Insight into molecular stability and physiological properties of the diheme cytochrome CYC41 from the acidophilic bacterium Acidithiobacillus ferrooxidans

Biochemistry

Volumn 44, Issue 17, 2005, Pages 6471-6481

  Malarte, Guillaume ^a   Leroy, Gisèle ^a   Lojou, Elisabeth ^a   Abergel, Chantal ^b   Bruschi, Mireille ^a   Giudici Orticoni, Marie Thérèse ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b CNRS Aix Marseille University   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRONS; ENZYMES; ESCHERICHIA COLI; REDOX REACTIONS; SUBSTITUTION REACTIONS;

ALANINE; DIHEME; FERROXIDANS; MOLECULAR STABILITY;

GENES;

BACTERIAL ENZYME; CYTOCHROME; CYTOCHROME C OXIDASE; CYTOCHROME P450 CYC41; GLUTAMIC ACID; HEME; MUTANT PROTEIN; PHENYLALANINE; RUSTICYANIN; TYROSINE; UNCLASSIFIED DRUG;

ACIDITHIOBACILLUS FERROOXIDANS; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; ELECTRON; ENZYME ACTIVITY; ENZYME STABILITY; ESCHERICHIA COLI; FERMENTATION; GENE EXPRESSION; GENE SEQUENCE; MOLECULAR CLONING; MOLECULAR INTERACTION; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PH; POINT MUTATION; PRIORITY JOURNAL;

ACIDITHIOBACILLUS; AZURIN; CYTOCHROME C GROUP; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX IV; ENZYME STABILITY; ESCHERICHIA COLI; HEME; HYDROGEN-ION CONCENTRATION; MUTAGENESIS, SITE-DIRECTED; OXIDATION-REDUCTION; OXIDOREDUCTASES; RECOMBINANT PROTEINS; SURFACE PLASMON RESONANCE; TYROSINE;

ACIDITHIOBACILLUS FERROOXIDANS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 17844394680     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048425b     Document Type: Article

References (60)

1. Rohwerder, T., Gehrke, T., Kinzler, K., and Sand, W. (2003) Bioleaching review part A: progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation, Appl. Microbiol. Biotechnol. 63, 239-248.
2. Valdes, J., Veloso, F., Jedlicki, E., and Holmes, D. (2003) Metabolic reconstruction of sulfur assimilation in the extremophile Acidithiobacillus ferrooxidans based on genome analysis, BMC Genomics 4, 51-67.
3. 2+ oxidation at pH 2.0 in Thiobacillus ferro-oxidans, FEBS Lett. 93, 157-160.
4. Nunzi, F., Guerlesquin, F., Shepard, W., Guigliarelli, B., and Bruschi, M. (1994) Active site geometry in the high oxidoreduction potential rusticyanin from Thiobacillus ferrooxidans, Biochem. Biophys. Res. Commun. 203, 1655-1662.
5. Nunzi, F., Woudstra, M., Campese, D., Bonicel, J., Morin, D., and Bruschi, M. (1993) Amino-acid sequence of rusticyanin from Thiobacillus ferrooxidans and its comparison with other blue copper proteins, Biochim. Biophys. Acta 1162, 28-34.
6. Casimiro, D.R., Toy-Palmer, A., Blake, R. C., 2nd, and Dyson, H. J. (1995) Gene synthesis, high-level expression, and mutagenesis of Thiobacillus ferrooxidans rusticyanin His 85 is a ligand to the blue copper center, Biochemistry 20, 6640-6648.
7. 4 isolated from Thiobacillus ferrooxidans, Eur. J. Biochem. 242, 308-314.
8. 4-type cytochrome isolated from Thiobacillus ferrooxidans, Biochemistry 39, 7205-7211.
9. Elbehti, A., and Lemesle-Meunier, D. (1996) Identification of membrane-bound c-type cytochromes in an acidophilic ferrous ion oxidizing bacterium Thiobacillus ferrooxidans, FEMS Microbiol. Lett. 136, 51-56.
10. Yarzabal, A., Brasseur, G., Ratouchniak, J., Lund, K., Lemesle-Meunier, D., DeMoss, J. A., and Bonnefoy, V. (2002) The high-molecular-weight cytochrome c Cyc2 of Acidithiobacillus ferrooxidans is an outer membrane protein, J. Bacteriol. 184, 313-317.
11. Cavazza, C., Guigliarelli, B., Bertrand, P., and Bruschi, M. (1995) Biochemical and EPR characterization of a high potential iron-sulfur protein Thiobacillus ferrooxidans, FEMS Microbiol Lett. 130, 193-200.
12. Elbehti, A., Nitschke, W., Tron, P., Michel, C., and Lemesle-Meunier, D. (1999) Redox components of cytochrome bc-type enzymes in acidophilic prokaryotes. I. Characterization of the cytochrome bcl-type complex of the acidophilic ferrous ion-oxidizing bacterium Thiobacillus ferrooxidans, J. Biol. Chem. 274, 16760-16765.
13. Brugna, M., Nitschke, W., Asso, M., Guigliarelli, B., Lemesle-Meunier, D., and Schmidt, C. (1999) Redox components of cytochrome bc-type enzymes in acidophilic prokaryotes. II. The Rieske protein of phylogenetically distant acidophilic organisms, J. Biol. Chem. 274, 16766-16772.
14. Elbehti, A., Brasseur, G., and Lemesle-Meunier, D. (2000) First evidence for existence of an uphill electron transfer through the bc(l) and NADH-Q oxidoreductase complexes of the acidophilic obligate chemolithotrophic ferrous ion-oxidizing bacterium Thiobacillus ferrooxidans, J. Bacteriol. 182, 3602-3606.
15. Brasseur, G., Bruscella, P., Bonnefoy, V., and Lemesle-Meunier, D. (2002) The bc(l) complex of the iron-grown acidophilic chemolithotrophic bacterium Acidithiobacillus ferrooxidans functions in the reverse but not in the forward direction. Is there a second bc(l) complex?, Biochim. Biophys. Acta 1555, 37-43.
16. Brasseur, G., Levican, G., Bonnefoy, V., Holmes, D., Jedlicki, E., and Lemesle-Meunier, D. (2004) Apparent redundancy of electron-transfer pathways via bc(l) complexes and terminal oxidases in the extremophilic chemolithoautotrophic Acidithiobacillus ferrooxidans, Biochim. Biophys. Acta 1656, 114-126.
17. Kai, M., Yano, T., Fukumori, Y., and Yamanaka, T. (1989) Cytochrome oxidase of an acidophilic iron-oxidizing bacterium, Thiobacillus ferrooxidans, functions at pH 3.5, Biochem. Biophys. Res. Commun. 160, 839-843.
18. Shoji, K., Yamazaki, T., Nagano, T., Fukumori, Y., and Yamanaka, T. (1992) Thiobacillus novellus cytochrome c oxidase contains one haem alpha molecule and one copper atom per catalytic unit, J. Biochem. 111, 46-53.
19. Tamegai, H., and Fukumori, Y (1994) Purification and some molecular and enzymatic features of a novel ccb-type cytochrome c oxidase from a microaerobic denitrifier, Magnetospirillum magnetotacticum, FEBS Lett. 347, 22-26.
20. Shoji, K., Tanigawa, M., Hori, K., Tomozawa, Y., and Yamanaka, T. (1999) The effects of several nucleotides on the molecular state and catalytic activity of Thiobacillus novellus cytochrome c oxidase ATP affects the oxidase uniquely, Eur. J. Biochem. 264, 960-964.
21. Blake, R. C., 2nd, and Shute, E. A. (1994) Respiratory enzymes of Thiobacillus ferrooxidans. Kinetic properties of an acid-stable iron:rusticyanin oxidoreductase, Biochemistry 33, 220-9228.
22. 4 and a high-molecular-weight cytochrome c from Thiobacillus ferrooxidans ATCC 33020, FEMS Microbiol. Lett. 167, 171-177.
23. Appia-Ayme, C., Guiliani, N., Ratouchniak, J., and Bonnefoy, V. (1999) Characterization of an operon encoding two c-type cytochromes, an aa3-type cytochrome oxidase, and rusticyanin in Thiobacillus ferrooxidans ATCC 33020, Appl. Environ. Microbiol. 65, 4781-4787.
24. Giudici-Orticoni, M. T., Guerlesquin, F., Bruschi M., and Nitschke, W. (1999) A surface-exposed histidine acts as a redox switch in the blue copper protein rusticyanin, J. Biol. Chem. 274, 30365-30369.
25. 4 structure supports a complex-induced tuning of electron transfer, Structure 11, 547-555.
26. Schulz, H., Hennecke, H., and Thony-Meyer, L. (1998) Prototype of a haem chaperone essential for cytochrome c maturation, Science 281 (5380), 1197-1200.
27. Thöny-Meyer, L. (2000) Heam-polypeptide interactions during cytochrome c maturation Biochim. Biophys. Acta 1459, 316-324.
28. 555 from the hyperthermophilic bacterium Aquifex aeolicus. 2. Heterologous production of soluble cytochrome c555s and investigation of the role of methionine residues, Biochemistry 40, 13690-13698.
29. Ansaldi, M., Lepelletier, M., and Mejean, V. (1996) Site-specific mutagenesis by using an accurate recombinant polymerase chain reaction method, Anal. Biochem. 234, 110-111.
30. Pollock, W. B., and Voordouw, G. (1994) Aerobic expression of the cyf gene encoding cytochrome c-553 from Desulfovibrio vulgaris Hildenborough in Escherichia coli, Microbiology 140, 879-887.
31. Taniguchi, I., Toyosawa, K., Yamaguchi, H., and Yasukouchi, K. (1982) Voltammetric response of horse heart cytochrome c at a gold electrode in the presence of sulfur bridged bipyridines, J. Electroanal. Chem. 140, 187-193.
32. Morris, M. C., Mery, J., Heitz A, Heitz F, and Divita G. (1999) Design and synthesis of a peptide derived from positions 195-244 of human cdc25C phosphatase. J. Pept. Sci. 5, 263-271.
33. Furste, J. P., Pansegrau, W., Frank, R., Blocker, H., Scholz, P., Bagdasarian M, and Lanka, E. (1986) Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector, Gene 48, 119-131.
34. Moore, G. R., and Pettigrew, G. W. (1990) Cytochromes c Evolutionary, structural and physicochemical aspects, Springer Ser. Mol. Biol. 2, 53-56.
35. Myer, Y. P., Saturno, A. F., Verma, B. C., and Pande, A. (1979) Horse heart cytochrome c. The oxidation-reduction potential and protein structures, J. Biol. Chem. 254, 11202-11207.
36. Myer, Y. P., and Saturno, A. F. (1991) Horse heart ferricytochrome c: conformation and haem configuration of high ionic strength acidic forms, J. Protein Chem. 10, 481-494.
37. 4), J. Inorg. Biochem. 88, 316-327.
38. Yer, Y. P., and Pande, A. (1978) in The Porphyrins (Dolphin, D., Ed.) pp 271-322, Academic Press, New York.
39. Slonczewki, J., and Foster, J. (1996) pH-regulated genes and survival at extreme pH in Escherichia coli and Salmonella. Cellular and molecular biology (Neidhardt, K. C., Ed.) pp 1539-1549, ASM Press: Washington, D.C.
40. Ferguson, S. J. (2001) Keilin's cytochromes: how bacteria use them, vary them and make them, Biochem. Soc. Trans. 29, 629-640.
41. Page, M. D., Salbongi, Y., and Fergusson, S. J. (1998) Contrasting routes of c-type cytochrome assembly in mitochondria, chloroplast and bacteria, Trends Biochem. Sci. 23, 103-108.
42. Kranz, R., Lill, R., Goldman, B., Bonnard, G., and Merchant, S. (1998) Molecular mechanisms of cytochrome c biogenesis: three distinct systems, Mol. Microbiol. 29, 382-396.
43. Sambongi, Y., Uchiyama, S., Kobayashi, Y., Igarashi Y., and Hasegawa, J. (2002) Cytochrome c from thermophilic bacterium has provided insights into mechanisms of protein maturation, folding and stability, Eur. J. Biochem. 269, 3355-3361.
44. Hall, J. H., Kanbi, L. D., Harvey, I., Murphy, L. M., and Hasnain, S. S. (1998) Modulating the redox potential and acid stability of rusticyanin by site-directed mutagenesis of Ser86, Biochemistry 37, 11451-11458.
45. Kusano, T., Takeshima, T., Sugawara, K., Inoue, C., Shiratori, T., Yano, T., Fukumori, Y., and Yamanaka, T. (1992) Molecular cloning of the gene encoding Thiobacillus ferrooxidans Fe(II) oxidase, J. Biol. Chem. 16, 11242-11247.
46. Schmidt, C. L., Hatzfeld, O. M., Petersen, A., Link, T. A., and Schäfer, G. (1997) Expression of the Sulfolobus acidocaldarius Rieske iron sulfur protein II (SOXF) with correctly inserted [2Fe-2S] cluster in Escherichia coli, Biochem. Biophys. Res. Commun. 234, 283-287.
47. Rafferty, S. P., Pearce, L. L., Barker, P. D., Guillemette, J. G., Kay, C. M., Smith, M., and Mauk, A. G. (1990) Electrochemical, kinetic, and circular dichroic consequences of mutations at position 82 of yeast iso-1-cytochrome c, Biochemistry 29, 9365-9369.
48. Sinibaldi, F., Fiorucci, L., Mei, G., Ferri, T., Desideri, A., Ascoli, F., and Santucci, R. (2001) Cytochrome c reconstituted from two peptide fragments displays native-like redox properties, Eur. J. Biochem. 268, 4537-4543.
49. Lett, M. C., and Guillemette, G. L. (2002) Increasing the redox potential of isoform 1 of yeast cytochrome c through the modification of select heam interactions, Biochem. J. 362, 281-287.
50. Luntz, T. L., Schejter, A., Garber, E. A., and Margoliash, E. (1989) Structural significance of an internal water molecule studied by site-directed mutagenesis of tyrosine-67 in rat cytochrome c, Proc. Natl. Acad. Sci. U.S.A. 86, 3524-3532.
51. Santucci, R., Brunori, M., and Ascoli, F. (1987) Unfolding and flexibility in hemoproteins shown in the case of carboxymethylated cytochrome c, Biochim. Biophys. Acta 914, 185-189.
52. Zhen, Y., Hoganson, C. W., Babcock, G. T., and Ferguson-Miller, S. (1999) Definition of the interaction domain for cytochrome c on cytochrome c oxidase. I. Biochemical, spectral, and kinetic characterization of surface mutants in subunit ii of Rhodobacter sphaeroides cytochrome aa(3), J. Biol. Chem. 274, 38032-38041.
53. Wang, K., Zhen, Y., Sadoski, R., Grinnell, S., Geren, L., Ferguson-Miller, S., Durham, B., and Millett, F. (1999) Definition of the interaction domain for cytochrome c on cytochrome c oxidase. II. Rapid kinetic analysis of electron transfer from cytochrome c to Rhodobacter sphaeroides cytochrome oxidase surface mutants, J. Biol. Chem. 274, 38042-38050.
54. Roberts, V. A., and Pique, M. E. (1999) Definition of the interaction domain for cytochrome c on cytochrome c oxidase. III. Prediction of the docked complex by a complete, systematic search, J. Biol. Chem. 274, 38051-38060.
55. Maneg, O., Malatesta, F., Ludwig, B., and Drosou, V. (2004) Interaction of cytochrome c with cytochrome oxidase: two different docking scenarios, Biochim. Biophys. Acta. 1655, 274-281.
56. Witt, H., Malatesta, F., Nicoletti, F., Brunori, M., and Ludwig, B. (1998) Cytochrome-c-binding site on cytochrome oxidase in Paracoccus denitrificans, Eur. J. Biochem. 251, 367-373.
57. Drosou, V., Reincke, B., Schneider, M., and Ludwig, B. (2002) Specificity of the interaction between the Paracoccus denitrificans oxidase and its substrate cytochrome c: comparing the mitochondrial to the homologous bacterial cytochrome c(552), and its truncated and site-directed mutants, Biochemistry 41, 10629-10634.
58. Maneg, O., Ludwig, B., and Malatesta, F. (2003) Different interaction modes of two cytochrome-c oxidase soluble CuA fragments with their substrates, J. Biol. Chem. 278, 46734-46740.
59. Ritchie, D. W., and Kemp, G. J. (2000) Protein docking using spherical polar Fourier correlations, Proteins 39, 178-94.
60. Nicholls, A., Sharp, K. A., and Honig, B. (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons, Proteins 11, 281-96.