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
2019-10-18
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. [CrossRef]
    [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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][PubMed]
    [Google Scholar]
  7. Dahl C.. ( 2008;). Inorganic sulfur compounds as electron donors in purple sulfur bacteria. . In Sulfur in Phototrophic Organisms, pp. 289–317. Edited by Hell R., Dahl C., Knaff D. B., Leustek T... Dordrecht:: Springer;. [CrossRef]
    [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. [CrossRef][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. [CrossRef][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. [CrossRef][PubMed]
    [Google Scholar]
  11. Frigaard N.-U., Bryant D. A.. ( 2008;). Genomic insights into the sulfur metabolism of phototrophic green sulfur bacteria. . In Sulfur Metabolism in Phototrophic Organisms, pp. 337–355. Edited by Hell R., Dahl C., Knaff D. B., Leustek T... Dordrecht:: Springer;. [CrossRef]
    [Google Scholar]
  12. Frigaard N.-U., Dahl C.. ( 2008;). Sulfur metabolism in phototrophic sulfur bacteria. . Adv Microb Physiol 54:, 103–200. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][PubMed]
    [Google Scholar]
  21. Horton R. M.. ( 1995;). PCR-mediated recombination and mutagenesis. . Mol Biotechnol 3:, 93–99. [CrossRef][PubMed]
    [Google Scholar]
  22. Imhoff J. F.. ( 2005a;). Family I. Chromatiaceae Bavendamm 1924, 125AL emend. Imhoff 1984b, 339. . In Bergey's Manual of Systematic Bacteriology, pp. 3–40. Edited by 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. . In Bergey's Manual of Systematic Bacteriology, pp. 41–57. Edited by 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. [CrossRef][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. [CrossRef][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. [CrossRef][PubMed]
    [Google Scholar]
  27. Kappler U., Maher M. J.. ( 2013;). The bacterial SoxAX cytochromes. . Cell Mol Life Sci 70:, 977–992. [CrossRef][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. [CrossRef][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. [CrossRef]
    [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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. ? In Programme & Abstract Book EMBO Workshop on Microbial Sulfur Metabolism, Noordwijkerhout, p. 29.
    [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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef]
    [Google Scholar]
  44. Park H., Bakalinsky A. T.. ( 2000;). SSU1 mediates sulphite efflux in Saccharomyces cerevisiae. . Yeast 16:, 881–888. [CrossRef][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. [CrossRef]
    [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. [CrossRef][PubMed]
    [Google Scholar]
  47. Pfennig N., Trüper H. G.. ( 1992;). The family Chromatiaceae. . In The Prokaryotes. A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications, pp. 3200–3221. Edited by 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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef]
    [Google Scholar]
  53. Rodriguez J., Hiras J., Hanson T. E.. ( 2011;). Sulfite oxidation in Chlorobaculum tepidum. . Front Microbiol 2:, 112. [CrossRef][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. [CrossRef][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, 2nd edn. 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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][PubMed]
    [Google Scholar]
  62. Simon J., Kroneck P. M.. ( 2013;). Microbial sulfite respiration. . Adv Microb Physiol 62:, 45–117. [CrossRef][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. [CrossRef]
    [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. [CrossRef][PubMed]
    [Google Scholar]
  65. Suzuki I.. ( 1999;). Oxidation of inorganic sulfur compounds: chemical and enzymatic reactions. . Can J Microbiol 45:, 97–105. [CrossRef]
    [Google Scholar]
  66. Weaver P. F., Wall J. D., Gest H.. ( 1975;). Characterization of Rhodopseudomonas capsulata. . Arch Microbiol 105:, 207–216. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][PubMed]
    [Google Scholar]
  71. Wilson J. J., Kappler U.. ( 2009;). Sulfite oxidation in Sinorhizobium meliloti. . Biochim Biophys Acta 1787:, 1516–1525. [CrossRef][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...

Supplements

Supplementary material 

PDF
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