The reaction cycle of the reconstituted Sox enzyme system of Paracoccus pantotrophus requires the periplasmic proteins SoxYZ, SoxXA, SoxB, and SoxCD. The heme enzyme SoxXA covalently binds the sulfur substrate to the thiol of the single cysteine residue of SoxY located at its carboxy-terminal end. Bound sulfur is then oxidized to sulfate by a series of reactions. These involve sulfur dehydrogenase SoxCD which oxidizes the protein-bound sulfane sulfur to sulfone in a unique six-electron transfer. Bound sulfone is then hydrolyzed off by the sulfate thiohydrolase SoxB to regenerate SoxYZ. The flavoprotein SoxF enhances the rate of sulfur oxidation in vivo as evident from mutant analysis and we have specified its action in vitro. SoxYZ unlike the other Sox proteins is inactivated upon reduction. When the Sox system is reconstituted with inactivated SoxYZ, the thiosulfate-oxidizing activity is drastically decreased. SoxF reverses this inactivation and may mediate a conformational change of SoxYZ possibly by a transient interprotein disulfide. The membrane protein SoxV and the thioredoxin SoxS are essential for chemotrophic growth as evident from homogenote mutants defective in these proteins. Evidence is presented that both proteins transfer reductant from the cytoplasm to the periplasm and that SoxYZ is the final target of this transfer to balance the redox state of the Sox enzyme system or reduce a SoxY..Y interprotein disulfide.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Arnesano F, Banci L, Bertini I, Mangani S, Thompsett AR (2003) A redox switch in CopC: an intriguing copper trafficking protein that binds copper(I) and copper(II) at different sites. Proc Natl Acad Sci USA 100:3814–3819.
Bamford VA, Bruno S, Rasmussen T, Appia-Ayme C, Cheesman MR, Berks BC, Hemmings AM (2002) Structural basis for the oxidation of thiosulfate by a sulfur cycle enzyme. EMBO J 21:5599–5610.
Bardischewsky F, Friedrich CG (2001) Identification of ccdA in Paracoccus pantotrophus GB17: disruption of ccdA causes complete deficiency in c-type cytochromes. J Bacteriol 183:257–263.
Bardischewsky F, Quentmeier A, Rother D, Hellwig P, Kostka S, Friedrich CG (2005) Sulfur dehydrogenase of Paracoccus pantotrophus: the heme-2 domain of the molybdoprotein cytochrome c complex is dispensable for catalytic activity. Biochemistry 44:7024–7034.
Bardischewsky F, Fischer J, Höller B, Friedrich CG (2006a) SoxV transfers electrons to the periplasm of Paracoccus pantotrophus–an essential reaction for chemotrophic sulfur oxidation. Microbiology 152:465–472.
Bardischewsky F, Quentmeier A, Friedrich CG (2006b) The flavoprotein SoxF functions in chemotrophic thiosulfate oxidation of Paracoccus pantotrophus in vivo and in vitro. FEMS Microbiol Lett 258:121–126.
Brune D (1989) Sulfur oxidation by phototrophic bacteria. Biochim Biophys Acta 975:189–221.
Cusanovich MA, Meyer TE, Bartsch RG (1991) Flavocytochrome c. In: Müller F (ed) Chemistry and biochemistry of flavoenzymes. CRC, Boca Raton, pp 377–399.
Dahl C, Engels S, Pott-Sperling AS, Schulte A, Sander A, 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.
Dambe T, Quentmeier A, Rother D, Friedrich CG, Scheidig AJ (2005) Structure of the cytochrome complex SoxXA of Paracoccus pantotrophus, a heme enzyme initiating chemotrophic sulfur oxidation. J Struct Biol 152:229–234.
Fabianek RA, Hennecke H, Thöny-Meyer L (2000) Periplasmic protein thiol:disulfide oxidoreductases of Escherichia coli. FEMS Microbiol Rev 24:303–316.
Friedrich CG (1998) Physiology and genetics of sulfur-oxidizing bacteria. Adv Microbial Physiol 39:235–289.
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.
Friedrich CG, Bardischewsky F, Rother D, Quentmeier A, Fischer J (2005) Prokaryotic sulfur oxidation. Curr Opin Microbiol 8:253–259.
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 53:941–951.
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.
Kelly DP, Shergill LK, Lu W-P, Wood AP (1997) Oxidative metabolism of inorganic sulfur compounds by bacteria. Antonie Van Leeuwenhoek 71:95–107.
Kostanjevecki V, Brige A, Meyer TE, Cusanovich MA, Guisez Y, van Beeumen JJ (2000) A membrane-bound flavocytochrome c-sulfide dehydrogenase from the phototrophic purple sulfur bacterium Ectothiorhodospira vacuolata. J Bacteriol 182:3097–103.
Kusai A, Yamanaka T (1973) Cytochrome c (553, Chlorobium thiosulfatophilum) is a sulfide-cytochrome c reductase. FEBS Lett 34:235–237.
Lee C, Lee SM, Mukhopadhyay P, Kim SJ, Lee SC, Ahn W-S, Yu M-H, Storz G, Ryu SE (2004) Redox regulation of OxyR requires specific disulfide bond formation involving a rapid kinetic reaction path. Nat Struct Mol Biol 11:1179–1185.
Ludwig W, Mittenhuber G, Friedrich CG (1993) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Int J Syst Bacteriol 43:363–367.
Pattaragulwanit K, Brune DC, Trüper HG, Dahl C (1998) Molecular genetic evidence for cytoplasmic localization of sulfur globules in Chromatium vinosum. Arch Microbiol 169:434–444.
Quentmeier A, Friedrich CG (2001) The cysteine residue of the SoxY protein as the active site of protein-bound sulfur oxidation of Paracoccus pantotrophus GB17. FEBS Lett 503:168–172.
Quentmeier A, Hellwig P, Bardischewsky F, Grelle G, Kraft R, Friedrich CG (2003) Sulfur oxidation in Paracoccus pantotrophus: interaction of the sulfur-binding protein SoxYZ with the dimanganese SoxB protein. Biochem Biophys Res Comm 312:1011–1018.
Quentmeier A, Hellwig P, Bardischewsky F, Wichmann R, Friedrich CG (2004) Sulfide dehydrogenase activity of the monomeric flavoprotein SoxF of Paracoccus pantotrophus. Biochemistry 43:14696–14703.
Rainey FA, Kelly DP, Stackebrandt E, Burghardt J, Hiraishi A, Katayama Y, Wood AP (1999) A re-evaluation of the taxonomy of Paracoccus denitrificans and a proposal for the combination Paracoccus pantotrophus comb. nov. Int J Syst Bacteriol 49:645–651.
Range K, Ayala I, York D, Barry BA (2006) Normal modes of redox-active tyrosine: conformation dependence and comparison to experiment. J Phys Chem 110:10970–10981.
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.
Ritz D, Beckwith J (2001) Roles of thiol-redox pathways in bacteria. Annu Rev Microbiol 55:21–48.
Robertson LA, Kuenen JG (1983) Thiosphaera pantotropha gen. nov. sp. nov.: a facultatively anaerobic, facultatively autotrophic sulfur bacterium. J Gen Microbiol 129:2847–2855.
Rother D, Henrich H-J, Quentmeier A, Bardischewsky F, 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 183:4499–4508.
Rother D, Orawski G, Bardischewsky F, Friedrich CG (2005) SoxRS mediated regulation of chemotrophic sulfur oxidation in Paracoccus pantotrophus. Microbiology 151:1707–1716.
Sambongi Y, Ferguson SJ (1994) Specific thiol compounds complement deficiency in c-type cytochrome biogenesis in Escherichia coli carrying a mutation in a membrane-bound disulphide isomerise-like protein. FEBS Lett 353:235–238.
Swenson RP, Kasim M, Bradley LH, Druhan LJ (1999) Role of conformational dynamics and associated electrostatic and hydrogen bonding interactions in the regulation of redox potentials in the Clostridium beijerinckii flavodoxin. In: Ghisla S, Kroneck P, Macheroux P, Sund H (eds) Flavins and flavoproteins. Agency for Scientific Publications, Berlin, pp183–186.
Takano T, Dickerson RE (1980) Redox conformation changes in refined Tuna cytochrome. Proc Natl Acad Sci 77:6371–6375.
Visser JM, de Jong GAH, Robertson LA, Kuenen JG (1997) A novel membrane-bound flavocytochrome c sulfide dehydrogenase from the colorless sulfur bacterium Thiobacillus sp. W5. Arch Microbiol 167:295–301.
Wodara C, Bardischewsky F, Friedrich CG (1997) Cloning and characterization of sulfite dehydrogenase, two c-type cytochromes, and a flavoprotein of Paracoccus denitrificans GB17: essential role of sulfite dehydrogenase in lithotrophic sulfur oxidation. J Bacteriol 179:5014–5023.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2008 Springer-Verlag Berlin Heidelberg
About this paper
Cite this paper
Friedrich, C.G. et al. (2008). Redox Control of Chemotrophic Sulfur Oxidation of Paracoccus pantotrophus. In: Dahl, C., Friedrich, C.G. (eds) Microbial Sulfur Metabolism. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-72682-1_12
Download citation
DOI: https://doi.org/10.1007/978-3-540-72682-1_12
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-72679-1
Online ISBN: 978-3-540-72682-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)