This Article Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Reprints and Permissions Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Thony-Meyer, L. Articles by Hennecke, H. Search for Related Content PubMed PubMed Citation Articles by Thony-Meyer, L. Articles by Hennecke, H.

 Previous Article  |  Next Article 

J. Bacteriol., 08 1995, 4321-4326, Vol 177, No. 15
Copyright © 1995, American Society for Microbiology

Escherichia coli genes required for cytochrome c maturation

L Thony-Meyer, F Fischer, P Kunzler, D Ritz and H Hennecke
Mikrobiologisches Institut, Eidgenossische Technische Hochschule, Zurich, Switzerland.

The so-called aeg-46.5 region of Escherichia coli contains genes whose expression is induced under anaerobic growth conditions in the presence of nitrate or nitrite as the terminal electron acceptor. In this work, we have examined more closely several genes of this cluster, here designated ccmABCDEFGH, that are homologous to two separate Bradyrhizobium japonicum gene clusters required for the biogenesis of c- type cytochromes. A deletion mutant of E. coli which lacked all of these genes was constructed. Maturation of indigenous c-type cytochromes synthesized under anaerobic respiratory conditions, with nitrite, nitrate, or trimethylamine N-oxide as the electron acceptor, was found to be defective in the mutant. The biogenesis of foreign cytochromes, such as the soluble B. japonicum cytochrome c550 and the membrane-bound Bacillus subtilis cytochrome c550, was also investigated. None of these cytochromes was synthesized in its mature form when expressed in the mutant, as opposed to the situation in the wild type. The results suggest that the E. coli ccm gene cluster present in the aeg-46.5 region is required for a general pathway involved in cytochrome c maturation.

This article has been cited by other articles:

• Gao, T., O'Brian, M. R. (2007). Control of DegP-Dependent Degradation of c-Type Cytochromes by Heme and the Cytochrome c Maturation System in Escherichia coli. J. Bacteriol. 189: 6253-6259 [Abstract] [Full Text]  
• Rayapuram,, N., Hagenmuller,, J., Grienenberger, J.-M., Giege, P., Bonnard, G. (2007). AtCCMA Interacts with AtCcmB to Form a Novel Mitochondrial ABC Transporter Involved in Cytochrome c Maturation in Arabidopsis. J. Biol. Chem. 282: 21015-21023 [Abstract] [Full Text]  
• Garcia-Rubio, I., Braun, M., Gromov, I., Thony-Meyer, L., Schweiger, A. (2007). Axial Coordination of Heme in Ferric CcmE Chaperone Characterized by EPR Spectroscopy. Biophys. J 92: 1361-1373 [Abstract] [Full Text]  
• Dale, J. R., Wade, R. Jr., DiChristina, T. J. (2007). A Conserved Histidine in Cytochrome c Maturation Permease CcmB of Shewanella putrefaciens Is Required for Anaerobic Growth below a Threshold Standard Redox Potential. J. Bacteriol. 189: 1036-1043 [Abstract] [Full Text]  
• Koide, T., Vencio, R. Z. N., Gomes, S. L. (2006). Global Gene Expression Analysis of the Heat Shock Response in the Phytopathogen Xylella fastidiosa.. J. Bacteriol. 188: 5821-5830 [Abstract] [Full Text]  
• Muresanu, L., Pristovsek, P., Lohr, F., Maneg, O., Mukrasch, M. D., Ruterjans, H., Ludwig, B., Lucke, C. (2006). The Electron Transfer Complex between Cytochrome c552 and the CuA Domain of the Thermus thermophilus ba3 Oxidase: A COMBINED NMR AND COMPUTATIONAL APPROACH. J. Biol. Chem. 281: 14503-14513 [Abstract] [Full Text]  
• Harvat, E. M., Stevens, J. M., Redfield, C., Ferguson, S. J. (2005). Functional Characterization of the C-terminal Domain of the Cytochrome c Maturation Protein CcmE. J. Biol. Chem. 280: 36747-36753 [Abstract] [Full Text]  
• Meyer, E. H., Giege, P., Gelhaye, E., Rayapuram, N., Ahuja, U., Thony-Meyer, L., Grienenberger, J.-M., Bonnard, G. (2005). AtCCMH, an essential component of the c-type cytochrome maturation pathway in Arabidopsis mitochondria, interacts with apocytochrome c. Proc. Natl. Acad. Sci. USA 102: 16113-16118 [Abstract] [Full Text]  
• Pittman, M. S., Robinson, H. C., Poole, R. K. (2005). A Bacterial Glutathione Transporter (Escherichia coli CydDC) Exports Reductant to the Periplasm. J. Biol. Chem. 280: 32254-32261 [Abstract] [Full Text]  
• Braun, M., Thony-Meyer, L. (2005). Cytochrome c Maturation and the Physiological Role of c-Type Cytochromes in Vibrio cholerae. J. Bacteriol. 187: 5996-6004 [Abstract] [Full Text]  
• Bouhenni, R., Gehrke, A., Saffarini, D. (2005). Identification of Genes Involved in Cytochrome c Biogenesis in Shewanella oneidensis, Using a Modified mariner Transposon. Appl. Environ. Microbiol. 71: 4935-4937 [Abstract] [Full Text]  
• Ahuja, U., Thony-Meyer, L. (2005). CcmD Is Involved in Complex Formation between CcmC and the Heme Chaperone CcmE during Cytochrome c Maturation. J. Biol. Chem. 280: 236-243 [Abstract] [Full Text]  
• Uchida, T., Stevens, J. M., Daltrop, O., Harvat, E. M., Hong, L., Ferguson, S. J., Kitagawa, T. (2004). The Interaction of Covalently Bound Heme with the Cytochrome c Maturation Protein CcmE. J. Biol. Chem. 279: 51981-51988 [Abstract] [Full Text]  
• Braun, M., Thony-Meyer, L. (2004). Biosynthesis of artificial microperoxidases by exploiting the secretion and cytochrome c maturation apparatuses of Escherichia coli. Proc. Natl. Acad. Sci. USA 101: 12830-12835 [Abstract] [Full Text]  
• Edeling, M. A., Ahuja, U., Heras, B., Thony-Meyer, L., Martin, J. L. (2004). The Acidic Nature of the CcmG Redox-Active Center Is Important for Cytochrome c Maturation in Escherichia coli. J. Bacteriol. 186: 4030-4033 [Abstract] [Full Text]  
• Ahuja, U., Thony-Meyer, L. (2003). Dynamic Features of a Heme Delivery System for Cytochrome c Maturation. J. Biol. Chem. 278: 52061-52070 [Abstract] [Full Text]  
• Allen, J. W. A., Barker, P. D., Ferguson, S. J. (2003). A Cytochrome b562 Variant with a c-Type Cytochrome CXXCH Heme-binding Motif as a Probe of the Escherichia coli Cytochrome c Maturation System. J. Biol. Chem. 278: 52075-52083 [Abstract] [Full Text]  
• Kaderbhai, M. A., Hopper, D. J., Akhtar, K. M., Abbas, S. K., Kaderbhai, N. N. (2003). A Cytochrome c from a Lupanine-Transforming Pseudomonas putida Strain Is Expressed in Escherichia coli during Aerobic Cultivation and Efficiently Exported and Assembled in the Periplasm. Appl. Environ. Microbiol. 69: 4727-4731 [Abstract] [Full Text]  
• Pitts, K. E., Dobbin, P. S., Reyes-Ramirez, F., Thomson, A. J., Richardson, D. J., Seward, H. E. (2003). Characterization of the Shewanella oneidensis MR-1 Decaheme Cytochrome MtrA: EXPRESSION IN ESCHERICHIA COLI CONFERS THE ABILITY TO REDUCE SOLUBLE FE(III) CHELATES. J. Biol. Chem. 278: 27758-27765 [Abstract] [Full Text]  
• Sheehan, B. J., Bosse, J. T., Beddek, A. J., Rycroft, A. N., Kroll, J. S., Langford, P. R. (2003). Identification of Actinobacillus pleuropneumoniae Genes Important for Survival during Infection in Its Natural Host. Infect. Immun. 71: 3960-3970 [Abstract] [Full Text]  
• Enggist, E., Thony-Meyer, L. (2003). The C-Terminal Flexible Domain of the Heme Chaperone CcmE Is Important but Not Essential for Its Function. J. Bacteriol. 185: 3821-3827 [Abstract] [Full Text]  
• Stevens, J. M., Daltrop, O., Higham, C. W., Ferguson, S. J. (2003). Interaction of Heme with Variants of the Heme Chaperone CcmE Carrying Active Site Mutations and a Cleavable N-terminal His Tag. J. Biol. Chem. 278: 20500-20506 [Abstract] [Full Text]  
• Enggist, E., Schneider, M. J., Schulz, H., Thony-Meyer, L. (2003). Biochemical and Mutational Characterization of the Heme Chaperone CcmE Reveals a Heme Binding Site. J. Bacteriol. 185: 175-183 [Abstract] [Full Text]  
• Soriano, G. M., Guo, L.-W., de Vitry, C., Kallas, T., Cramer, W. A. (2002). Electron Transfer from the Rieske Iron-Sulfur Protein (ISP) to Cytochrome f in Vitro. IS A GUIDED TRAJECTORY OF THE ISP NECESSARY FOR COMPETENT DOCKING?. J. Biol. Chem. 277: 41865-41871 [Abstract] [Full Text]  
• Allen, J. W. A., Tomlinson, E. J., Hong, L., Ferguson, S. J. (2002). The Escherichia coli Cytochrome c Maturation (Ccm) System Does Not Detectably Attach Heme to Single Cysteine Variants of an Apocytochrome c. J. Biol. Chem. 277: 33559-33563 [Abstract] [Full Text]  
• Daltrop, O., Stevens, J. M., Higham, C. W., Ferguson, S. J. (2002). The CcmE protein of the c-type cytochrome biogenesis system: Unusual in vitro heme incorporation into apo-CcmE and transfer from holo-CcmE to apocytochrome. Proc. Natl. Acad. Sci. USA 99: 9703-9708 [Abstract] [Full Text]  
• Ren, Q., Ahuja, U., Thony-Meyer, L. (2002). A Bacterial Cytochrome c Heme Lyase. CcmF FORMS A COMPLEX WITH THE HEME CHAPERONE CcmE AND CcmH BUT NOT WITH APOCYTOCHROME c. J. Biol. Chem. 277: 7657-7663 [Abstract] [Full Text]  
• Schulz, H., Thöny-Meyer, L. (2000). Interspecies Complementation of Escherichia coli ccm Mutants: CcmE (CycJ) from Bradyrhizobium japonicum Acts as a Heme Chaperone during Cytochrome c Maturation. J. Bacteriol. 182: 6831-6833 [Abstract] [Full Text]  
• Pujol, C. J., Kado, C. I. (2000). Genetic and Biochemical Characterization of the Pathway in Pantoea citrea Leading to Pink Disease of Pineapple. J. Bacteriol. 182: 2230-2237 [Abstract] [Full Text]  
• Tichy, M., Vermaas, W. (1999). Accumulation of Pre-apocytochrome f in a Synechocystis sp. PCC 6803 Mutant Impaired in Cytochrome c Maturation. J. Biol. Chem. 274: 32396-32401 [Abstract] [Full Text]  
• Bolhuis, A., Venema, G., Quax, W. J., Bron, S., van Dijl, J. M. (1999). Functional Analysis of Paralogous Thiol-disulfide Oxidoreductases in Bacillus subtilis. J. Biol. Chem. 274: 24531-24538 [Abstract] [Full Text]  
• Holtwick, R., Keweloh, H., Meinhardt, F. (1999). cis/trans Isomerase of Unsaturated Fatty Acids of Pseudomonas putida P8: Evidence for a Heme Protein of the Cytochrome c Type. Appl. Environ. Microbiol. 65: 2644-2649 [Abstract] [Full Text]  
• Schulz, H., Fabianek, R. A., Pellicioli, E. C., Hennecke, H., Thony-Meyer, L. (1999). Heme transfer to the heme chaperone CcmE during cytochrome c maturation requires the CcmC protein, which may function independently of the ABC-transporter CcmAB. Proc. Natl. Acad. Sci. USA 96: 6462-6467 [Abstract] [Full Text]  
• Kraiß, A., Schlör, S., Reidl, J. (1998). In Vivo Transposon Mutagenesis in Haemophilus influenzae. Appl. Environ. Microbiol. 64: 4697-4702 [Abstract] [Full Text]  
• Tomii, K., Kanehisa, M. (1998). A Comparative Analysis of ABC Transporters in Complete Microbial Genomes. Genome Res 8: 1048-1059 [Abstract] [Full Text]  
• Berlyn, M. K. B. (1998). Linkage Map of Escherichia coli K-12, Edition 10: The Traditional Map. Microbiol. Mol. Biol. Rev. 62: 814-984 [Abstract] [Full Text]  
• Schulz, H., Hennecke, H., Thöny-Meyer, L. (1998). Prototype of a Heme Chaperone Essential for Cytochrome c Maturation. Science 281: 1197-1200 [Abstract] [Full Text]  
• Fabianek, R. A., Hennecke, H., Thöny-Meyer, L. (1998). The Active-Site Cysteines of the Periplasmic Thioredoxin-Like Protein CcmG of Escherichia coli Are Important but Not Essential for Cytochrome c Maturation In Vivo. J. Bacteriol. 180: 1947-1950 [Abstract] [Full Text]  
• Fabianek, R. A., Huber-Wunderlich, M., Glockshuber, R., Kunzler, P., Hennecke, H., Thony-Meyer, L. (1997). Characterization of the Bradyrhizobium japonicum CycY Protein, a Membrane-anchored Periplasmic Thioredoxin That May Play a Role as a Reductant in the Biogenesis of c-Type Cytochromes. J. Biol. Chem. 272: 4467-4473 [Abstract] [Full Text]  
• Spielewoy, N., Schulz, H., Grienenberger, J. M., Thony-Meyer, L., Bonnard, G. (2001). CCME, a Nuclear-encoded Heme-binding Protein Involved in Cytochrome c Maturation in Plant Mitochondria. J. Biol. Chem. 276: 5491-5497 [Abstract] [Full Text]  
• Pacello, F., Langford, P. R., Kroll, J. S., Indiani, C., Smulevich, G., Desideri, A., Rotilio, G., Battistoni, A. (2001). A Novel Heme Protein, the Cu,Zn-Superoxide Dismutase from Haemophilus ducreyi. J. Biol. Chem. 276: 30326-30334 [Abstract] [Full Text]  
• Ren, Q., Thony-Meyer, L. (2001). Physical Interaction of CcmC with Heme and the Heme Chaperone CcmE during Cytochrome c Maturation. J. Biol. Chem. 276: 32591-32596 [Abstract] [Full Text]