Revealing the structural origin of the redox-Bohr effect: The first solution structure of a cytochrome from Geobacter sulfurreducens

Biochemical Journal

Volumn 441, Issue 1, 2012, Pages 179-187

  Morgado, Leonor ^a   Paixão, Vitor B ^b   Schiffer, Marianne ^c   Pokkuluri, P Raj ^c   Bruix, Marta ^d   Salgueiro, Carlos A ^a  

^a UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^b UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^c ARGONNE NATIONAL LABORATORY   (United States)

^d INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

Author keywords

Geobacter sulfurreducens; Multihaem cytochrome; NMR; Redox protein; Structure function relationship

Indexed keywords

CYTOCHROME; CYTOCHROME PPCA; UNCLASSIFIED DRUG;

ARTICLE; BOHR EFFECT; CONFORMATIONAL TRANSITION; ELECTRON TRANSPORT; GEOBACTER SULFURREDUCENS; HETERONUCLEAR SINGLE QUANTUM COHERENCE; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; NUCLEAR OVERHAUSER EFFECT; OXIDATION REDUCTION REACTION; PH; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; PROTON TRANSPORT;

BACTERIAL PROTEINS; CYTOCHROMES; GENE EXPRESSION REGULATION, BACTERIAL; GEOBACTER; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; OXIDATION-REDUCTION; PROTEIN CONFORMATION;

EID: 82355175841     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111103     Document Type: Article

References (35)

1. Lovley, D.R. (2003) Cleaning up with genomics: applying molecular biology to bioremediation. Nat. Rev. Microbiol. 1, 35-44
2. Lovley, D. R. (2008) The microbe electric: conversion of organic matter to electricity. Curr. Opin. Biotechnol. 19, 564-571
3. Methé, B. A., Nelson, K. E., Eisen, J. A., Paulsen, I. T., Nelson, W., Heidelberg, J. F., Wu, D., Wu, M., Ward, N., Beanan, M. J. et al. (2003) Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science 302, 1967-1969 (Pubitemid 37523504)
4. Pokkuluri, P. R., Londer, Y. Y., Duke, N. E., Long, W. C. and Schiffer, M. (2004) Family of cytochrome c 7-type proteins from Geobacter sulfurreducens: structure of one cytochrome c 7 at 1.45A° resolution. Biochemistry 43, 849-859 (Pubitemid 38141481)
5. Ding, Y. H., Hixson, K. K., Giometti, C. S., Stanley, A., Esteve-Núñez, A., Khare, T., Tollaksen, S. L., Zhu, W., Adkins, J. N., Lipton, M. S. et al. (2006) The proteome of dissimilatory metal-reducing microorganism Geobacter sulfurreducens under various growth conditions. Biochim. Biophys. Acta 1764, 1198-1206 (Pubitemid 44080859)
6. Shelobolina, E. S., Coppi, M. V., Korenevsky, A. A., Didonato, L. N., Sullivan, S. A., Konishi, H., Xu, H., Leang, C., Butler, J. E., Kim, B. C. et al. (2007) Importance of c -type cytochromes for U(VI) reduction by Geobacter sulfurreducens. BMC Microbiol. 7, 16
7. Lloyd, J. R., Leang, C., Hodges Myerson, A. L., Coppi, M. V., Cuifo, S., Methe, B., Sandler, S. J. and Lovley, D. R. (2003) Biochemical and genetic characterization of PpcA, a periplasmic c -type cytochrome in Geobacter sulfurreducens. Biochem. J. 369, 153-161 (Pubitemid 36174134)
8. Morgado, L., Bruix, M., Pessanha, M., Londer, Y. Y. and Salgueiro, C. A. (2010) Thermodynamic characterization of a triheme cytochrome family from Geobacter sulfurreducens reveals mechanistic and functional diversity. Biophys. J. 99, 293-301
9. Mahadevan, R., Bond, D. R., Butler, J. E., Esteve-Núñez, A., Coppi, M. V., Palsson, B. O., Schilling, C. H. and Lovley, D. R. (2006) Characterization of metabolism in the Fe(III)-reducing organism Geobacter sulfurreducens by constraint-based modeling. Appl. Environ. Microbiol. 72, 1558-1568 (Pubitemid 43271271)
10. Morgado, L., Bruix, M., Orshonsky, V., Londer, Y. Y., Duke, N. E., Yang, X., Pokkuluri, P. R., Schiffer, M. and Salgueiro, C. A. (2008) Structural insights into the modulation of the redox properties of two Geobacter sulfurreducens homologous triheme cytochromes. Biochim. Biophys. Acta 1777, 1157-1165
11. Pokkuluri, P. R., Londer, Y. Y., Yang, X., Duke, N. E., Erickson, J., Orshonsky, V., Johnson, G. and Schiffer, M. (2010) Structural characterization of a family of cytochromes c 7 involved in Fe(III) respiration by Geobacter sulfurreducens. Biochim. Biophys. Acta 1797, 222-232
12. Fernandes, A. P., Couto, I., Morgado, L., Londer, Y. Y. and Salgueiro, C. A. (2008) Isotopic labeling of c -type multiheme cytochromes overexpressed in E. coli. Protein Expression Purif. 59, 182-188
13. Arslan, E., Schulz, H., Zufferey, R., Kunzler, P. and Thöny-Meyer, L. (1998) Overproduction of the Bradyrhizobium japonicum c -type cytochrome subunits of the cbb 3 oxidase in Escherichia coli. Biochem. Biophys. Res. Commun. 251, 744-747 (Pubitemid 28512781)
14. Londer, Y. Y., Pokkuluri, P. R., Tiede, D. M. and Schiffer, M. (2002) Production and preliminary characterization of a recombinant triheme cytochrome c 7 from Geobacter sulfurreducens in Escherichia coli. Biochim. Biophys. Acta 1554, 202-211 (Pubitemid 34874936)
15. 15N chemical shift referencing in biomolecular NMR. J. Biomol. NMR 6, 135-140
16. Reference deleted
17. Garrett, D. S., Seok, Y. J., Peterkofsky, A., Clore, G. M. and Gronenborn, A. M. (1997) Identification by NMR of the binding surface for the histidine-containing phosphocarrier protein HPr on the N-terminal domain of enzyme I of the Escherichia coli phosphotransferase system. Biochemistry 36, 4393-4398 (Pubitemid 27180285)
18. Morgado, L., Paixão, V. B., Salgueiro, C. A. and Bruix, M. (2011) Backbone, side chain and heme resonance assignments of the triheme cytochrome PpcA from Geobacter sulfurreducens. Biomol. NMR Assign. 5, 113-116
19. Turner, D. L., Brennan, L., Chamberlin, S. G., Louro, R. O. and Xavier, A. V. (1998) Determination of solution structures of paramagnetic proteins by NMR. Eur. Biophys. J. 27, 367-375 (Pubitemid 28319747)
20. Paixão, V. B., Salgueiro, C. A., Brennan, L., Reid, G. A., Chapman, S. K. and Turner, D. L. (2008) The solution structure of a tetraheme cytochrome from Shewanella frigidimarina reveals a novel family structural motif. Biochemistry 47, 11973-11980
21. Güntert, P., Braun, W. and Wüthrich, K. (1991) Efficient computation of three-dimensional protein structures in solution from nuclear magnetic resonance data using the program DIANA and the supporting programs CALIBA, HABAS and GLOMSA. J. Mol. Biol. 217, 517-530
22. 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
23. Koradi, R., Billeter, M. and Wüthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 29-32
24. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R. and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486 (Pubitemid 126706801)
25. Turner, D. L., Salgueiro, C. A., LeGall, J. and Xavier, A. V. (1992) Structural studies of Desulfovibrio vulgaris ferrocytochrome c 3 by two-dimensional NMR. Eur. J. Biochem. 210, 931-936 (Pubitemid 23015794)
26. Assfalg, M., Banci, L., Bertini, I., Bruschi, M., Giudici-Orticoni, M. T. and Turano, P. (1999) A proton-NMR investigation of the fully reduced cytochrome c 7 from Desulfuromonas acetoxidans. Comparison between the reduced and the oxidized forms. Eur. J. Biochem. 266, 634-643
27. Mandel, A. M., Akke, M. and Palmer, III, A. G. (1995) Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme. J. Mol. Biol. 246, 144-163
28. 15N NMR relaxation methods. J. Biomol. NMR 24, 301-316
29. Fushman, D., Cahill, S. and Cowburn, D. (1997) The main-chain dynamics of the dynamin pleckstrin homology (PH) domain in solution: analysis of 15N relaxation with monomer/dimer equilibration. J. Mol. Biol. 266, 173-194 (Pubitemid 27170527)
30. Perutz, M. F., Wilkinson, A. J., Paoli, M. and Dodson, G. G. (1998) The stereochemical mechanism of the cooperative effects in hemoglobin revisited. Annu. Rev. Biophys. Biomol. Struct. 27, 1-34 (Pubitemid 28286007)
31. Moss, G. P. (1988) Nomenclature of tetrapyrroles. Recommendations 1986 IUPAC-IUB Joint Commission on Biochemical Nomenclature (JCBN). Eur. J. Biochem. 178, 277-328
32. Dantas, J. M., Morgado, L., Londer, Y. Y., Fernandes, A. P., Louro, R. O., Pokkuluri, P. R., Schiffer, M. and Salgueiro, C. A. (2011) Pivotal role of the strictly conserved aromatic residue F15 in the cytochrome c 7 family. J. Biol. Inorg. Chem., doi:10.1007/s00775-00011-00821-00778
33. Fonseca, B. M., Saraiva, I. H., Paquete, C. M., Soares, C. M., Pacheco, I., Salgueiro, C. A. and Louro, R. O. (2009) The tetraheme cytochrome from Shewanella oneidensis MR-1 shows thermodynamic bias for functional specificity of the hemes. J. Biol. Inorg. Chem. 14, 375-385
34. 7 from Desulfuromonas acetoxidans. Eur. J. Biochem. 256, 261-270
35. 7 from Desulfuromonas acetoxidans at 1.9A° resolution. Acta Crystallogr. Sect. D Biol. Crystallogr. 57, 670-678