MacA is a second cytochrome c peroxidase of Geobacter sulfurreducens

Biochemistry

Volumn 51, Issue 13, 2012, Pages 2747-2756

  Seidel, Julian ^a   Hoffmann, Maren ^a   Ellis, Katie E ^b   Seidel, Antonia ^a   Spatzal, Thomas ^a   Gerhardt, Stefan ^a   Elliott, Sean J ^b   Einsle, Oliver ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b Boston University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; C-TYPE CYTOCHROME; CONFORMATIONAL CHANGE; CYTOCHROME C; DIHEME CYTOCHROME C; ELECTRON DONORS; ELECTRON TRANSFER; GEOBACTER SULFURREDUCENS; LOOP REGIONS; METAL OXIDES; OPEN LOOP STRUCTURES; OXIDATION STATE; PROTEOBACTERIUM; RECOMBINANT EXPRESSION; REDUCTASE ACTIVITY; REDUCTIVE ACTIVATION; SEQUENCE COMPARISONS; STRUCTURAL VARIATIONS; SULFURREDUCENS; THREE-DIMENSIONAL STRUCTURE; TURNOVER NUMBER;

ELECTRON TRANSITIONS; ESCHERICHIA COLI; HYDROGEN PEROXIDE; IRON COMPOUNDS;

PORPHYRINS;

CYTOCHROME C PEROXIDASE; HEME; HYDROGEN PEROXIDE; LIGAND;

ARTICLE; BACTERIAL GENE; ELECTROCHEMICAL ANALYSIS; ELECTRON TRANSPORT; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE MACA; GENE STRUCTURE; GEOBACTER SULFURREDUCENS; NONHUMAN; OXIDATION KINETICS; PRIORITY JOURNAL; PROTEIN CONFORMATION;

BASE SEQUENCE; BIOCATALYSIS; CYTOCHROME-C PEROXIDASE; DNA PRIMERS; ELECTROCHEMISTRY; GEOBACTER; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; OXIDATION-REDUCTION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; GEOBACTER SULFURREDUCENS; LEPIDIUM MEYENII; PROTEOBACTERIA;

EID: 84859418589     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300249u     Document Type: Article

References (42)

1. Lovley, D. R. (1993) Dissimilatory metal reduction Annu. Rev. Microbiol. 47, 263-290
2. Lovley, D. R., Holmes, D. E., and Nevin, K. P. (2004) Dissimilatory Fe(III) and Mn(IV) reduction Adv. Microb. Physiol. 49, 219-286
3. Leang, C., Coppi, M. V., and Lovley, D. R. (2003) OmcB, a c -type polyheme cytochrome, involved in Fe(III) reduction in Geobacter sulfurreducens J. Bacteriol. 185, 2096-2103
4. Mehta, T., Coppi, M. V., Childers, S. E., and Lovley, D. R. (2005) Outer membrane c -type cytochromes required for Fe(III) and Mn(IV) oxide reduction in Geobacter sulfurreducens Appl. Environ. Microbiol. 71, 8634-8641
5. Weber, K. A., Achenbach, L. A., and Coates, J. D. (2006) Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction Nat. Rev. Microbiol. 4, 752-764
6. Clarke, T. A., Edwards, M. J., Gates, A. J., Hall, A., White, G. F., Bradley, J., Reardon, C. L., Shi, L., Beliaev, A. S., Marshall, M. J., Wang, Z. M., Watmough, N. J., Fredrickson, J. K., Zachara, J. M., Butt, J. N., and Richardson, D. J. (2011) Structure of a bacterial cell surface decaheme electron conduit Proc. Natl. Acad. Sci. U. S. A. 108, 9384-9389
7. 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., Dodson, R. J., Madupu, R., Brinkac, L. M., Daugherty, S. C., DeBoy, R. T., Durkin, A. S., Gwinn, M., Kolonay, J. F., Sullivan, S. A., Haft, D. H., Selengut, J., Davidsen, T. M., Zafar, N., White, O., Tran, B., Romero, C., Forberger, H. A., Weidman, J., Khouri, H., Feldblyum, T. V., Utterback, T. R., Van Aken, S. E., Lovley, D. R., and Fraser, C. M. (2003) Genome of Geobacter sulfurreducens: metal reduction in subsurface environments Science 302, 1967-1969
8. Butler, J. E., Kaufmann, F., Coppi, M. V., Nunez, C., and Lovley, D. R. (2004) MacA, a diheme c -type cytochrome involved in Fe(III) reduction by Geobacter sulfurreducens J. Bacteriol. 186, 4042-4045
9. Atack, J. M. and Kelly, D. J. (2007) Structure, mechanism and physiological roles of bacterial cytochrome c peroxidases Adv. Microb. Physiol. 52, 73-106
10. Pettigrew, G. W., Echalier, A., and Pauleta, S. R. (2006) Structure and mechanism in the bacterial dihaem cytochrome c peroxidases J. Inorg. Biochem. 100, 551-567
11. Caccavo, F., Jr., Lonergan, D. J., Lovley, D. R., Davis, M., Stolz, J. F., and McInerney, M. J. (1994) Geobacter sulfurreducens sp. nov., a hydrogen- and acetate-oxidizing dissimilatory metal-reducing microorganism Appl. Environ. Microbiol. 60, 3752-3759
12. Lin, W. C., Coppi, M. V., and Lovley, D. R. (2004) Geobacter sulfurreducens can grow with oxygen as a terminal electron acceptor Appl. Environ. Microbiol. 70, 2525-2528
13. De Smet, L., Savvides, S. N., Van Horen, E., Pettigrew, G., and Van Beeumen, J. J. (2006) Structural and mutagenesis studies on the cytochrome c peroxidase from Rhodobacter capsulatus provide new insights into structure-function relationships of bacterial di-heme peroxidases J. Biol. Chem. 281, 4371-4379
14. 2+ activation of the di-heme cytochrome c peroxidase from Pseudomonas nautica 617 Structure 12, 961-973
15. Echalier, A., Goodhew, C. F., Pettigrew, G. W., and Fülöp, V. (2006) Activation and catalysis of the di-heme cytochrome c peroxidase from Paracoccus pantotrophus Structure 14, 107-117
16. Fülöp, V., Ridout, C. J., Greenwood, C., and Hajdu, J. (1995) Crystal structure of the di-haem cytochrome c peroxidase from Pseudomonas aeruginosa Structure 3, 1225-1233
17. Hoffmann, M., Seidel, J., and Einsle, O. (2009) CcpA from Geobacter sulfurreducens is a basic di-heme cytochrome c peroxidase J. Mol. Biol. 393, 951-965
18. Shimizu, H., Schuller, D. J., Lanzilotta, W. N., Sundaramoorthy, M., Arciero, D. M., Hooper, A. B., and Poulos, T. L. (2001) Crystal structure of Nitrosomonas europaea cytochrome c peroxidase and the structural basis for ligand switching in bacterial di-heme peroxidases Biochemistry 40, 13483-13490
19. Ellfolk, N., Ronnberg, M., Aasa, R., Andreasson, L. E., and Vanngard, T. (1983) Properties and function of the two hemes in Pseudomonas cytochrome c peroxidase Biochim. Biophys. Acta 743, 23-30
20. Arciero, D. M. and Hooper, A. B. (1994) A di-heme cytochrome c peroxidase from Nitrosomonas europaea catalytically active in both the oxidized and half-reduced states J. Biol. Chem. 269, 11878-11886
21. 551 peroxidase with the use of magnetic circular dichroism Biochem. J. 223, 369-378
22. Pauleta, S. R., Cooper, A., Nutley, M., Errington, N., Harding, S., Guerlesquin, F., Goodhew, C. F., Moura, I., Moura, J. J., and Pettigrew, G. W. (2004) A copper protein and a cytochrome bind at the same site on bacterial cytochrome c peroxidase Biochemistry 43, 14566-14576
23. Pauleta, S. R., Guerlesquin, F., Goodhew, C. F., Devreese, B., Van Beeumen, J., Pereira, A. S., Moura, I., and Pettigrew, G. W. (2004b) Paracoccus pantotrophus pseudoazurin is an electron donor to cytochrome c peroxidase Biochemistry 43, 11214-11225
24. 3 oxidase in Escherichia coli Biochem. Biophys. Res. Commun. 251, 744-747
25. Heitmann, D. and Einsle, O. (2005) Structural and biochemical characterization of DHC2, a novel diheme cytochrome c from G eobacter sulfurreducens Biochemistry 44, 12411-12419
26. 6-type cytochrome OmcF from Geobacter sulfurreducens is mediated by an N-terminal Strep-tag II Acta Crystallogr. D 64, 919-926
27. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J., and Klenk, D. C. (1985) Measurement of protein using bicinchoninic acid Anal. Biochem. 150, 76-85
28. Otwinowski, Z. and Minor, W. (1996) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326
29. Vagin, A. A. and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement J. Appl. Crystallogr. 30, 1022-1025
30. Collaborative Computational Project No. 4. (1994) The CCP4 Suite: Programs for protein crystallography. Acta Crystallogr. D50, 760-763.
31. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot Acta Crystallogr. D 66, 486-501
32. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D53, 240-255
33. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: A program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26, 283-291
34. DeLano, W. L. (2002) The PyMOL Molecular Graphic System, DeLano Scientific, San Carlos.
35. 3 complex Biochem. J. 187, 809-818
36. Childs, R. E. and Bardsley, W. G. (1975) The steady-state kinetics of peroxidase with 2,2′ azino-di-(3-ethyl-benzthiazoline-6-sulphonic acid) as chromogen Biochem. J. 145, 93-103
37. 2 solutions in the UV) Anal. Biochem. 49, 474-478
38. Fourmond, V., Hoke, K., Heering, H. A., Baffert, C., Leroux, F., Bertrand, P., and Léger, C. (2009) SOAS: A free program to analyze electrochemical data and other one-dimensional signals Bioelectrochemistry 76, 141-147
39. Becker, C. F., Watmough, N. J., and Elliott, S. J. (2009) Electrochemical evidence for multiple peroxidatic heme states of the diheme cytochrome c peroxidase of Pseudomonas aeruginosa Biochemistry 48, 87-95
40. Ellis, K. E., Seidel, J., Einsle, O., and Elliott, S. J. (2011) Geobacter sulfurreducens cytochrome c peroxidases: electrochemical classification of catalytic mechanisms Biochemistry 50, 4513-4520
41. Firer-Sherwood, M. A., Bewley, K. D., Mock, J. Y., and Elliott, S. J. (2011) Tools for resolving complexity in the electron transfer networks of multiheme cytochromes c Metallomics 3, 344-348
42. Weiss, M. and Hilgenfeld, R. (1997) On the use of the merging R factor as a quality indicator for X-ray data J. Appl. Crystallogr. 30, 203-205