Sperling A. S., Schulte A., Sander J., Lübbe Y., Deuster O., Brune D. C.( 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 [View Article][PubMed]
    [Google Scholar]
  9. Denkmann K., Grein F., Zigann R., Siemen A., Bergmann J., van Helmont S., Nicolai A., Pereira I. A. C., Dahl C.( 2012). Thiosulfate dehydrogenase: a widespread unusual acidophilic c-type cytochrome. Environ Microbiol 14:2673–2688 [View Article][PubMed]
    [Google Scholar]
  10. Friedrich C. G., 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 [View Article][PubMed]
    [Google Scholar]
  11. Frigaard N.-U., Bryant D. A.( 2008). Genomic insights into the sulfur metabolism of phototrophic green sulfur bacteria. Sulfur Metabolism in Phototrophic Organisms337–355 Hell R., Dahl C., Knaff D. B., Leustek T. Dordrecht: Springer; [View Article]
    [Google Scholar]
  12. Frigaard N.-U., Dahl C.( 2008). Sulfur metabolism in phototrophic sulfur bacteria. Adv Microb Physiol 54:103–200 [View Article][PubMed]
    [Google Scholar]
  13. Gregersen L. H., Bryant D. A., Frigaard N.-U.( 2011). Mechanisms and evolution of oxidative sulfur metabolism in green sulfur bacteria. Front Microbiol 2:116 [View Article][PubMed]
    [Google Scholar]
  14. Grein F., Pereira I. A. C., Dahl C.( 2010a). Biochemical characterization of individual components of the Allochromatium vinosum DsrMKJOP transmembrane complex aids understanding of complex function in vivo. J Bacteriol 192:6369–6377 [View Article][PubMed]
    [Google Scholar]
  15. Grein F., Venceslau S. S., Schneider L., Hildebrandt P., Todorovic S., Pereira I. A. C., Dahl C.( 2010b). DsrJ, an essential part of the DsrMKJOP transmembrane complex in the purple sulfur bacterium Allochromatium vinosum, is an unusual triheme cytochrome c. Biochemistry 49:8290–8299 [View Article][PubMed]
    [Google Scholar]
  16. Grein F., Ramos A. R., Venceslau S. S., Pereira I. A. C.( 2013). Unifying concepts in anaerobic respiration: insights from dissimilatory sulfur metabolism. Biochim Biophys Acta 1827:145–160 [View Article][PubMed]
    [Google Scholar]
  17. Heinzinger N. K., Fujimoto S. Y., Clark M. A., Moreno M. S., Barrett E. L.( 1995). Sequence analysis of the phs operon in Salmonella typhimurium and the contribution of thiosulfate reduction to anaerobic energy metabolism. J Bacteriol 177:2813–2820[PubMed]
    [Google Scholar]
  18. Hensel M., Hinsley A. P., Nikolaus T., Sawers G., Berks B. C.( 1999). The genetic basis of tetrathionate respiration in Salmonella typhimurium. Mol Microbiol 32:275–287 [View Article][PubMed]
    [Google Scholar]
  19. Hensen D., Sperling D., Trüper H. G., Brune D. C., Dahl C.( 2006). Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum. Mol Microbiol 62:794–810 [View Article][PubMed]
    [Google Scholar]
  20. Hipp W. M., Pott A. S., Thum-Schmitz N., Faath I., Dahl C., Trüper H. G.( 1997). Towards the phylogeny of APS reductases and sirohaem sulfite reductases in sulfate-reducing and sulfur-oxidizing prokaryotes. Microbiology 143:2891–2902 [View Article][PubMed]
    [Google Scholar]
  21. Horton R. M.( 1995). PCR-mediated recombination and mutagenesis. Mol Biotechnol 3:93–99 [View Article][PubMed]
    [Google Scholar]
  22. Imhoff J. F.( 2005a). Family I. Chromatiaceae Bavendamm 1924, 125AL emend. Imhoff 1984b, 339. Bergey's Manual of Systematic Bacteriology3–40 Brenner D. J., Krieg N. R., Staley J. T., Garrity G. M. New York: Springer;
    [Google Scholar]
  23. Imhoff J. F.( 2005b). Family II. Ectothiorhodospiraceae Imhoff 1984b, 339VP. Bergey's Manual of Systematic Bacteriology41–57 Brenner D. J., Krieg N. R., Staley J. T., Garrity G. M. New York: Springer;
    [Google Scholar]
  24. Imhoff J. F., 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 [View Article][PubMed]
    [Google Scholar]
  25. Jormakka M., Yokoyama K., Yano T., Tamakoshi M., Akimoto S., Shimamura T., Curmi P., Iwata S.( 2008). Molecular mechanism of energy conservation in polysulfide respiration. Nat Struct Mol Biol 15:730–737 [View Article][PubMed]
    [Google Scholar]
  26. Kappler U., 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 280:24999–25007 [View Article][PubMed]
    [Google Scholar]
  27. Kappler U., Maher M. J.( 2013). The bacterial SoxAX cytochromes. Cell Mol Life Sci 70:977–992 [View Article][PubMed]
    [Google Scholar]
  28. Kappler U., Bennett B., Rethmeier J., Schwarz G., Deutzmann R., McEwan A. G., 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 275:13202–13212 [View Article][PubMed]
    [Google Scholar]
  29. Kelly D. P., Chambers L. A., Trudinger P. A.( 1969). Cyanolysis and spectrophotometric estimation of trithionate in mixture with thiosulfate and tetrathionate. Anal Chem 41:898–901 [View Article]
    [Google Scholar]
  30. Kisker C., Schindelin H., Baas D., Rétey J., Meckenstock R. U., Kroneck P. M.( 1998). A structural comparison of molybdenum cofactor-containing enzymes. FEMS Microbiol Rev 22:503–521 [View Article][PubMed]
    [Google Scholar]
  31. Kovach M. E., Elzer P. H., Hill D. S., Robertson G. T., Farris M. A., Roop R. M. II, Peterson K. M.( 1995). Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175–176 [View Article][PubMed]
    [Google Scholar]
  32. Krafft T., Bokranz M., Klimmek O., Schröder I., Fahrenholz F., Kojro E., Kröger A.( 1992). Cloning and nucleotide sequence of the psrA gene of Wolinella succinogenes polysulphide reductase. Eur J Biochem 206:503–510 [View Article][PubMed]
    [Google Scholar]
  33. Krejčík Z., Denger K., Weinitschke S., Hollemeyer K., Paces V., Cook A. M., Smits T. H. M.( 2008). Sulfoacetate released during the assimilation of taurine-nitrogen by Neptuniibacter caesariensis: purification of sulfoacetaldehyde dehydrogenase. Arch Microbiol 190:159–168 [View Article][PubMed]
    [Google Scholar]
  34. Laska S., Lottspeich F., Kletzin A.( 2003). Membrane-bound hydrogenase and sulfur reductase of the hyperthermophilic and acidophilic archaeon Acidianus ambivalens. Microbiology 149:2357–2371 [View Article][PubMed]
    [Google Scholar]
  35. Léchenne B., Reichard U., Zaugg C., Fratti M., Kunert J., Boulat O., Monod M.( 2007). Sulphite efflux pumps in Aspergillus fumigatus and dermatophytes. Microbiology 153:905–913 [View Article][PubMed]
    [Google Scholar]
  36. Leenhouts K. J., Kok J., Venema G.( 1990). Stability of integrated plasmids in the chromosome of Lactococcus lactis. Appl Environ Microbiol 56:2726–2735[PubMed]
    [Google Scholar]
  37. Lehmann S., Johnston A. W. B., Curson A. R. J., Todd J. D., Cook A. M.( 2012). SoeABC, a novel sulfite dehydrogenase in the Roseobacters. Programme & Abstract Book EMBO Workshop on Microbial Sulfur Metabolism, Noordwijkerhout29
    [Google Scholar]
  38. Lenk S., Moraru C., Hahnke S., Arnds J., Richter M., Kube M., Reinhardt R., Brinkhoff T., Harder J.& other authors ( 2012). Roseobacter clade bacteria are abundant in coastal sediments and encode a novel combination of sulfur oxidation genes. ISME J 6:2178–2187 [View Article][PubMed]
    [Google Scholar]
  39. Lübbe Y. J., Youn H.-S., Timkovich R., 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 sulphur oxidation. FEMS Microbiol Lett 261:194–202 [View Article][PubMed]
    [Google Scholar]
  40. Meyer B., Kuever J.( 2007). Molecular analysis of the distribution and phylogeny of dissimilatory adenosine-5′-phosphosulfate reductase-encoding genes (aprBA) among sulfur-oxidizing prokaryotes. Microbiology 153:3478–3498 [View Article][PubMed]
    [Google Scholar]
  41. Meyer B., Imhoff J. F., Kuever J.( 2007). Molecular analysis of the distribution and phylogeny of the soxB gene among sulfur-oxidizing bacteria – evolution of the Sox sulfur oxidation enzyme system. Environ Microbiol 9:2957–2977 [View Article][PubMed]
    [Google Scholar]
  42. Nardi T., Corich V., Giacomini A., Blondin B.( 2010). A sulphite-inducible form of the sulphite efflux gene SSU1 in a Saccharomyces cerevisiae wine yeast. Microbiology 156:1686–1696 [View Article][PubMed]
    [Google Scholar]
  43. Parey K., Demmer U., Warkentin E., Wynen A., Ermler U., Dahl C.( 2013). Structural, biochemical and genetic characterization of ATP sulfurylase from Allochromatium vinosum. PLoS ONE 8:e74707 [View Article]
    [Google Scholar]
  44. Park H., Bakalinsky A. T.( 2000). SSU1 mediates sulphite efflux in Saccharomyces cerevisiae. Yeast 16:881–888 [View Article][PubMed]
    [Google Scholar]
  45. 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 [View Article]
    [Google Scholar]
  46. Pattaragulwanit K., Brune D. C., Trüper H. G., Dahl C.( 1998). Molecular genetic evidence for extracytoplasmic localization of sulfur globules in Chromatium vinosum. Arch Microbiol 169:434–444 [View Article][PubMed]
    [Google Scholar]
  47. Pfennig N., Trüper H. G.( 1992). The family Chromatiaceae. The Prokaryotes. A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications3200–3221 Balows A., Trüper H. G., Dworkin M., Harder W., Schleifer K.-H. New York: Springer;
    [Google Scholar]
  48. Pott A. S., Dahl C.( 1998). Sirohaem sulfite reductase and other proteins encoded by genes at the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur. Microbiology 144:1881–1894 [View Article][PubMed]
    [Google Scholar]
  49. Prange A., Engelhardt H., Trüper H. G., 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 [View Article][PubMed]
    [Google Scholar]
  50. Ramos A. R., Keller K. L., Wall J. D., Pereira I. A. C.( 2012). The membrane QmoABC complex interacts directly with the dissimilatory adenosine 5′-phosphosulfate reductase in sulfate reducing bacteria. Front Microbiol 3:137 [View Article][PubMed]
    [Google Scholar]
  51. Reinartz M., Tschäpe J., Brüser T., Trüper H. G., Dahl C.( 1998). Sulfide oxidation in the phototrophic sulfur bacterium Chromatium vinosum. Arch Microbiol 170:59–68 [View Article][PubMed]
    [Google Scholar]
  52. Rethmeier J., Rabenstein A., Langer M., Fischer U.( 1997). Detection of traces of oxidized and reduced sulfur compounds in small samples by combination of different high- performance liquid chromatography methods. J Chromatogr A 760:295–302 [View Article]
    [Google Scholar]
  53. Rodriguez J., Hiras J., Hanson T. E.( 2011). Sulfite oxidation in Chlorobaculum tepidum. Front Microbiol 2:112 [View Article][PubMed]
    [Google Scholar]
  54. Rother D., Henrich H. J., Quentmeier A., Bardischewsky F., Friedrich C. G.( 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 183:4499–4508 [View Article][PubMed]
    [Google Scholar]
  55. Roy A. B., Trudinger P. A.( 1970). The Biochemistry of Inorganic Compounds of Sulfur London: Cambridge University Press;
    [Google Scholar]
  56. Sambrook J., Fritsch E. F., Maniatis T.( 1989). Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
    [Google Scholar]
  57. Sánchez O., Ferrera I., Dahl C., Mas J.( 2001). In vivo role of adenosine-5′-phosphosulfate reductase in the purple sulfur bacterium Allochromatium vinosum. Arch Microbiol 176:301–305 [View Article][PubMed]
    [Google Scholar]
  58. Sander J., Engels-Schwarzlose S., 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 186:357–366 [View Article][PubMed]
    [Google Scholar]
  59. Sauvé V., Bruno S., Berks B. C., Hemmings A. M.( 2007). The SoxYZ complex carries sulfur cycle intermediates on a peptide swinging arm. J Biol Chem 282:23194–23204 [View Article][PubMed]
    [Google Scholar]
  60. Schäfer A., Tauch A., Jäger W., Kalinowski J., Thierbach G., Pühler A.( 1994). Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145:69–73 [View Article][PubMed]
    [Google Scholar]
  61. Simon J., Kern M.( 2008). Quinone-reactive proteins devoid of haem b form widespread membrane-bound electron transport modules in bacterial respiration. Biochem Soc Trans 36:1011–1016 [View Article][PubMed]
    [Google Scholar]
  62. Simon J., Kroneck P. M.( 2013). Microbial sulfite respiration. Adv Microb Physiol 62:45–117 [View Article][PubMed]
    [Google Scholar]
  63. Simon R., Priefer U., Pühler A.( 1983). A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Biotechnology (N Y) 1:784–791 [View Article]
    [Google Scholar]
  64. Steudel R., Steudel Y.( 2010). Derivatives of cysteine related to the thiosulfate metabolism of sulfur bacteria by the multi-enzyme complex “Sox” studied by B3LYP-PCM and G3X(MP2) calculations. Phys Chem Chem Phys 12:630–644 [View Article][PubMed]
    [Google Scholar]
  65. Suzuki I.( 1999). Oxidation of inorganic sulfur compounds: chemical and enzymatic reactions. Can J Microbiol 45:97–105 [View Article]
    [Google Scholar]
  66. Weaver P. F., Wall J. D., Gest H.( 1975). Characterization of Rhodopseudomonas capsulata. Arch Microbiol 105:207–216 [View Article][PubMed]
    [Google Scholar]
  67. Weinitschke S., Denger K., Cook A. M., Smits T. H. M.( 2007). The DUF81 protein TauE in Cupriavidus necator H16, a sulfite exporter in the metabolism of C2 sulfonates. Microbiology 153:3055–3060 [View Article][PubMed]
    [Google Scholar]
  68. Weissgerber T., Zigann R., Bruce D., Chang Y.-J., Detter J. C., Han C., Hauser L., Jeffries C. D., Land M.& other authors ( 2011). Complete genome sequence of Allochromatium vinosum DSM 180(T).. Stand Genomic Sci 5:311–330 [View Article][PubMed]
    [Google Scholar]
  69. Weissgerber T., Dobler N., Polen T., Latus J., Stockdreher Y., Dahl C.( 2013). Genome-wide transcriptional profiling of the purple sulfur bacterium Allochromatium vinosum DSM 180T during growth on different reduced sulfur compounds. J Bacteriol 195:4231–4245 [View Article][PubMed]
    [Google Scholar]
  70. Welte C., Hafner S., Krätzer C., Quentmeier A. T., Friedrich C. G., Dahl C.( 2009). Interaction between Sox proteins of two physiologically distinct bacteria and a new protein involved in thiosulfate oxidation. FEBS Lett 583:1281–1286 [View Article][PubMed]
    [Google Scholar]
  71. Wilson J. J., Kappler U.( 2009). Sulfite oxidation in Sinorhizobium meliloti. Biochim Biophys Acta 1787:1516–1525 [View Article][PubMed]
    [Google Scholar]
  72. Zaar A., Fuchs G., Golecki J. R., Overmann J.( 2003). A new purple sulfur bacterium isolated from a littoral microbial mat, Thiorhodococcus drewsii sp. nov. Arch Microbiol 179:174–183[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.071019-0
Loading
/content/journal/micro/10.1099/mic.0.071019-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error