• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of jbacterPermissionsJournals.ASM.orgJournalJB ArticleJournal InfoAuthorsReviewers
J Bacteriol. Aug 1995; 177(15): 4321–4326.
PMCID: PMC177179

Escherichia coli genes required for cytochrome c maturation.

Abstract

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.

Full Text

The Full Text of this article is available as a PDF (307K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Beck R, Crooke H, Jarsch M, Cole J, Burtscher H. Mutation in dipZ leads to reduced production of active human placental alkaline phosphatase in Escherichia coli. FEMS Microbiol Lett. 1994 Dec 1;124(2):209–214. [PubMed]
  • Beckman DL, Kranz RG. Cytochromes c biogenesis in a photosynthetic bacterium requires a periplasmic thioredoxin-like protein. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2179–2183. [PMC free article] [PubMed]
  • Beckman DL, Trawick DR, Kranz RG. Bacterial cytochromes c biogenesis. Genes Dev. 1992 Feb;6(2):268–283. [PubMed]
  • Berks BC, Richardson DJ, Robinson C, Reilly A, Aplin RT, Ferguson SJ. Purification and characterization of the periplasmic nitrate reductase from Thiosphaera pantotropha. Eur J Biochem. 1994 Feb 15;220(1):117–124. [PubMed]
  • Bott M, Thöny-Meyer L, Loferer H, Rossbach S, Tully RE, Keister D, Appleby CA, Hennecke H. Bradyrhizobium japonicum cytochrome c550 is required for nitrate respiration but not for symbiotic nitrogen fixation. J Bacteriol. 1995 Apr;177(8):2214–2217. [PMC free article] [PubMed]
  • Brickman E, Beckwith J. Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and phi80 transducing phages. J Mol Biol. 1975 Aug 5;96(2):307–316. [PubMed]
  • Chepuri V, Lemieux L, Au DC, Gennis RB. The sequence of the cyo operon indicates substantial structural similarities between the cytochrome o ubiquinol oxidase of Escherichia coli and the aa3-type family of cytochrome c oxidases. J Biol Chem. 1990 Jul 5;265(19):11185–11192. [PubMed]
  • Choe M, Reznikoff WS. Identification of the regulatory sequence of anaerobically expressed locus aeg-46.5. J Bacteriol. 1993 Feb;175(4):1165–1172. [PMC free article] [PubMed]
  • Crooke H, Cole J. The biogenesis of c-type cytochromes in Escherichia coli requires a membrane-bound protein, DipZ, with a protein disulphide isomerase-like domain. Mol Microbiol. 1995 Mar;15(6):1139–1150. [PubMed]
  • Drygas ME, Lambowitz AM, Nargang FE. Cloning and analysis of the Neurospora crassa gene for cytochrome c heme lyase. J Biol Chem. 1989 Oct 25;264(30):17897–17906. [PubMed]
  • Dumont ME, Ernst JF, Hampsey DM, Sherman F. Identification and sequence of the gene encoding cytochrome c heme lyase in the yeast Saccharomyces cerevisiae. EMBO J. 1987 Jan;6(1):235–241. [PMC free article] [PubMed]
  • Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol. 1983 Jun 5;166(4):557–580. [PubMed]
  • Hussain H, Grove J, Griffiths L, Busby S, Cole J. A seven-gene operon essential for formate-dependent nitrite reduction to ammonia by enteric bacteria. Mol Microbiol. 1994 Apr;12(1):153–163. [PubMed]
  • Iobbi-Nivol C, Crooke H, Griffiths L, Grove J, Hussain H, Pommier J, Mejean V, Cole JA. A reassessment of the range of c-type cytochromes synthesized by Escherichia coli K-12. FEMS Microbiol Lett. 1994 Jun 1;119(1-2):89–94. [PubMed]
  • Kereszt A, Slaska-Kiss K, Putnoky P, Banfalvi Z, Kondorosi A. The cycHJKL genes of Rhizobium meliloti involved in cytochrome c biogenesis are required for "respiratory" nitrate reduction ex planta and for nitrogen fixation during symbiosis. Mol Gen Genet. 1995 Apr 10;247(1):39–47. [PubMed]
  • Kohara Y, Akiyama K, Isono K. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell. 1987 Jul 31;50(3):495–508. [PubMed]
  • Kündig C, Hennecke H, Göttfert M. Correlated physical and genetic map of the Bradyrhizobium japonicum 110 genome. J Bacteriol. 1993 Feb;175(3):613–622. [PMC free article] [PubMed]
  • Meissner PS, Sisk WP, Berman ML. Bacteriophage lambda cloning system for the construction of directional cDNA libraries. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4171–4175. [PMC free article] [PubMed]
  • Nicholson DW, Stuart RA, Neupert W. Biogenesis of cytochrome c1. Role of cytochrome c1 heme lyase and of the two proteolytic processing steps during import into mitochondria. J Biol Chem. 1989 Jun 15;264(17):10156–10168. [PubMed]
  • Page MD, Ferguson SJ. Cloning and sequence analysis of cycH gene from Paracoccus denitrificans: the cycH gene product is required for assembly of all c-type cytochromes, including cytochrome c1. Mol Microbiol. 1995 Jan;15(2):307–318. [PubMed]
  • Rabin RS, Stewart V. Dual response regulators (NarL and NarP) interact with dual sensors (NarX and NarQ) to control nitrate- and nitrite-regulated gene expression in Escherichia coli K-12. J Bacteriol. 1993 Jun;175(11):3259–3268. [PMC free article] [PubMed]
  • Ramseier TM, Winteler HV, Hennecke H. Discovery and sequence analysis of bacterial genes involved in the biogenesis of c-type cytochromes. J Biol Chem. 1991 Apr 25;266(12):7793–7803. [PubMed]
  • Ritz D, Bott M, Hennecke H. Formation of several bacterial c-type cytochromes requires a novel membrane-anchored protein that faces the periplasm. Mol Microbiol. 1993 Aug;9(4):729–740. [PubMed]
  • Ritz D, Thöny-Meyer L, Hennecke H. The cycHJKL gene cluster plays an essential role in the biogenesis of c-type cytochromes in Bradyrhizobium japonicum. Mol Gen Genet. 1995 Apr 10;247(1):27–38. [PubMed]
  • Sambongi Y, Crooke H, Cole JA, Ferguson SJ. A mutation blocking the formation of membrane or periplasmic endogenous and exogenous c-type cytochromes in Escherichia coli permits the cytoplasmic formation of Hydrogenobacter thermophilus holo cytochrome c552. FEBS Lett. 1994 May 16;344(2-3):207–210. [PubMed]
  • Sambongi Y, Ferguson SJ. Specific thiol compounds complement deficiency in c-type cytochrome biogenesis in Escherichia coli carrying a mutation in a membrane-bound disulphide isomerase-like protein. FEBS Lett. 1994 Oct 24;353(3):235–238. [PubMed]
  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [PMC free article] [PubMed]
  • Siddiqui RA, Warnecke-Eberz U, Hengsberger A, Schneider B, Kostka S, Friedrich B. Structure and function of a periplasmic nitrate reductase in Alcaligenes eutrophus H16. J Bacteriol. 1993 Sep;175(18):5867–5876. [PMC free article] [PubMed]
  • Thöny-Meyer L, Ritz D, Hennecke H. Cytochrome c biogenesis in bacteria: a possible pathway begins to emerge. Mol Microbiol. 1994 Apr;12(1):1–9. [PubMed]
  • Thöny-Meyer L, Stax D, Hennecke H. An unusual gene cluster for the cytochrome bc1 complex in Bradyrhizobium japonicum and its requirement for effective root nodule symbiosis. Cell. 1989 May 19;57(4):683–697. [PubMed]
  • von Wachenfeldt C, Hederstedt L. Bacillus subtilis holo-cytochrome c-550 can be synthesised in aerobic Escherichia coli. FEBS Lett. 1990 Sep 17;270(1-2):147–151. [PubMed]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...