Tuning of functional heme reduction potentials in Shewanella fumarate reductases

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1787, Issue 2, 2009, Pages 113-120

  Pessanha, Miguel ^a   Rothery, Emma L ^b   Miles, Caroline S ^b   Reid, Graeme A ^b   Chapman, Stephen K ^b   Louro, Ricardo O ^c   Turner, David L ^c,d   Salgueiro, Carlos A ^a   Xavier, António V ^c  

^a DEPARTAMENTO DE QUÍMICA   (Portugal)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^d UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Electrostatic interaction; Fumarate; Heme; NMR; Redox; Respiratory enzyme

Indexed keywords

FUMARATE REDUCTASE; HEME;

ARTICLE; CONTROLLED STUDY; ELECTRICITY; ELECTRON TRANSPORT; ENZYME ACTIVE SITE; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; REDUCTION; SHEWANELLA; SHEWANELLA FRIGIDIMARINA; SHEWANELLA ONEIDENSIS; THERMODYNAMICS;

CATALYTIC DOMAIN; CYTOCHROME C GROUP; ELECTRONS; HEME; HYDROGEN-ION CONCENTRATION; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; OXIDATION-REDUCTION; PROTEIN BINDING; SHEWANELLA; SOLUBILITY; SUCCINATE DEHYDROGENASE; THERMODYNAMICS;

SHEWANELLA; SHEWANELLA FRIGIDIMARINA; SHEWANELLA ONEIDENSIS;

EID: 58649111025     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2008.11.007     Document Type: Article

References (53)

1. Nealson K.H., Belz A., and McKee B. Breathing metals as a way of life: geobiology in action. Antonie Van Leeuwenhoek 81 (2002) 215-222
2. 3 from Shewanella frigidimarina NCIMB400. Biochemistry 38 (1999) 3302-3309
3. Leys D., Tsapin A.S., Nealson K.H., Meyer T.E., Cusanovich M.A., and Van Beeumen J.J. Structure and mechanism of the flavocytochrome c fumarate reductase of Shewanella putrefaciens MR-1. Nat. Struct. Biol. 6 (1999) 1113-1117
4. Taylor P., Pealing S.L., Reid G.A., Chapman S.K., and Walkinshaw M.D. Structural and mechanistic mapping of a unique fumarate reductase. Nat. Struct Biol. 6 (1999) 1108-1112
5. Lemos R.S., Fernandes A.S., Pereira M.M., Gomes C.M., and Teixeira M. Quinol:fumarate oxidoreductases and succinate:quinone oxidoreductases: phylogenetic relationships, metal centres and membrane attachment. Biochim. Biophys. Acta 1553 (2002) 158-170
6. Iverson T.M., Luna-Chavez C., Cecchini G., and Rees D.C. Structure of the Escherichia coli fumarate reductase respiratory complex. Science 284 (1999) 1961-1966
7. Lancaster C.R., Kroger A., Auer M., and Michel H. Structure of fumarate reductase from Wolinella succinogenes at 2.2 Å resolution. Nature 402 (1999) 377-385
8. Kortner C., Lauterbach F., Tripier D., Unden G., and Kroger A. Wolinella succinogenes fumarate reductase contains a dihaem cytochrome b. Mol. Microbiol. 4 (1990) 855-860
9. Ohnishi T., Moser C.C., Page C.C., Dutton P.L., and Yano T. Simple redox-linked proton-transfer design: new insights from structures of quinol-fumarate reductase. Structure 8 (2000) R23-32
10. Morris C.J., Black A.C., Pealing S.L., Manson F.D., Chapman S.K., Reid G.A., Gibson D.M., and Ward F.B. Purification and properties of a novel cytochrome: flavocytochrome c from Shewanella putrefaciens. Biochem. J. 302 (1994) 587-593
11. Schwalb C., Chapman S.K., and Reid G.A. The membrane-bound tetrahaem c-type cytochrome CymA interacts directly with the soluble fumarate reductase in Shewanella. Biochem. Soc. Trans. 30 (2002) 658-662
12. Schwalb C., Chapman S.K., and Reid G.A. The tetraheme cytochrome CymA is required for anaerobic respiration with dimethyl sulfoxide and nitrite in Shewanella oneidensis. Biochemistry 42 (2003) 9491-9497
13. 3 fumarate reductase. Nat. Struct. Biol, 6 (1999) 1104-1107
14. Doherty M.K., Pealing S.L., Miles C.S., Moysey R., Taylor P., Walkinshaw M.D., Reid G.A., and Chapman S.K. Identification of the active site acid/base catalyst in a bacterial fumarate reductase: a kinetic and crystallographic study. Biochemistry 39 (2000) 10695-10701
15. Reid G.A., Miles C.S., Moysey R.K., Pankhurst K.L., and Chapman S.K. Catalysis in fumarate reductase. Biochim. Biophys. Acta 1459 (2000) 310-315
16. Mowat C.G., Moysey R., Miles C.S., Leys D., Doherty M.K., Taylor P., Walkinshaw M.D., Reid G.A., and Chapman S.K. Kinetic and crystallographic analysis of the key active site acid/base arginine in a soluble fumarate reductase. Biochemistry 40 (2001) 12292-12298
17. Pankhurst K.L., Mowat C.G., Miles C.S., Leys D., Walkinshaw M.D., Reid G.A., and Chapman S.K. Role of His505 in the soluble fumarate reductase from Shewanella frigidimarina. Biochemistry 41 (2002) 8551-8556
18. Mowat C.G., Pankhurst K.L., Miles C.S., Leys D., Walkinshaw M.D., Reid G.A., and Chapman S.K. Engineering water to act as an active site acid catalyst in a soluble fumarate reductase. Biochemistry 41 (2002) 11990-11996
19. Rothery E.L., Mowat C.G., Miles C.S., Walkinshaw M.D., Reid G.A., and Chapman S.K. Histidine 61: an important heme ligand in the soluble fumarate reductase from Shewanella frigidimarina. Biochemistry 42 (2003) 13160-13169
20. 3 heme-copper oxygen reductase from Bradyrhizobium japonicum. Biochemistry 46 (2007) 13245-13253
21. Fontecilla-Camps J.C., Volbeda A., Cavazza C., and Nicolet Y. Structure/function relationships of [NiFe]- and [FeFe]-hydrogenases. Chem. Rev. 107 (2007) 4273-4303
22. Doukov T.I., Iverson T.M., Seravalli J., Ragsdale S.W., and Drennan C.L. A Ni-Fe-Cu center in a bifunctional carbon monoxide dehydrogenase/acetyl-CoA synthase. Science 298 (2002) 567-572
23. Pealing S.L., Cheesman M.R., Reid G.A., Thomson A.J., Ward F.B., and Chapman S.K. Spectroscopic and kinetic studies of the tetraheme flavocytochrome c from Shewanella putrefaciens NCIMB400. Biochemistry 34 (1995) 6153-6158
24. Pealing S.L., Black A.C., Manson F.D., Ward F.B., Chapman S.K., and Reid G.A. Sequence of the gene encoding flavocytochrome c from Shewanella putrefaciens: a tetraheme flavoenzyme that is a soluble fumarate reductase related to the membrane-bound enzymes from other bacteria. Biochemistry 31 (1992) 12132-12140
25. 3, the soluble fumarate reductase from Shewanella NCIMB400. Biochem. Soc. Trans. 26 (1998) 418-421
26. Jones A.K., Camba R., Reid G.A., Chapman S.K., and Armstrong F.A. Interruption and time-resolution of catalysis by a flavoenzyme using fast scan protein film voltammetry. J. Am. Chem. Soc. 122 (2000) 6494-6495
27. Jeuken L.J., Jones A.K., Chapman S.K., Cecchini G., and Armstrong F.A. Electron-transfer mechanisms through biological redox chains in multicenter enzymes. J. Am. Chem. Soc. 124 (2002) 5702-5713
28. Rothery E.L., Mowat C.G., Miles C.S., Mott S., Walkinshaw M.D., Reid G.A., and Chapman S.K. Probing domain mobility in a flavocytochrome. Biochemistry 43 (2004) 4983-4989
29. 3. Eur. J. Biochem. 141 (1984) 283-296
30. 1H-NMR. FEBS Lett. 390 (1996) 59-62
31. 3 from Desulfovibrio vulgaris. Eur. J. Biochem. 241 (1996) 723-731
32. 3: the importance of mechano-chemical coupling for energy transduction. ChemBioChem 2 (2001) 831-837
33. 3 from Desulfuromonas acetoxidans. Eur. J. Biochem. 269 (2002) 5722-5730
34. Pereira P.M., Pacheco I., Turner D.L., and Louro R.O. Structure-function relationship in type II cytochrome c3 from Desulfovibrio africanus: a novel function in a familiar heme core. J. Biol. Inorg. Chem. 7 (2002) 815-822
35. 3. Biochem. J. 370 (2003) 489-495
36. + energy transduction. Biochemistry 45 (2006) 13910-13917
37. 3 from D. vulgaris Miyazaki F. Biochim. Biophys. Acta 1293 (1996) 45-54
38. Coutinho I.B., and Xavier A.V. Tetraheme cytochromes. Methods Enzymol. 243 (1994) 119-140
39. 3. J. Biol. Inorg. Chem. 12 (2007) 1-10
40. Simonneaux G., and Bondon A. Mechanism of electron transfer in heme proteins and models: the NMR approach. Chem. Rev. 105 (2005) 2627-2646
41. Correia I.J., Paquete C.M., Coelho A., Almeida C.C., Catarino T., Louro R.O., Frazao C., Saraiva L.M., Carrondo M.A., Turner D.L., and Xavier A.V. Proton-assisted two-electron transfer in natural variants of tetraheme cytochromes from Desulfomicrobium Sp. J. Biol. Chem. 279 (2004) 52227-52237
42. 2O: studies on polyaza and polyoxa-polyaza macrocycles and a general correlation. Analytica Chimica Acta 245 (1991) 271-282
43. Bartels C., Xia T., Billeter M., Güntert P., and Wüthrich K. The program XEASY for computer-supported NMR spectral analysis of biological macromolecules. J. Biomol. NMR 6 (1995) 1-10
44. Turner D.L. Obtaining ligand geometries from paramagnetic shifts in low-spin haem proteins. J. Biol. Inorg. Chem. 5 (2000) 328-332
45. 1H-nuclear-magnetic-resonance spectroscopy. Biochem. J. 294 (1993) 909-915
46. 1H NMR chemical shifts to measure the quality of protein structures. J. Mol. Biol. 247 (1995) 541-546
47. Dutton P.L. Redox potentiometry: determination of midpoint potentials of oxidation-reduction components of biological electron-transfer systems. Methods Enzymol. 54 (1978) 411-435
48. 3, Ph.D Thesis, Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Lisbon, 1998.
49. 3 from Shewanella frigidimarina probed by NMR. FEBS Lett. 578 (2004) 185-190
50. Hudson J.M., Heffron K., Kotlyar V., Sher Y., Maklashina E., Cecchini G., and Armstrong F.A. Electron transfer and catalytic control by the iron-sulfur clusters in a respiratory enzyme, E. coli fumarate reductase. J. Am. Chem. Soc. 127 (2005) 6977-6989
51. Paixão V.B., Salgueiro C.A., Brennan L., Reid G.A., Chapman S.K., and Turner D.L. Solution structure of a tetrahaem cytochrome from Shewanella frigidimarina reveals a novel family structural motif. Biochemistry 47 (2008) 11973-11980
52. Harada E., Kumagai J., Ozawa K., Imabayashi S., Tsapin A.S., Nealson K.H., Meyer T.E., Cusanovich M.A., and Akutsu H. A directional electron transfer regulator based on heme-chain architecture in the small tetraheme cytochrome c from Shewanella oneidensis. FEBS Lett. 532 (2002) 333-337
53. Page C.C., Moser C.C., Chen X., and Dutton P.L. Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 402 (1999) 47-52