Mutational analysis of sulfite reductase hemoprotein reveals the mechanism for coordinated electron and proton transfer

Biochemistry

Volumn 51, Issue 49, 2012, Pages 9857-9868

  Smith, Kyle W ^a   Stroupe, M Elizabeth ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ANION BINDING; ELECTRON TRANSFER; HEMOPROTEINS; IRON ATOMS; MACROCYCLES; MUTATIONAL ANALYSIS; NEGATIVE CHARGE; PER UNIT; POSITIVELY CHARGED; SIROHEME; SUBSTRATE BINDS; SULFITE REDUCTASE;

ELECTRON TRANSITIONS; IONS; PROTON TRANSFER; SULFUR;

AMINO ACIDS;

ANION; HEMOPROTEIN; SULFITE REDUCTASE; SULFUR;

ARTICLE; BINDING SITE; CHEMICAL STRUCTURE; ELECTRON; ELECTRON TRANSPORT; GENETIC VARIABILITY; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTON TRANSPORT; STOICHIOMETRY;

AMINO ACID SEQUENCE; BASE SEQUENCE; CRYSTALLOGRAPHY, X-RAY; ELECTRON TRANSPORT; HEMEPROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; OXIDOREDUCTASES ACTING ON SULFUR GROUP DONORS; PROTONS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84870872781     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300947a     Document Type: Article

References (29)

1. Sekowska, A., Kung, H. F., and Danchin, A. (2000) Sulfur metabolism in Escherichia coli and related bacteria: Facts and fiction J. Mol. Microbiol. Biotechnol. 2, 145-177
2. Rabus, R., Hansen, T. A., and Widdel, F. (2006) Dissimilatory Sulfate- and Sulfur-Reducing Prokaryotes. In The Prokaryotes: Ecophysiology and Biochemistry (Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K., and Stackebrandt, E., Eds.) pp 659-768, Springer, New York.
3. Crane, B. R., Siegel, L. M., and Getzoff, E. D. (1995) Sulfite reductase structure at 1.6 Å: Evolution and catalysis for reduction of inorganic anions Science 270, 59-67
4. 4]-dependent NirA from Mycobacterium tuberculosis is a sulfite reductase with a covalent Cys-Tyr bond in the active site J. Biol. Chem. 280, 27319-27328
5. Schiffer, A., Parey, K., Warkentin, E., Diederichs, K., Huber, H., Stetter, K. O., Kroneck, P. M., and Ermler, U. (2008) Structure of the dissimilatory sulfite reductase from the hyperthermophilic archaeon Archaeoglobus fulgidus J. Mol. Biol. 379, 1063-1074
6. Oliveira, T. F., Vonrhein, C., Matias, P. M., Venceslau, S. S., Pereira, I. A., and Archer, M. (2008) The crystal structure of Desulfovibrio vulgaris dissimilatory sulfite reductase bound to DsrC provides novel insights into the mechanism of sulfate respiration J. Biol. Chem. 283, 34141-34149
7. Hsieh, Y. C., Liu, M. Y., Wang, V. C., Chiang, Y. L., Liu, E. H., Wu, W. G., Chan, S. I., and Chen, C. J. (2010) Structural insights into the enzyme catalysis from comparison of three forms of dissimilatory sulphite reductase from Desulfovibrio gigas Mol. Microbiol. 78, 1101-1116
8. Fritz, G., Roth, A., Schiffer, A., Buchert, T., Bourenkov, G., Bartunik, H. D., Huber, H., Stetter, K. O., Kroneck, P. M., and Ermler, U. (2002) Structure of adenylylsulfate reductase from the hyperthermophilic Archaeoglobus fulgidus at 1.6-Å resolution Proc. Natl. Acad. Sci. U.S.A. 99, 1836-1841
9. Stroupe, M. E. and Getzoff, E. D. (2005) The role of siroheme in sulfite and nitrite reductases. In Tetrapyrroles: Their birth, life, and death (Warren, M. J. and Smith, A., Eds.) Landes Bioscience, Georgetown, TX.
10. Murphy, M. J. and Siegel, L. M. (1973) Siroheme and sirohydrochlorin. The basis for a new type of porphyrin-related prosthetic group common to both assimilatory and dissimilatory sulfite reductases J. Biol. Chem. 248, 6911-6919
11. Crane, B. R., Siegel, L. M., and Getzoff, E. D. (1997) Probing the catalytic mechanism of sulfite reductase by X-ray crystallography: Structures of the Escherichia coli hemoprotein in complex with substrates, inhibitors, intermediates, and products Biochemistry 36, 12120-12137
12. Parey, K., Warkentin, E., Kroneck, P. M., and Ermler, U. (2010) Reaction cycle of the dissimilatory sulfite reductase from Archaeoglobus fulgidus Biochemistry 49, 8912-8921
13. 4-containing active center of sulfite reductase in different states of oxidation: Heme activation via reduction-gated exogenous ligand exchange Biochemistry 36, 12101-12119
14. Schlegel, B. P., Jez, J. M., and Penning, T. M. (1998) Mutagenesis of 3α-hydroxysteroid dehydrogenase reveals a "push-pull" mechanism for proton transfer in aldo-keto reductases Biochemistry 37, 3538-3548
15. Janick, P. A., Rueger, D. C., Krueger, R. J., Barber, M. J., and Siegel, L. M. (1983) Characterization of complexes between Escherichia coli sulfite reductase hemoprotein subunit and its substrates sulfite and nitrite Biochemistry 22, 396-408
16. Wu, J. Y., Siegel, L. M., and Kredich, N. M. (1991) High-level expression of Escherichia coli NADPH-sulfite reductase: Requirement for a cloned cysG plasmid to overcome limiting siroheme cofactor J. Bacteriol. 173, 325-333
17. Siegel, L. M., Rueger, D. C., Barber, M. J., Krueger, R. J., Orme-Johnson, N. R., and Orme-Johnson, W. H. (1982) Escherichia coli sulfite reductase hemoprotein subunit. Prosthetic groups, catalytic parameters, and ligand complexes J. Biol. Chem. 257, 6343-6350
18. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K. A., Tomita, M., Wanner, B. L., and Mori, H. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: The Keio collection Mol. Syst. Biol. 2, 0008
19. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd ed., Vol. 3, Cold Spring Harbor Laboratory Press, Plainview, NJ.
20. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray Diffraction Data Collected in Oscillation Mode Methods Enzymol. 276, 307-326
21. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D66, 213-221
22. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot Acta Crystallogr. D66, 486-501
23. Thorneley, R. N. (1974) A convenient electrochemical preparation of reduced methyl viologen and a kinetic study of the reaction with oxygen using an anaerobic stopped-flow apparatus Biochim. Biophys. Acta 333, 487-496
24. Siegel, L. M. (1965) A Direct Microdetermination for Sulfide Anal. Biochem. 11, 126-132
25. Read, R. J. (1986) Imporved Fourier coefficients for maps using phases from partial structures with errors Acta Crystallogr. A42, 140-149
26. Murphy, M. J., Siegel, L. M., and Kamin, H. (1974) Reduced nicotinamide adenine dinucleotide phosphate-sulfite reductase of enterobacteria. VI. The reaction of carbon monoxide with the Escherichia coli holoenzyme, the hemoprotein, and free siroheme J. Biol. Chem. 249, 1610-1614
27. Siegel, L. M., Davis, P. S., and Kamin, H. (1974) Reduced nicotinamide adenine dinucleotide phosphate-sulfite reductase of enterobacteria. 3. The Escherichia coli hemoflavoprotein: Catalytic parameters and the sequence of electron flow J. Biol. Chem. 249, 1572-1586
28. 4 prosthetic groups in complexes of Escherichia coli sulfite reductase hemoprotein with added ligands Biochemistry 22, 504-515
29. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera: A visualization system for exploratory research and analysis J. Comput. Chem. 25, 1605-1612