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.
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
Frausto da Silva JJR, Williams RJP (2001) The biological chemistry of the elements—the inorganic chemistry of life. Oxford University Press, Oxford
Kappler U (2011) Biochim Biophys Acta 1807:1–10
Rajagopalan KV, Coughlan MP (1980) Molybdenum and molybdenum-containing enzymes. Pergamon Press, Oxford, pp 243–272
Hille R, Hall J, Basu P (2014) Chem Rev 114:3963–4038
Di Salle A, D’Errico G, La Cara F, Cannio R, Rossi M (2006) Extremophiles 10:587–598
Kappler U, Bennett B, Rethmeier J, Schwarz G, Deutzmann R, McEwan AG, Dahl C (2000) J Biol Chem 275:13202–13212
Wilson JJ, Kappler U (2009) Biochim Biophys Acta 1787:1516–1525
Denger K, Weinitschke S, Smits THM, Schleheck D, Cook AM (2008) Microbiology 154:256–263
Myers JD, Kelly DJ (2005) Microbiology 151:233–242
Lyric RM, Suzuki I (1969) Can J Biochem 48:334–343
Charles AM, Suzuki I (1965) Biochem Biophys Res Comm 19:686–690
D’Errico G, Di Salle A, La Cara F, Rossi M, Cannio R (2006) J Bacteriol 188:694–701
Low L, Kilmartin JR, Bernhardt PV, Kappler U (2011) Front Microbiol 2:58. doi:10.3389/fmicb.2011.00058
Robin S, Arese M, Forte E, Sarti P, Giuffre A, Soulimane T (2011) J Bacteriol 193:3988–3997
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
Leustek T, Saito K (1999) Plant Physiol 120:637–644
Schwarz G, Mendel RR (2006) Annu Rev Plant Biol 57:623–647
Byrne RS, Hänsch R, Mendel RR, Hille R (2009) J Biol Chem 284:35479–35484
Cohen HJ, Becher-Lange S, Kessler DL, Rajagopalan KV (1972) J Biol Chem 247:7759–7766
Griffith OW (1987) Methods Enzymol 143:366–376
Johnson JL (2003) Prenatal Diagn 23:6–8
Dublin AB, Hald JK, Wootton-Gorges SL (2002) AJNR Am J Neuroradiol 23:484–485
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
Leimkuehler S, Wuebbens MM, Rajagopalan KV (2011) Coord Chem Rev 255:1129–1144
Mendel RR (2013) J Biol Chem 288:13165–13172
Johnson JL, Coyne KE, Garrett RM, Zabot M-T, Dorche C, Kisker C, Rajagopalan KV (2002) Hum Mutat 20:74–79
Kappler U (2008) Microbial sulfur metabolism. Springer, Berlin, pp 151–169
Workun GJ, Moquin K, Rothery RA, Weiner JH (2008) Microbiol Mol Biol Rev 72:228–248
Schrader N, Fischer K, Theis K, Mendel RR, Schwarz G, Kisker C (2003) Structure 11:1251–1263
Wilson HL, Wilkinson SR, Rajagopalan KV (2006) Biochemistry 45:2149–2160
Kisker C, Schindelin H, Pacheco A, Wehbi WA, Garrett RM, Rajagopalan KV, Enemark JH, Rees DC (1997) Cell 91:973–983
Pacheco A, Hazzard JT, Tollin G, Enemark JH (1999) J Biol Inorg Chem 4:390–401
Southerland WM, Rajagopalan KV (1978) J Biol Chem 253:8753–8758
Southerland WM, Winge DR, Rajagopalan KV (1978) J Biol Chem 253:8747–8752
Feng CJ, Kedia RV, Hazzard JT, Hurley JK, Tollin G, Enemark JH (2002) Biochemistry 41:5816–5821
Johnson-Winters K, Nordstrom AR, Emesh S, Astashkin AV, Rajapakshe A, Berry RE, Tollin G, Enemark JH (2010) Biochemistry 49:1290–1296
Kappler U, Bailey S (2005) J Biol Chem 280:24999–25007
Utesch T, Mroginski MA (2010) J Phys Chem Lett 1:2159–2164
Reichenbecher W, Kelly DP, Murrell JC (1999) Arch Microbiol 172:387–392
McGrath AP, Laming EM, Guss JM, Trewhella J, Calmes B, Bernhardt PV, Hanson GR, Kappler U, Maher MJ submitted
Brody MS, Hille R (1999) Biochemistry 38:6668–6677
Qiu JA, Wilson HL, Rajagopalan KV (2012) Biochemistry 51:1134–1147
Wilson HL, Rajagopalan KV (2004) J Biol Chem 279:15105–15113
Kalimuthu P, Heath MD, Santini JM, Kappler U, Bernhardt PV (2014) Biochim Biophys Acta 1837:112–120
Rapson TD, Kappler U, Hanson GR, Bernhardt PV (2011) Biochim Biophys Acta 1807:108–118
Bailey S, Rapson T, Winters-Johnson K, Astashkin AV, Enemark JH, Kappler U (2009) J Biol Chem 284:2053–2063
Hänsch R, Lang C, Riebeseel E, Lindigkeit R, Gessler A, Rennenberg H, Mendel RR (2006) J Biol Chem 281:6884–6888
Hemann C, Hood BL, Fulton M, Hänsch R, Schwarz G, Mendel RR, Kirk ML, Hille R (2005) J Am Chem Soc 127:16567–16577
Feng C, Wilson HL, Hurley JK, Hazzard JT, Tollin G, Rajagopalan KV, Enemark JH (2003) Biochemistry 42:12235–12242
Spence JT, Kipke CA, Enemark JH, Sunde RA (1991) Inorg Chem 30:3011–3015
Feng C, Wilson HL, Hurley JK, Hazzard JT, Tollin G, Rajagopalan KV, Enemark JH (2003) J Biol Chem 278:2913
Feng CJ, Kappler U, Tollin G, Enemark JH (2003) J Am Chem Soc 125:14696–14697
Bar-Even A, Noor E, Savir Y, Liebermeister W, Davidi D, Tawfik DS, Milo R (2011) Biochemistry 50:4402–4410
Belaidi AA, Roeper J, Krizowski S, Schwarz G (2014) submitted for publication
Hille R (1994) Biochim Biophys Acta 1184:143–169
Enemark JH, Astashkin AV, Raitsimring AM (2006) Dalton Trans 29:3501–3514
Klein EL, Belaidi AA, Raitsimring AM, Davis AC, Krämer T, Astashkin AV, Neese F, Schwarz G, Enemark JH (2014) Inorg Chem 53:961–971
Mabbs FE, Collison D (1992) Electron paramagnetic resonance of d transition metal complexes. Elsevier, Amsterdam
Klein EL, Astashkin AV, Raitsimring AM, Enemark JH (2013) Coord Chem Rev 257:110–118
Astashkin AV, Johnson-Winters K, Klein EL, Byrne RS, Hille R, Raitsimring AM, Enemark JH (2007) J Am Chem Soc 129:14800–14810
Cohen HJ, Fridovich I, Rajagopalan KV (1971) J Biol Chem 246:374–382
Lamy MT, Gutteridge S, Bray RC (1980) Biochem J 185:397–403
Bray RC, Lamy MT, Gutteridge S, Wilkinson T (1982) Biochem J 201:241–243
Astashkin AV, Mader ML, Pacheco A, Enemark JH, Raitsimring AM (2000) J Am Chem Soc 122:5294–5302
Bray RC, Gutteridge S, Lamy MT, Wilkinson T (1983) Biochem J 211:227–236
Doonan CJ, Wilson HL, Bennett B, Prince RC, Rajagopalan KV, George GN (2008) Inorg Chem 47:2033–2038
Astashkin AV, Klein EL, Enemark JH (2007) J Inorg Biochem 101:1623–1629
Klein EL, Astashkin AV, Ganyushin D, Riplinger C, Johnson-Winters K, Neese F, Enemark JH (2009) Inorg Chem 48:4743–4752
George GN (1985) J Magn Reson 64:384–394
Raitsimring AM, Kappler U, Feng CJ, Astashkin AV, Enemark JH (2005) Inorg Chem 44:7283–7285
Sullivan EP, Hazzard JT, Tollin G, Enemark JH (1992) J Am Chem Soc 114:9662–9663
Pacheco A, Basu P, Borbat P, Raitsimring AM, Enemark JH (1996) Inorg Chem 35:7001–7008
Astashkin AV, Hood BL, Feng CJ, Hille R, Mendel RR, Raitsimring AM, Enemark JH (2005) Biochemistry 44:13274–13281
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
Rajapakshe A, Johnson-Winters K, Nordstrom AR, Meyers KT, Emesh S, Astashkin AV, Enemark JH (2010) Biochemistry 49:5154–5159
Rapson TD, Astashkin AV, Johnson-Winters K, Bernhardt PV, Kappler U, Raitsimring AM, Enemark JH (2010) J Biol Inorg Chem 15:505–514
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
Kappler U, Bailey S, Feng CJ, Honeychurch MJ, Hanson GR, Bernhardt PV, Tollin G, Enemark JH (2006) Biochemistry 45:9696–9705
Raitsimring AM, Astashkin AV, Feng C, Wilson HL, Rajagopalan KV, Enemark JH (2008) Inorg Chim Acta 361:941–946
Dahl C (1996) Microbiology 142:3363–3372
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
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
Wagner-Döbler I, Biebl H (2006) Annu Rev Microbiol 60:255–280
Buchan A, Gonzalez JM, Moran MA (2005) Appl Environ Microbiol 71:5665–5677
Dahl C, Franz B, Hensen D, Kesselheim A, Zigann R (2013) Microbiology 159:2626–2638
Acknowledgments
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editors: José Moura and Paul Bernhardt.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00775-014-1197-3