1887

Abstract

The gene has been cloned and sequenced. Whereas disruption of (), the hydrophilic C-terminal domain of which has been deduced to be periplasmic and to function as a protein-disuifide reductase, leads to the absence of -type cytochromes, disruption of attenuated, but did not abolish, holo--type cytochrome biosynthesis. Comparison of the DipZ sequence with three other DipZ sequences indicated that there are not only two conserved cysteine residues in the C-terminal hydrophilic domain, but also two more in the central highly hydrophobic domain. The latter would be located toward the centre of two of the eight membrane-spanning α-helices predicted to compose the hydrophobic central domain of DipZ. Both these cysteine residues, plus other transmembrane helix residues, notably prolines and glycines, are also conserved in a group of membrane proteins, related to CcdA, which lack the N- and C-terminal hydrophilic domains of the DipZ proteins. It is proposed that DipZ of and other organisms transfers reducing power from the cytoplasm to the periplasm through reduction and reoxidation of an intramembrane disulfide bond, or other mechanism involving these cysteine residues, and that this function can also be performed by CcdA and other CcdA-like proteins. The failure of disruption to abolish -type cytochrome synthesis in suggests that, in contrast to the situation in , the absence of DipZ can be compensated for by one or more other proteins, for example a CcdA-like protein acting in tandem with one or more thioredoxin-like proteins.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-143-10-3111
1997-10-01
2021-04-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/143/10/mic-143-10-3111.html?itemId=/content/journal/micro/10.1099/00221287-143-10-3111&mimeType=html&fmt=ahah

References

  1. Aboagye-Kwarteng K., Smith K., Fairlamb A. H. 1992; Molecular characterisation of trypanothione reductase from crithidia fasciculata and trypanosoma brucei: Comparison with other flavoprotein disulfide oxidoreductases with respect to substrate specificity and reaction mechanism. Mol Microbiol 6:3089–3099
    [Google Scholar]
  2. Alefounder P. R., Ferguson S. J. 1981; A periplasmic location for methanol dehydrogenase from paracoccus denitrificans: Implications for proton pumping by cytochrome aa3. Biocbem Biophys Res Commun 98:778–784
    [Google Scholar]
  3. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410
    [Google Scholar]
  4. Bagdasarian M., Lurz R., Rllckert B., Franklin F. C. H., Bagdasarian M. M., Frey I., Timmis K. N. 1981; Specific-purpose plasmid cloning vector II. Broad host range, high copy number rsfl0l0-derived vectors and a host-vector system for gene cloning in pseudomonas . Gene 16:237–247
    [Google Scholar]
  5. Bardwell J. C. A., McGovern K., Beckwith J. 1991; Identification of a protein required for disulfide bond formation in vivo . Cell 67:581–589
    [Google Scholar]
  6. Bardwell J. C. A., Lee J.-O., Jander G., Martin N., 8T Belin D. 1993; A pathway for disulfide bond formation in vivo . Proc Natl Acad Sci USA 90:1038–1042
    [Google Scholar]
  7. Beckman D. L., Kranz R. G. 1993; Cytochromes c biogenesis in a photosynthetic bacterium requires a periplasmic thioredoxin- like protein. Proc Natl Acad Sci USA 90:2179–2183
    [Google Scholar]
  8. Beckman D. L., Trawick D. R., Kranz R. G. 1992; Bacterial cytochrome c biogenesis. Genes Dev 6:268–283
    [Google Scholar]
  9. Best E. A., Knauf V. C. 1993; Organization and nucleotide sequence of the genes encoding the biotin carboxyl carrier protein and biotin carboxylase protein of pseudomonas aeruginosa acetyl coenzyme a carboxylase. J Bacteriol 175:6881–6889
    [Google Scholar]
  10. Brendel V., Trifonov E. N. 1984; A computer algorithm for testing potential prokaryotic terminators. Nucleic Acids Res 12:4411–4427
    [Google Scholar]
  11. Crooke H., Cole J. 1995; The biogenesis of c-type cytochromes in escherichia coli requires a membrane-bound protein, dipz, with a protein-disulphide isomerase-like domain. Mol Microbiol 15:1139–1150
    [Google Scholar]
  12. Devereux J., Haeberli P., Smithies O. 1984; A comprehensive set of sequence analysis programs for the vax. Nucleic Acids Res 12:387–395
    [Google Scholar]
  13. Ellfolk N., Soininen R. 1970; Pseudomonas cytochrome c peroxidase. I. purification procedure. Acta Chem Scand 24:2126–2136
    [Google Scholar]
  14. Ellis L. B. M., Saurugger P., Woodward C. 1992; Identification of the three-dimensional thioredoxin motif: Related structure in the orf3 protein of the staphylococcus aureus mer operon. Biochemistry 31:4882–4891
    [Google Scholar]
  15. Fleischmann R. D., Adams M. D., White O. 37 Other Authors 1995; Whole-genome sequencing and assembly of haemophilus influenzae rd. Science 269:496–512
    [Google Scholar]
  16. Fong S.-T., Camakaris J., Lee B. T. O. 1995; Molecular genetics of a chromosomal locus involved in copper tolerance in escherichia coli k-12. Mol Microbiol 15:1127–1137
    [Google Scholar]
  17. Foote N., Peterson J., Gadsby P. M. A., Greenwood C., Thomson A. J. 1985; Redox-linked spin-state changes in the dihaem cytochrome c-551 peroxidase from pseudomonas aeruginosa . Biochem J 230:227–237
    [Google Scholar]
  18. Goldberg J. B., Ohman D. E. 1984; Cloning and expression in pseudomonas aeruginosa of a gene involved with the production of alginate. J Bacteriol 158:1115–1121
    [Google Scholar]
  19. Von Heijne G. 1989; The structure of signal peptides from bacterial lipoproteins. Protein Eng 2:531–534
    [Google Scholar]
  20. Von Heijne G. 1992; Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J Mol Biol 225:487–494
    [Google Scholar]
  21. Holloway B. W., Krishnapillai V., Morgan A. F. 1979; Chromosomal genetics of pseudomonas . Microbiol Rev 43:73–102
    [Google Scholar]
  22. Jones D. T., Taylor W. R., Thornton J. M. 1994; A model recognition approach to the prediction of all-helical membrane structure and topology. Biochemistry 33:3038–3049
    [Google Scholar]
  23. Kaneko T., Tanaka A., Sato S., Kotani H., Sazuka T., Miyajima N., Sugiura M., Tabata S. 1995; Sequence analysis of the genome of the unicellular cyanobacterium synechocystis sp. Strain pcc6803.1. sequence features in the 1 mb region from map positions 64% to 92% of the genome. DNA Res 2:153–166
    [Google Scholar]
  24. Kaneko T., Sato S., Kotani H. 21 other authors 1996; Sequence analysis of the genome of the unicellular cyanobacterium synechocystis sp. Strain pcc6803. ii. sequence determination of the entire genome and assignment of protein-coding regions. DNA Res 3:109–136
    [Google Scholar]
  25. Laddaga R. A., Chu L., Misra T. K., Silver S. 1987; Nucleotide sequence and expression of the mercurial-resistance operon from staphylococcus aureus plasmid pi258. Proc Natl Acad Sci USA 84:5106–5110
    [Google Scholar]
  26. Lalonde G., O'Hanley P. D., Stocker B. A. D., Denich K. T. 1994; Characterisation of a 3-dehydroquinase gene from actinobacillus pleuropneumoniae with homology to the eukaryotic genes qa-2 and qute. Mol Microbiol 11:273–280
    [Google Scholar]
  27. Li S. C., Deber C. M. 1992; Glycine and beta-branched residues support and modulate peptide helicity in membrane environments. FEBS Lett 311:217–220
    [Google Scholar]
  28. Matsushita K., Shinagawa E., Adachi O., Ameyama M. 1982; Membrane-bound cytochromes c of pseudomonas aeruginosa grown aerobically. Purification and characterisation of cytochromes c551 and c555. J Biochem 92:1607–1613
    [Google Scholar]
  29. Metheringham R., Griffiths L., Crooke H., Forsythe S., Cole J. 1995; An essential role for dsba in cytochrome c synthesis and formate-dependent nitrite reduction by escherichia coli k-12. Arch Microbiol 164:301–307
    [Google Scholar]
  30. Metheringham R., Tyson K. L., Crooke H., Missiakas D., Raina S., Cole J. 1996; Effects of mutations in genes for proteins involved in disulphide bond formation in the periplasm on the activities of anaerobically induced electron transfer chains in escherichia coli k12. Mol Gen Genet 253:95–102
    [Google Scholar]
  31. Missiakas D., Georgopoulos C., Raina S. 1993; Identification and characterisation of the escherichia coli gene dsbB, Whose product is involved in the formation of disulfide bonds in vivo. Proc Natl Acad Sci USA 90:7084–7088
    [Google Scholar]
  32. Missiakas D., Schwager F., Raina S. 1995; Identification and characterisation of a new disulphide-isomerase-like protein (Dsbd) in escherichia coli. EMBO J 14:3415–3424
    [Google Scholar]
  33. Nicholls D. G., Ferguson S. J. 1992 Bioenergetics 2 London: Academic Press;
    [Google Scholar]
  34. Nielsen H., Engelbrecht J., Brunak S., Von Heijne G. 1997; Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1–6
    [Google Scholar]
  35. Page M. D., Pearce D. A., Norris H. A. C., Ferguson S. J. 1997; The paracoccus denitrificans ccmaA,B and C genes: Cloning and sequencing, and analysis of the potential of their products to form a haem or apo c-type cytochrome transporter. Microbiology 143:563–576
    [Google Scholar]
  36. Pakula A. A., Simon M. P. 1992; Determination of transmembrane protein structure by disulfide cross-linking: The escherichia coli tar receptor. Proc Natl Acad Sci USA 89:4144–4148
    [Google Scholar]
  37. Persson B., Argos P. 1994; Predictions of transmembrane segments in proteins utilising multiple sequence alignments. J Mol Biol 237:182–192
    [Google Scholar]
  38. Philipp W. J., Poulet S., Eiglmeier K., Pascopella L., Balasubra- Manian V., Heym B., Bergh S., Bloom B. R., Jacobs W. R. Jr, Cole S. T. 1996; An integrated map of the genome of the tubercle bacillus, mycobacterium tuberculosis H37Rv, and comparison with mycobacterium leprae. Proc Natl Acad Sci USA 93:3132–3137
    [Google Scholar]
  39. Ramseier T., Winteler H. V., Hennecke H. 1991; Discovery and sequence analysis of bacterial genes involved in the biogenesis of c-type cytochromes. J Biol Chem 266:7793–7803
    [Google Scholar]
  40. Reichmann P., Gorisch H. 1993; Cytochrome c550 from pseudomonas aeruginosa . Biochem J 289:173–178
    [Google Scholar]
  41. Reith M. E., Munholland J. 1995; Complete nucleotide sequence of the porphyra purpurea chloroplast genome. Plant Mol Biol 13:333–335
    [Google Scholar]
  42. Reitsch A., Belin D., Martin N., Beckwith J. 1996; An in vivo pathway for disufide bond isomerisation in escherichia coli . Proc Natl Acad Sci USA 93:13048–13053
    [Google Scholar]
  43. Roe B. A., Clifton S., Dyer D. W. 1997; Gonococcal Genome Sequencing Project . 15 February 1997 data release http://www.genome.ou.edu/gono.html
  44. Roe B. A., McShan M., Ferretti J. 1997; Streptococcal Genome Sequencing Project . 15 February 1997 data release http://www.genome.ou.edu/strep.html
    [Google Scholar]
  45. Sambongi Y., Ferguson S. J. 1994; 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 353:235–238
    [Google Scholar]
  46. Sambongi Y., Ferguson J. 1996; Mutants of escherichia coli lacking disulphide oxidoreductases Dsba and Dsbb cannot synthesise an exogenous monohaem c-type cytochrome except in the presence of disulphide compounds. FEBS Lett 398:265–268
    [Google Scholar]
  47. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: A Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  48. Schiött T., Von Wachenfeldt C., Hederstedt L. 1997; Identification and characterisation of the ccda gene, required for cytochrome c synthesis in bacillus subtilis . J Bacteriol 179:1962–1973
    [Google Scholar]
  49. Schrover J. M., Frank J., Van Wielink J. E., Duine J. A. 1993; Quaternary structure of quinoprotein ethanol dehydrogenase from pseudomonas aeruginosa and its reoxidation with a novel cytochrome c from this organism. Biochem J 290:123–127
    [Google Scholar]
  50. Sedlmeier R., Altenbuchner J. 1992; Cloning and sequence analysis of the mercury resistance genes of streptomyces lividans . Mol Gen Genet 236:76–78
    [Google Scholar]
  51. Simon R., Priefer U., PUhler A. 1983; A broad host range mobilization system for in vivo genetic engineering: Transposon mutagenesis in gram-negative bacteria. Bio/Technology 1:37–45
    [Google Scholar]
  52. Van Spanning R. J. M., Wansell C. W., Van Reijnders W. N. M., Harms N., Ras J., Oltmann L. F., Stouthamer A. H. 1991; A method for introduction of unmarked mutations in the genome of paracoccus denitrificans: Construction of strains with multiple mutations in the genes encoding periplasmic cytochromes c550, c5511 and c553i. J Bacteriol 173:6962–6970
    [Google Scholar]
  53. Sutcliffe J. G. 1979; Complete nucleotide sequence of the escherichia coli plasmid pbr322. Cold Spring Harbor Symp Quant Biol 43:77–90
    [Google Scholar]
  54. ThOny-Meyer L., Fischer F., KUnzer P., Ritz D., Hennecke H. 1995; Escherichia coli genes required for cytochrome c maturation. J Bacteriol 177:4321–4326
    [Google Scholar]
  55. Timkovich R., Dhesi R., Martinkus K. J., Robinson M. K., Rea T. M. 1982; Isolation of paracoccus denitrificans cytochrome cd1 ; comparative kinetics with other nitrite reductases. Arch Biochim Biophys 215:47–58
    [Google Scholar]
  56. West S. E., Iglewski B. H. 1988; Codon usage in pseudomonas aeruginosa . Nucleic Acids Res 16:9323–9335
    [Google Scholar]
  57. Whitley P., Von Heijne G. 1993; The DsbA-DsbB system affects the formation of disulfide bonds in periplasmic but not in intramembraneous protein domains. FEBS Lett 332:49–51
    [Google Scholar]
  58. Whitley P., Nilsson L., Von Heijne G. 1993; Three-dimensional model for the membrane domain of escherichia coli leader peptidase based on disulfide mapping. Biochemistry 32:8534–8539
    [Google Scholar]
  59. Wieles B., Van Soolingen D., Holmgren A., Offringa R., Ottenhoff T. H. M., Thole J. E. R. 1995; Unique gene organisation of thioredoxin and thioredoxin reductase in mycobacterium leprae . Mol Microbiol 16:921–929
    [Google Scholar]
  60. Wieles B., Van Noort J., Drijfhout J. W., Offringa R., Holmgren A., Ottenhoff T. H. 1995; Purification and functional analysis of the mycobacterium leprae thioredoxin/thioredoxin reductase hybrid protein. J Biol Chem 270:25684–25686
    [Google Scholar]
  61. Willison J. C., John P. 1979; Mutants of paracoccus denitrificans deficient in c-type cytochromes. J Gen Microbiol 115:443–450
    [Google Scholar]
  62. Woolfson D. N., Williams D. H. 1990; The influence of proline residues on alpha-helical structure. FEBS Lett 277:185–188
    [Google Scholar]
  63. Yamanaka T., Kijimoto S., Okunuki K. 1963; Biological significance of pseudomonas cytochrome oxidase in pseudomonas aeruginosa . J Biochem 53:416–421
    [Google Scholar]
  64. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 phage cloning vectors and host strains: Nucleotide sequences of the m13 and puc19 vectors. Gene 33:103–119
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-143-10-3111
Loading
/content/journal/micro/10.1099/00221287-143-10-3111
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error