The bacterial SoxAX cytochromes

Cellular and Molecular Life Sciences

Volumn 70, Issue 6, 2013, Pages 977-992

  Kappler, Ulrike ^a   Maher, Megan J ^b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

Author keywords

Crystal structure; Cytochromes; Heme thiolate proteins; Redox centres; SoxAX cytochromes; Sulfur oxidation

Indexed keywords

BACTERIAL PROTEIN; COPPER; CYSTEINE; SOXA PROTEIN; SOXAX PROTEIN; SOXX PROTEIN; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG;

BACTERIAL GENE; BINDING SITE; COMPLEX FORMATION; CRYSTAL STRUCTURE; ELECTRON SPIN RESONANCE; GENETIC CODE; LIGAND BINDING; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; OXIDATION REDUCTION REACTION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REVIEW; SIGNAL TRANSDUCTION; SOXAX GENE; SULFATION;

AMINO ACID SEQUENCE; BACTERIA; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CLUSTER ANALYSIS; CYTOCHROMES; DIMERIZATION; ELECTRON SPIN RESONANCE SPECTROSCOPY; HEME; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PHYLOGENY; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION; THIOSULFATES;

BACTERIA (MICROORGANISMS);

EID: 84875221746     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-1098-y     Document Type: Review

References (55)

1. 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(21):5599-5610 (Pubitemid 35315260)
2. Lu WP, Kelly DP (1988) Respiration-driven proton translocation in Thiobacillus versutus and the role of the periplasmic thiosulphate-oxidizing enzyme system. Arch Microbiol 149:297-302
3. Omura T (2005) Heme-thiolate proteins. Biochem Biophys Res Comm 338(1):404-409 (Pubitemid 41540582)
4. Green MT (2009) CH bond activation in heme proteins: the role of thiolate ligation in cytochrome P450. Curr Opin Chem Biol 13(1):84-88
5. Pazicni S, Cherney MM, Lukat-Rodgers GS, Oliveriusova J, Rodgers KR, Kraus JP, Burstyn JN (2005) The heme of cystathionine beta-synthase likely undergoes a thermally induced redox-mediated ligand switch. Biochemistry 44(51):16785-16795 (Pubitemid 43007207)
6. Youn H, Conrad M, Chung SY, Roberts GP (2006) Roles of the heme and heme ligands in the activation of CooA, the CO-sensing transcriptional activator. Biochem Biophys Res Comm 348(2):345-350 (Pubitemid 44188579)
7. Dhawan IK, Shelver D, Thorsteinsson MV, Roberts GP, Johnson MK (1999) Probing the heme axial ligation in the CO-sensing CooA protein with magnetic circular dichroism spectroscopy. Biochemistry 38(39):12805-12813 (Pubitemid 29463276)
8. Alric J, Tsukatani Y, Yoshida M, Matsuura K, Shimada K, Hienerwadel R, Schoepp-Cothenet B, Nitschke W, Nagashima KVP, Vermeglio A (2004) Structural and functional characterization of the unusual triheme cytochrome bound to the reaction center of Rhodovulum sulfidophilum. J Biol Chem 279(25):26090-26097 (Pubitemid 38798753)
9. Grein F, Venceslau SS, Schneider L, Hildebrandt P, Todorovic S, Pereira IAC, Dahl C (2010) DsrJ, an essential part of the DsrMKJOP transmembrane complex in the purple sulfur bacterium Allochromatium vinosum, is an unusual triheme cytochrome c. Biochemistry 49(38):8290-8299
10. Grein F, Pereira IAC, Dahl C (2010) Biochemical characterization of individual components of the Allochromatium vinosum DsrMKJOP transmembrane complex aids understanding of complex function in vivo. J Bacteriol 192(24):6369-6377
11. Lu WP, Swoboda BEP, Kelly DP (1985) Properties of the thiosulphate oxidising multi-enzyme system from Thiobacillus versutus. Biochim Biophys Acta 828:116-122 (Pubitemid 15105078)
12. Lu WP, Kelly DP (1984) Properties and role of sulphite:cytochrome c oxidoreductase purified from Thiobacillus versutus. J Gen Microbiol 130:1683-1692 (Pubitemid 14058782)
13. Lu W-P, Kelly DP (1984) Purification and characterization of two essential cytochromes of the thiosulphate-oxidizing multi-enzyme system from Thiobacillus A2 (Thiobacillus versutus). Biochim Biophys Acta 765(2):106-117
14. Katayama Y, Hiraishi A, Kuraishi H (1995) Paracoccus thiocyanatus sp. nov., a new species of thiocyanate- utilizing facultative chemolithotroph, and transfer of Thiobacillus versutus to the genus Paracoccus as Paracoccus versutus comb. nov. with emendation of the genus. Microbiology 141:1469-1477
15. Kelly DP, Shergill JK, Lu WP, Wood AP (1997) Oxidative metabolism of inorganic sulfur compounds by bacteria. Antonie Van Leeuwenhoek 71(1-2):95-107 (Pubitemid 27075767)
16. Mittenhuber G, Sonomoto K, Egert M, Friedrich CG (1991) Identification of the DNA region responsible for sulfur-oxidizing ability of Thiosphaera pantotropha. J Bacteriol 173(2):7340-7344
17. Wodara C, Kostka S, Egert M, Kelly DP, Friedrich CG (1994) Identification and sequence analysis of the soxB gene essential for sulfur oxidation of Paracoccus denitrificans GB17. J Bacteriol 176:6188-6191 (Pubitemid 24313796)
18. Ludwig W, Mittenhuber G, Friedrich CG (1993) Transfer of Thiosphaera pantotropha to Paracoccus denitrificans. Int J Sys Bacteriol 43(2):363-367 (Pubitemid 23118482)
19. Quentmeier A, Li L, Friedrich CG (2008) Identification of two inactive forms of the central sulfur cycle protein SoxYZ of Paracoccus pantotrophus. FEBS Lett 582(25-26):3701-3704
20. Reijerse EJ, Sommerhalter M, Hellwig P, Quentmeier A, Rother D, Laurich C, Bothe E, Lubitz W, Friedrich CG (2007) The unusual redox properties of SoxXA, a novel c-type heme-enzyme essential for chemotrophic sulfur-oxidation of Paracoccus pantotrophus. Biochemistry 46(26):7804-7810 (Pubitemid 47016063)
21. Bardischewsky F, Quentmeier A, Friedrich CG (2006) The flavoprotein SoxF functions in chemotrophic thiosulfate oxidation of Paracoccus pantotrophus in vivo and in vitro. FEMS Microbiol Lett 258(1):121-126
22. 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(18):7024-7034 (Pubitemid 40632420)
23. Friedrich CG, Rother D, Bardischewsky F, Quentmeier A, Fischer J (2001) Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanisms? Appl Environ Microbiol 67(7):2873-2882 (Pubitemid 33644748)
24. Quentmeier A, Kraft R, Kostka S, Klockenkamper R, Friedrich CG (2000) Characterization of a new type of sulfite dehydrogenase from Paracoccus pantotrophus GB17. Arch Microbiol 173(2):117-125 (Pubitemid 30080555)
25. Rother D, Ringk J, Friedrich CG (2008) Sulfur oxidation of Paracoccus pantotrophus: the sulfur-binding protein SoxYZ is the target of the periplasmic thiol-disulfide oxidoreductase SoxS. Microbiology 154:1980-1988
26. Bardischewsky F, Fischer J, Holler B, Friedrich CG (2006) SoxV transfers electrons to the periplasm of Paracoccus pantotrophus - an essential reaction for chemotrophic sulfur oxidation. Microbiology 152:465-472 (Pubitemid 43210677)
27. Rother D, Orawski G, Bardischewsky F, Friedrich CG (2005) SoxRS-mediated regulation of chemotrophic sulfur oxidation in Paracoccus pantotrophus. Microbiology 151:1707-1716 (Pubitemid 40711815)
28. 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(1):257-263 (Pubitemid 32003131)
29. Bardischewsky F, Friedrich CG (2001) The shxVW locus is essential for oxidation of inorganic sulfur and molecular hydrogen by Paracoccus pantotrophus GB17: a novel function for lithotrophy. FEMS Microbiol Lett 202:215-220 (Pubitemid 32772838)
30. Friedrich CG, Bardischewsky F, Rother D, Quentmeier A, Fischer J (2005) Prokaryotic sulfur oxidation. Curr Opin Microbiol 8(3):253-259 (Pubitemid 40813066)
31. 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(9):2932-2945 (Pubitemid 34184624)
32. 551 from the photographic green sulfur bacterium Chlorobium limicola, strain Tassajara, reveals a novel c-type cytochrome. Biochemistry 37(30):10555-10562 (Pubitemid 28357855)
33. Frigaard NU, Dahl C, Robert KP (2008) Sulfur metabolism in phototrophic sulfur bacteria. In: Advances in Microbial Physiology, vol 54. Academic Press, pp 103-200
34. Hensen D, Sperling D, Truper HG, Brune DC, Dahl C (2006) Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum. Mol Microbiol 62(3):794-810 (Pubitemid 44571603)
35. Sauve V, Bruno S, Berks BC, Hemmings AM (2007) The SoxYZ complex carries sulfur cycle intermediates on a peptide swinging arm. J Biol Chem 282(32):23194-23204 (Pubitemid 47311913)
36. Ghosh W, Roy P (2007) Chemolithoautotrophic oxidation of thiosulfate, tetrathionate and thiocyanate by a novel rhizobacterium belonging to the genus Paracoccus. FEMS Microbiol Lett 270(1):124-131 (Pubitemid 46597352)
37. Sauve V, Roversi P, Leath KJ, Garman EF, Antrobus R, Lea SM, Berks BC (2009) Mechanism for the hydrolysis of a sulfur-sulfur bond based on the crystal structure of the thiosulfohydrolase SoxB. J Biol Chem 284(32):21707-21718
38. Zander U, Faust A, Klink BU, de Sanctis D, Panjikar S, Quentmeier A, Bardischewsky F, Friedrich CG, Scheidig AJ (2011) Structural basis for the oxidation of protein-bound sulfur by the sulfur cycle molybdohemo-enzyme sulfane dehydrogenase SoxCD. J Biol Chem 286(10):8349-8360. doi: 10.1074/jbc.M110. 193631
39. Frigaard NU, Dahl C (2009) Sulfur metabolism in phototrophic sulfur bacteria. Adv Microb Phys 54:103-200
40. Kappler U, Aguey-Zinsou KF, Hanson GR, Bernhardt PV, McEwan AG (2004) Cytochrome c551 from Starkeya novella: characterization, spectroscopic properties, and phylogeny of a diheme protein of the SoxAX family. J Biol Chem 279(8):6252-6260 (Pubitemid 38248758)
41. Ogawa T, Furusawa T, Nomura R, Seo D, Hosoya-Matsuda N, Sakurai H, Inoue K (2008) SoxAX binding protein, a novel component of the thiosulfate-oxidizing multienzyme system in the green sulfur bacterium Chlorobium tepidum. J Bacteriol 190(18):6097-6110
42. Orawski G, Bardischewsky F, Quentmeier A, Rother D, Friedrich CG (2007) The periplasmic thioredoxin SoxS plays a key role in activation in vivo of chemotrophic sulfur oxidation of Paracoccus pantotrophus. Microbiology 153:1081-1086 (Pubitemid 46605805)
43. Gregersen LH, Bryant DA, Frigaard N-U (2011) Mechanisms and evolution of oxidative sulfur metabolism in green sulfur bacteria. Frontiers Microbiol 2:116. doi: 10.3389/fmicb.2011.00116
44. Sakurai H, Ogawa T, Shiga M, Inoue K (2010) Inorganic sulfur oxidizing system in green sulfur bacteria. Photosynth Res 104(2-3):163-176. doi: 10.1007/s11120-010-9531-2
45. Kilmartin JR, Maher MJ, Krusong K, Noble CJ, Hanson GR, Bernhardt PV, Riley MJ, Kappler U (2011) Insights into structure and function of the active site of SoxAX cytochromes. J Biol Chem 286(28):24872-24881
46. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739
47. Rother D, Henrich HJ, 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(15):4499-4508 (Pubitemid 32645999)
48. Dambe T, Quentmeier A, Rother D, Friedrich C, Scheidig AJ (2005) Structure of the cytochrome complex SoxXA of Paracoccus pantotrophus, a heme enzyme initiating chemotrophic sulfur oxidation. J Struct Biol 152(3):229-234 (Pubitemid 41785520)
49. Friedrich CG, Quentmeier A, Bardischewsky F, Rother D, Kraft R, Kostka S, Prinz H (2000) Novel genes coding for lithotrophic sulfur oxidation of Paracoccus pantotrophus GB17. J Bacteriol 182(17):4677-4687 (Pubitemid 30641786)
50. Kappler U, Bernhardt PV, Kilmartin J, Riley MJ, Teschner J, McKenzie KJ, Hanson GR (2008) SoxAX cytochromes, a new type of heme copper protein involved in bacterial energy generation from sulfur compounds. J Biol Chem 283(32):22206-22214
51. Frausto da Silva JJR, Williams RJP (2001) The biological chemistry of the elements - the inorganic chemistry of life. Oxford University Press, Oxford
52. Cheesman MR, Little PJ, Berks BC (2001) Novel heme ligation in a c-type cytochrome involved in thiosulfate oxidation: EPR and MCD of SoxAX from Rhodovulum sulfidophilum. Biochemistry 40:10562-10569 (Pubitemid 32816666)
53. Kappler U, Hanson GR, Jones A, McEwan AG (2005) A recombinant diheme SoxAX cytochrome-implications for the relationship between EPR signals and modified heme-ligands. FEBS Lett 579:2491-2498 (Pubitemid 40569527)
54. Welte C, Hafner S, Kratzer C, Quentmeier A, Friedrich CG, Dahl C (2009) Interaction between Sox proteins of two physiologically distinct bacteria and a new protein involved in thiosulfate oxidation. FEBS Lett 583(8):1281-1286
55. Multhaup G, Schlicksupp A, Hesse L, Beher D, Ruppert T, Masters CL, Beyreuther K (1996) The amyloid precursor protein of Alzheimer's disease in the reduction of copper(II) to copper(I). Science 271(5254):1406-1409 (Pubitemid 26089474)