Skip to main content
Log in

Sulfite-oxidizing enzymes

  • Minireview
  • Published:
JBIC Journal of Biological Inorganic Chemistry Aims and scope Submit manuscript

Abstract

Sulfite-oxidizing enzymes (SOEs) are molybdenum enzymes that exist in almost all forms of life where they carry out important functions in protecting cells and organisms against sulfite-induced damage. Due to their nearly ubiquitous presence in living cells, these enzymes can be assumed to be evolutionarily ancient, and this is reflected in the fact that the basic domain architecture and fold structure of all sulfite-oxidizing enzymes studied so far are similar. The Mo centers of all SOEs have five-coordinate square pyramidal coordination geometry, which incorporates a pyranopterin dithiolene cofactor. However, significant differences exist in the quaternary structure of the enzymes, as well as in the kinetic properties and the nature of the electron acceptors used. In addition, some SOEs also contain an integral heme group that participates in the overall catalytic cycle. Catalytic turnover involves the paramagnetic Mo(V) oxidation state, and EPR spectroscopy, especially high-resolution pulsed EPR spectroscopy, provides detailed information about the molecular and electronic structure of the Mo center and the Mo-based sulfite oxidation reaction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

CSO:

Chicken sulfite oxidase

CW EPR:

Continuous wave electron paramagnetic resonance

Cyt c :

Cytochrome c

DFT:

Density functional theory

ESE:

Electron spin echo

ESEEM:

Electron spin echo envelope modulation

HSO:

Human sulfite oxidase

IET:

Intramolecular electron transfer

PPT:

Pyranopterin dithiolene

PSO:

Plant sulfite oxidase

SDH:

Sulfite dehydrogenase

SO:

Sulfite oxidase

SOE:

Sulfite-oxidizing enzyme

SorAB:

SorAB sulfite dehydrogenase from Starkeya novella

SorT:

SorT sulfite dehydrogenase from Sinorhizobium meliloti

SorU:

c-type cytochrome, natural electron acceptor for SorT

SUOX:

Sulfite oxidase

References

  1. Frausto da Silva JJR, Williams RJP (2001) The biological chemistry of the elements—the inorganic chemistry of life. Oxford University Press, Oxford

    Google Scholar 

  2. Kappler U (2011) Biochim Biophys Acta 1807:1–10

    Article  CAS  PubMed  Google Scholar 

  3. Rajagopalan KV, Coughlan MP (1980) Molybdenum and molybdenum-containing enzymes. Pergamon Press, Oxford, pp 243–272

    Google Scholar 

  4. Hille R, Hall J, Basu P (2014) Chem Rev 114:3963–4038

    Article  CAS  PubMed  Google Scholar 

  5. Di Salle A, D’Errico G, La Cara F, Cannio R, Rossi M (2006) Extremophiles 10:587–598

    Article  PubMed  Google Scholar 

  6. Kappler U, Bennett B, Rethmeier J, Schwarz G, Deutzmann R, McEwan AG, Dahl C (2000) J Biol Chem 275:13202–13212

    Article  CAS  PubMed  Google Scholar 

  7. Wilson JJ, Kappler U (2009) Biochim Biophys Acta 1787:1516–1525

    Article  CAS  PubMed  Google Scholar 

  8. Denger K, Weinitschke S, Smits THM, Schleheck D, Cook AM (2008) Microbiology 154:256–263

    Article  CAS  PubMed  Google Scholar 

  9. Myers JD, Kelly DJ (2005) Microbiology 151:233–242

    Article  CAS  PubMed  Google Scholar 

  10. Lyric RM, Suzuki I (1969) Can J Biochem 48:334–343

    Article  Google Scholar 

  11. Charles AM, Suzuki I (1965) Biochem Biophys Res Comm 19:686–690

    Article  CAS  PubMed  Google Scholar 

  12. D’Errico G, Di Salle A, La Cara F, Rossi M, Cannio R (2006) J Bacteriol 188:694–701

    Article  PubMed Central  PubMed  Google Scholar 

  13. Low L, Kilmartin JR, Bernhardt PV, Kappler U (2011) Front Microbiol 2:58. doi:10.3389/fmicb.2011.00058

  14. Robin S, Arese M, Forte E, Sarti P, Giuffre A, Soulimane T (2011) J Bacteriol 193:3988–3997

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Eilers T, Schwarz G, Brinkmann H, Witt C, Richter T, Nieder J, Koch B, Hille R, Hänsch R, Mendel RR (2001) J Biol Chem 276:46989–46994

    Article  CAS  PubMed  Google Scholar 

  16. Leustek T, Saito K (1999) Plant Physiol 120:637–644

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Schwarz G, Mendel RR (2006) Annu Rev Plant Biol 57:623–647

    Article  CAS  PubMed  Google Scholar 

  18. Byrne RS, Hänsch R, Mendel RR, Hille R (2009) J Biol Chem 284:35479–35484

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Cohen HJ, Becher-Lange S, Kessler DL, Rajagopalan KV (1972) J Biol Chem 247:7759–7766

    CAS  PubMed  Google Scholar 

  20. Griffith OW (1987) Methods Enzymol 143:366–376

    Article  CAS  PubMed  Google Scholar 

  21. Johnson JL (2003) Prenatal Diagn 23:6–8

    Article  CAS  Google Scholar 

  22. Dublin AB, Hald JK, Wootton-Gorges SL (2002) AJNR Am J Neuroradiol 23:484–485

    PubMed  Google Scholar 

  23. Sass JO, Gunduz A, Araujo Rodrigues Funayama C, Korkmaz B, Dantas Pinto KG, Tuysuz B, Yanasse Dos Santos L, Taskiran E, de Fátima Turcato M, Lam C-W, Reiss J, Walter M, Yalcinkaya C, Camelo Junior JS (2010) Brain Dev 32:544–549

  24. Leimkuehler S, Wuebbens MM, Rajagopalan KV (2011) Coord Chem Rev 255:1129–1144

    Article  CAS  Google Scholar 

  25. Mendel RR (2013) J Biol Chem 288:13165–13172

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Johnson JL, Coyne KE, Garrett RM, Zabot M-T, Dorche C, Kisker C, Rajagopalan KV (2002) Hum Mutat 20:74–79

    Article  PubMed  Google Scholar 

  27. Kappler U (2008) Microbial sulfur metabolism. Springer, Berlin, pp 151–169

    Book  Google Scholar 

  28. Workun GJ, Moquin K, Rothery RA, Weiner JH (2008) Microbiol Mol Biol Rev 72:228–248

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Schrader N, Fischer K, Theis K, Mendel RR, Schwarz G, Kisker C (2003) Structure 11:1251–1263

    Article  CAS  PubMed  Google Scholar 

  30. Wilson HL, Wilkinson SR, Rajagopalan KV (2006) Biochemistry 45:2149–2160

    Article  CAS  PubMed  Google Scholar 

  31. Kisker C, Schindelin H, Pacheco A, Wehbi WA, Garrett RM, Rajagopalan KV, Enemark JH, Rees DC (1997) Cell 91:973–983

    Article  CAS  PubMed  Google Scholar 

  32. Pacheco A, Hazzard JT, Tollin G, Enemark JH (1999) J Biol Inorg Chem 4:390–401

    Article  CAS  PubMed  Google Scholar 

  33. Southerland WM, Rajagopalan KV (1978) J Biol Chem 253:8753–8758

    CAS  PubMed  Google Scholar 

  34. Southerland WM, Winge DR, Rajagopalan KV (1978) J Biol Chem 253:8747–8752

    CAS  PubMed  Google Scholar 

  35. Feng CJ, Kedia RV, Hazzard JT, Hurley JK, Tollin G, Enemark JH (2002) Biochemistry 41:5816–5821

    Article  CAS  PubMed  Google Scholar 

  36. Johnson-Winters K, Nordstrom AR, Emesh S, Astashkin AV, Rajapakshe A, Berry RE, Tollin G, Enemark JH (2010) Biochemistry 49:1290–1296

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. Kappler U, Bailey S (2005) J Biol Chem 280:24999–25007

    Article  CAS  PubMed  Google Scholar 

  38. Utesch T, Mroginski MA (2010) J Phys Chem Lett 1:2159–2164

    Article  CAS  Google Scholar 

  39. Reichenbecher W, Kelly DP, Murrell JC (1999) Arch Microbiol 172:387–392

    Article  CAS  PubMed  Google Scholar 

  40. McGrath AP, Laming EM, Guss JM, Trewhella J, Calmes B, Bernhardt PV, Hanson GR, Kappler U, Maher MJ submitted

  41. Brody MS, Hille R (1999) Biochemistry 38:6668–6677

    Article  CAS  PubMed  Google Scholar 

  42. Qiu JA, Wilson HL, Rajagopalan KV (2012) Biochemistry 51:1134–1147

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  43. Wilson HL, Rajagopalan KV (2004) J Biol Chem 279:15105–15113

    Article  CAS  PubMed  Google Scholar 

  44. Kalimuthu P, Heath MD, Santini JM, Kappler U, Bernhardt PV (2014) Biochim Biophys Acta 1837:112–120

    Article  CAS  PubMed  Google Scholar 

  45. Rapson TD, Kappler U, Hanson GR, Bernhardt PV (2011) Biochim Biophys Acta 1807:108–118

    Article  CAS  PubMed  Google Scholar 

  46. Bailey S, Rapson T, Winters-Johnson K, Astashkin AV, Enemark JH, Kappler U (2009) J Biol Chem 284:2053–2063

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Hänsch R, Lang C, Riebeseel E, Lindigkeit R, Gessler A, Rennenberg H, Mendel RR (2006) J Biol Chem 281:6884–6888

    Article  PubMed  Google Scholar 

  48. Hemann C, Hood BL, Fulton M, Hänsch R, Schwarz G, Mendel RR, Kirk ML, Hille R (2005) J Am Chem Soc 127:16567–16577

    Article  CAS  PubMed  Google Scholar 

  49. Feng C, Wilson HL, Hurley JK, Hazzard JT, Tollin G, Rajagopalan KV, Enemark JH (2003) Biochemistry 42:12235–12242

    Article  CAS  PubMed  Google Scholar 

  50. Spence JT, Kipke CA, Enemark JH, Sunde RA (1991) Inorg Chem 30:3011–3015

    Article  CAS  Google Scholar 

  51. Feng C, Wilson HL, Hurley JK, Hazzard JT, Tollin G, Rajagopalan KV, Enemark JH (2003) J Biol Chem 278:2913

    Article  CAS  PubMed  Google Scholar 

  52. Feng CJ, Kappler U, Tollin G, Enemark JH (2003) J Am Chem Soc 125:14696–14697

    Article  CAS  PubMed  Google Scholar 

  53. Bar-Even A, Noor E, Savir Y, Liebermeister W, Davidi D, Tawfik DS, Milo R (2011) Biochemistry 50:4402–4410

    Article  CAS  PubMed  Google Scholar 

  54. Belaidi AA, Roeper J, Krizowski S, Schwarz G (2014) submitted for publication

  55. Hille R (1994) Biochim Biophys Acta 1184:143–169

    Article  CAS  PubMed  Google Scholar 

  56. Enemark JH, Astashkin AV, Raitsimring AM (2006) Dalton Trans 29:3501–3514

  57. Klein EL, Belaidi AA, Raitsimring AM, Davis AC, Krämer T, Astashkin AV, Neese F, Schwarz G, Enemark JH (2014) Inorg Chem 53:961–971

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  58. Mabbs FE, Collison D (1992) Electron paramagnetic resonance of d transition metal complexes. Elsevier, Amsterdam

    Google Scholar 

  59. Klein EL, Astashkin AV, Raitsimring AM, Enemark JH (2013) Coord Chem Rev 257:110–118

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  60. Astashkin AV, Johnson-Winters K, Klein EL, Byrne RS, Hille R, Raitsimring AM, Enemark JH (2007) J Am Chem Soc 129:14800–14810

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  61. Cohen HJ, Fridovich I, Rajagopalan KV (1971) J Biol Chem 246:374–382

    CAS  PubMed  Google Scholar 

  62. Lamy MT, Gutteridge S, Bray RC (1980) Biochem J 185:397–403

    PubMed Central  CAS  PubMed  Google Scholar 

  63. Bray RC, Lamy MT, Gutteridge S, Wilkinson T (1982) Biochem J 201:241–243

    PubMed Central  CAS  PubMed  Google Scholar 

  64. Astashkin AV, Mader ML, Pacheco A, Enemark JH, Raitsimring AM (2000) J Am Chem Soc 122:5294–5302

    Article  CAS  Google Scholar 

  65. Bray RC, Gutteridge S, Lamy MT, Wilkinson T (1983) Biochem J 211:227–236

    PubMed Central  CAS  PubMed  Google Scholar 

  66. Doonan CJ, Wilson HL, Bennett B, Prince RC, Rajagopalan KV, George GN (2008) Inorg Chem 47:2033–2038

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  67. Astashkin AV, Klein EL, Enemark JH (2007) J Inorg Biochem 101:1623–1629

    Article  CAS  PubMed  Google Scholar 

  68. Klein EL, Astashkin AV, Ganyushin D, Riplinger C, Johnson-Winters K, Neese F, Enemark JH (2009) Inorg Chem 48:4743–4752

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  69. George GN (1985) J Magn Reson 64:384–394

    CAS  Google Scholar 

  70. Raitsimring AM, Kappler U, Feng CJ, Astashkin AV, Enemark JH (2005) Inorg Chem 44:7283–7285

    Article  CAS  PubMed  Google Scholar 

  71. Sullivan EP, Hazzard JT, Tollin G, Enemark JH (1992) J Am Chem Soc 114:9662–9663

    Article  CAS  Google Scholar 

  72. Pacheco A, Basu P, Borbat P, Raitsimring AM, Enemark JH (1996) Inorg Chem 35:7001–7008

    Article  CAS  PubMed  Google Scholar 

  73. Astashkin AV, Hood BL, Feng CJ, Hille R, Mendel RR, Raitsimring AM, Enemark JH (2005) Biochemistry 44:13274–13281

    Article  CAS  PubMed  Google Scholar 

  74. Astashkin AV, Johnson-Winters K, Klein EL, Feng CJ, Wilson HL, Rajagopalan KV, Raitsimring AK, Enemark JH (2008) J Am Chem Soc 130:8471–8480

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  75. Rajapakshe A, Johnson-Winters K, Nordstrom AR, Meyers KT, Emesh S, Astashkin AV, Enemark JH (2010) Biochemistry 49:5154–5159

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  76. Rapson TD, Astashkin AV, Johnson-Winters K, Bernhardt PV, Kappler U, Raitsimring AM, Enemark JH (2010) J Biol Inorg Chem 15:505–514

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  77. Klein EL, Raitsimring AM, Astashkin AV, Rajapakshe A, Johnson-Winters K, Arnold AR, Potapov A, Goldfarb D, Enemark JH (2012) Inorg Chem 51:1408–1418

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  78. Kappler U, Bailey S, Feng CJ, Honeychurch MJ, Hanson GR, Bernhardt PV, Tollin G, Enemark JH (2006) Biochemistry 45:9696–9705

    Article  CAS  PubMed  Google Scholar 

  79. Raitsimring AM, Astashkin AV, Feng C, Wilson HL, Rajagopalan KV, Enemark JH (2008) Inorg Chim Acta 361:941–946

    Article  CAS  Google Scholar 

  80. Dahl C (1996) Microbiology 142:3363–3372

    Article  CAS  PubMed  Google Scholar 

  81. Lenk S, Moraru C, Hahnke S, Arnds J, Richter M, Kube M, Reinhardt R, Brinkhoff T, Harder J, Amann R, Mussmann M (2012) ISME J 6:2178–2187

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  82. Moran MA, Belas R, Schell MA, Gonzalez JM, Sun F, Sun S, Binder BJ, Edmonds J, Ye W, Orcutt B, Howard EC, Meile C, Palefsky W, Goesmann A, Ren Q, Paulsen I, Ulrich LE, Thompson LS, Saunders E, Buchan A (2007) Appl Environ Microbiol 73:4559–4569

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  83. Wagner-Döbler I, Biebl H (2006) Annu Rev Microbiol 60:255–280

    Article  PubMed  Google Scholar 

  84. Buchan A, Gonzalez JM, Moran MA (2005) Appl Environ Microbiol 71:5665–5677

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  85. Dahl C, Franz B, Hensen D, Kesselheim A, Zigann R (2013) Microbiology 159:2626–2638

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

JHE gratefully acknowledges many years of financial support from NIGMS for research on molybdenum enzymes (Grant GM-037773). We thank A. Belaidi and G. Schwarz for a preprint of Ref. [54] and Dr. Megan Maher for help with the preparation of Figs. 1 and 3 and for a preprint of Ref. [40].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ulrike Kappler.

Additional information

Responsible Editors: José Moura and Paul Bernhardt.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 72 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kappler, U., Enemark, J.H. Sulfite-oxidizing enzymes. J Biol Inorg Chem 20, 253–264 (2015). https://doi.org/10.1007/s00775-014-1197-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00775-014-1197-3

Keywords

Navigation