1887

Abstract

The periplasmic cytochrome content of has been shown by immunological detection to be strongly dependent on the mode of growth. Cells grown under anaerobic, denitrifying conditions or methylotrophically in the presence of oxygen contained substantially more cytochrome than cells grown aerobically on multicarbon substrates. A similar pattern was observed when expression of the gene (encoding cytochrome ), was monitored using an alkaline phosphatase gene () fusion as a reporter of promoter activity. The increase in expression observed during growth on C substrates was substantially diminished if succinate was also present. These results reveal that expression of is subject to multiple regulatory controls and suggest that cytochrome has a general role in electron transfer to periplasmic reductases required for anaerobic denitrifying growth and from dehydrogenases required for aerobic growth on C compounds. Two major transcriptional initiation start points for the gene have been identified.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-142-9-2577
1996-09-01
2022-01-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/142/9/mic-142-9-2577.html?itemId=/content/journal/micro/10.1099/00221287-142-9-2577&mimeType=html&fmt=ahah

References

  1. Aiba H., Adhya S., de Crombrugghe B. 1981; Evidence for two functional gal promoters in intact Escherichia coli cells. J Biol Chem 256:11905–11910
    [Google Scholar]
  2. Alefounder P. R., Ferguson S. J. 1981; A periplasmic location for methanol dehydrogenase from Paraeoccus denitrificans: implications for proton pumping by cytochrome aa3. Biochem Biophys Res Commun 98:778–784
    [Google Scholar]
  3. Bagdasarian M., Lurz R., Rückert B., Franklin F. C. H., Bagdasarian M. M., Frey J., 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 cloning in Pseudomonas. Gene 16:237–247
    [Google Scholar]
  4. Bauer C. E., Bird T. E. 1996; Regulatory circuits controlling photosynthesis gene expression. Cell 85:5–8
    [Google Scholar]
  5. Benning M. M., Meyer T. E., Holden H. M. 1994; X-ray structure of the cytochrome c2 isolated from Paraeoccus denitrificansrefined to 1·7 Å resolution. Arch Biochem Biophys 310:460–466
    [Google Scholar]
  6. Berks B. C., Baratta D., Richardson J., Ferguson S. J. 1993; Purification and characterisation of a nitrous oxide reductase from Thiosphaera pantotropha. Implications for the mechanism of aerobic nitrous oxide reduction. Eur J Biochem 212:467–476
    [Google Scholar]
  7. de Boer A. P. N., Reijnders W. N. M., Kuenen J. G., Stouthamer A. H., van Spanning R. J. M. 1994; Isolation, sequencing and mutational analysis of a gene cluster involved in nitrite reduction in Paraeoccus denitrificans. Antonie Leeuwenhoek 66:111–127
    [Google Scholar]
  8. Boogerd F. C., van Verseveld H. W., Stouthamer A. H. 1980; Electron transport to nitrous oxide in Paraeoccus denitrificans. FEBS Lett 113:279–284
    [Google Scholar]
  9. Bosma G., Braster M., Stouthamer A. H., van Verseveld H. W. 1987; Subfractionation and characterisation of soluble c-type cytochromes from Paraeoccus denitrificans cultured under various limiting conditions in the chemosrat. Eur J Biochem 165:665–670
    [Google Scholar]
  10. Bott M., Thöny-Meyer L, Loferer H., Rossbach S., Tully R. E., Keister D., Appleby C. A., Hennecke H. 1995; Bradyrhizobium japonicum cytochrome c550 is required for nitrate respiration but not for symbiotic nitrogen fixation. J Bacteriol 177:2214–2217
    [Google Scholar]
  11. Bradford M. M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
    [Google Scholar]
  12. Brickman E., Beckwith J. 1975; Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and ɸ80 transducing phages. J Mol Biol 96:307–316
    [Google Scholar]
  13. Burnell J. N., John P., Whatley F. R. 1975; The reversibility of active sulphate transport in membrane vesicles of Paraeoccus denitrificans. Biochem J 150:527–536
    [Google Scholar]
  14. Davidson V. L., Kumar M. A. 1989; Cytochrome c550 mediates electron transfer from inducible periplasmic cytochromes to the cytoplasmic membrane of Paraeoccus denitrificans. FEBS Lett 245:271–273
    [Google Scholar]
  15. Dickins M. A., Dhawan T., Gunsalus R. P., Schroeder I., Cecchini G. 1995; Cloning, sequencing and expression of the succinate-ubiquinone oxidoreductase (SdhCDAB) operon from Paraeoccus denitrificans. EMBL database entry PDU31902.
    [Google Scholar]
  16. Eraso J. M., Kaplan S. 1994; prr4, a putative response regulator involved in oxygen regulation of photosynthesis gene expression in Rhodobacter sphaeroides. J Bacterial 176:32–43
    [Google Scholar]
  17. Ferguson S. J. 1987; Cytochrome c springs a surprise. Trends Biochem Sci 12:124–125
    [Google Scholar]
  18. Ferguson S. J., Page M. D. 1990; The functions and biosynthesis of the c-type cytochromes of bacterial respiratory chains with particular reference to autotrophs and the handling of C1compounds. FEMS Microbiol Rev 87:227–234
    [Google Scholar]
  19. Figurski D. H., Helinski D. R. 1979; Replication of an origin- containing derivative of plasmid RK2 dependent on a plasmid function derived in trans. Proc Natl Acad Sci USA 761648–1652
    [Google Scholar]
  20. Gerhus E., Steinrucke P., Ludwig B. 1990; Paraeoccus denitrificans cytochrome c1 gene replacement mutants. J Bacteriol 172:2392–2400
    [Google Scholar]
  21. de Gier J. W., Lubben M., Reijnders W. N., Tipker C. A., Slotboom D. J., van Spanning R. J., Stouthamer A. H., van der Oost J. 1994; The terminal oxidases of Paraeoccus denitrificans. Mol Microbiol 13:183–196
    [Google Scholar]
  22. De Gier J. L., van der Oost J., Harms N., Stouthamer A. H., van Spanning R.J.M. 1995; The oxidation of methylamine in Paraeoccus denitrificans. Eur J Biochem 229:148–154
    [Google Scholar]
  23. Goodhew C. F., Brown K. R., Pettigrew G. W. 1986; Haem staining in gels, a useful tool in the study of Bacteriol c-type cytochromes. Biochim Biophys Acta 852:288–294
    [Google Scholar]
  24. Goodhew C. F., Pettigrew G. W., Devreese B., van Beeumen J., van Spanning R. J. M., Baker S. C., Saunders N., Ferguson S. J., Thompson I. P. 1996; The cytochromes c550 of Paraeoccus denitrificans and Thiosphaera pantotropha: a need for re-evaluation of the history of Paraeoccus cultures. FEMS Microbiol Lett 137:95–101
    [Google Scholar]
  25. Goodwin P. M., Anthony C. 1995; The biosynthesis of periplasmic electron transport proteins in methylotrophic bacteria. Microbiology 141:1051–1064
    [Google Scholar]
  26. Harms N., Reijnders W. N. M., Anazawa H., van der Palen C.J.N.M., van Spanning R. J. M., Oltman L. F., Stouthamer A. H. 1993; Identification of a two-component regulatory system controlling methanol dehydrogenase synthesis in Paraeoccus denitrificans. Mol Microbiol 8:457–470
    [Google Scholar]
  27. John P., Whatley F. R. 1975; Paracoccus denitrificans and the evolutionary origin of mitochondria. Nature 254:495–498
    [Google Scholar]
  28. John P., Whatley F. R. 1977a; Paracoccus denitrificans Davis ( Micrococcus denitrificans Beijerinck) as a mitochondrion. Adv Bot Res 4:51–115
    [Google Scholar]
  29. John P., Whatley F. R. 1977b; The bioenergetics of Paracoccus denitrificans. Biochim Biophys Acta 463:129–153
    [Google Scholar]
  30. Johnstone A., Thorpe R. 1987 Immunochemistry in Practice, 2nd edn. pp. 257–260 Oxford: Blackwell Publications.;
    [Google Scholar]
  31. Kim K.S, Guarente L. 1989; Mutations that alter transcriptional activation but not DNA binding in the zinc finger of yeast activator HAP1. Nature 342:200–203
    [Google Scholar]
  32. Ludwig W., Mittenhuber G., Friedrich C. G. 1993; Transfer of Thiosphaera pantotropha to Paracoccus denitrificans. Int J Syst Bacteriol 43:363–367
    [Google Scholar]
  33. MacGregor B. J., Donohue T. J. 1991; Evidence for two promoters for the cytochrome c2 gene (cycA) of R hodobacter spberoides. J Bacteriol 173:3949–3957
    [Google Scholar]
  34. Matchova I., Kucera I. 1991; Evidence for the role of soluble cytochrome c in the dissimilatory reduction of nitrite and nitrous oxide by cells of Paracoccus denitrificans. Biochim Biophys Acta 1058:256–260
    [Google Scholar]
  35. Moir J. W. B., Ferguson S. J. 1994; Properties of a Paracoccus denitrificans mutant deleted in cytochrome c550 indicate that a copper protein can substitute for this cytochrome in electron transport to nitrite, nitric oxide and nitrous oxide. Microbiology 140:389–397
    [Google Scholar]
  36. Moir J. W. B., Baratta D., Richardson D. J., Ferguson S. J. 1993; The purification of a cd1-type nitrite reductase and the absence of a copper type nitrite reductase from the aerobic denitrifier Thiosphaera pantotropha; the role of pseudoazurin as an electron donor. Eur J Biochem 212:377–385
    [Google Scholar]
  37. Moir J. W. B., Richardson D. J., Ferguson S. J. 1995; The expression of redox proteins of denitrification in Thiosphaera pantotropha grown with oxygen, nitrate and nitrous oxide. Arch Microbiol 164:43–49
    [Google Scholar]
  38. Newton N. 1969; The two-haem nitrite reductase of Micrococcus denitrificans. Biochim Biophys Acta 185:316–331
    [Google Scholar]
  39. Page M. D., Ferguson S. J. 1990; Apo-forms of cytochrome c550 and cytochrome cd1 are translocated to the periplasm of Paracoccus denitrificans in the absence of haem incorportion caused by either mutation or inhibition of haem synthesis. Mol Microbiol 4:1181–1192
    [Google Scholar]
  40. Page M. D., Ferguson S. J. 1993; Mutants of Methylobacterium extorquens and Paracoccus denitrificans deficient in c-type cytochrome biogenesis synthesise the methylamine-dehydrogenase polypeptides that cannot assemble the tryptophan-tryptophylquinone group. Eur J Biochem 218:711–717
    [Google Scholar]
  41. Page M. D., Ferguson S. J. 1994; Differential reduction in soluble and membrane-bound cytochrome contents in a Paracoccus denitrificans mutant partially deficient in 5-aminolevulinate synthase activity. J Bacteriol 176:5919–5928
    [Google Scholar]
  42. Page M. D., Ferguson S. J. 1995; 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 15:307–315
    [Google Scholar]
  43. Page M. D., Carr G., Bell L. C., Ferguson S. J. 1989; Structure, control and assembly of a Bacteriol electron transport system as exemplified by Paracoccus denitrificans. Biochem Soc Trans 17:991–993
    [Google Scholar]
  44. Parsonage D., Greenfield A. J., Ferguson S. J. 1986; Evidence that the energy conserving electron transport pathways to nitrate and cytochrome o branch at ubiquinone in Paracoccus denitrificans. Arch Microbiol 145:191–196
    [Google Scholar]
  45. Pettigrew G. W., Moore G. R. 1987 Cytochromes c. Biological Aspects. Berlin, Heidelberg, New York: Springer-Verlag.;
    [Google Scholar]
  46. Raitio M., Pispa J. M., Metso T., Saraste M. 1990; Are there isoenzymes of cytochrome oxidase in Paracoccus denitrificans?. FEES Lett 261:431–435
    [Google Scholar]
  47. Richardson D. J., Bell L. C., Mcewan A. G., Jackson J. B., Ferguson S. J. 1991; Cytochrome c2 is essential for electron transfer to nitrous oxide reductase from physiological substrates in Rhodobacter capsulatus and can act as an electron donor to the reductase in vitro. Eur J Biochem 199:677–683
    [Google Scholar]
  48. Richter O.-M.H., Tao J.-S., Turba A., Ludwig B. 1994; A cytochrome ba3 functions as a quinol oxidase in Paracoccus denitrificans. Purification, cloning and sequence comparison. J Biol Chem 269:23079–23086
    [Google Scholar]
  49. Sambongi Y., Ferguson S. J. 1994; Synthesis of holo Paracoccus denitrificans cytochrome c550 requires targeting to the periplasm whereas that of holo Hydrogenobacter thermcphilus cytochrome c552 does not. FEBS Lett 340:65–70
    [Google Scholar]
  50. Sambongi Y., Stoll R., Ferguson S. J. 1996; Alteration of haem attachment and signal cleavage sites for Paracoccus denitrificanscytochrome c550 probes pathway of c-type cytochrome biogenesis in Escherichia coli. Mol Microbiol 19:1193–1204
    [Google Scholar]
  51. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn.. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory.;
    [Google Scholar]
  52. Samyn B., Berks B. C., Page M. D., Ferguson S. J., van Beeumen J. J. 1994; Characterisation and amino acid sequence of cytochrome c550 from Thiosphaera pantotropha. Eur J Biochem 219:585–594
    [Google Scholar]
  53. Sapshead L. M., Wimpenny J. W. T. 1972; The influence of oxygen and nitrate on the formation of the cytochrome pigments of the aerobic and anaerobic respiratory chain of Micrococcus denitrificans. Biochim Biophys Acta 267:388–397
    [Google Scholar]
  54. Schilke B. A., Donohue T. J. 1995; ChrR positively regulates transcription of the R hodobacter sphaeroides cytochrome c2 gene. J Bacteriol 177:1929–1937
    [Google Scholar]
  55. Scholes P. B., Smith L. 1968; Composition and properties of the membrane-bound respiratory chain system of Micrococcus denitrificans. Biochim Biophys Acta 153:363–375
    [Google Scholar]
  56. Smith L., Davies H. 1991; The reaction of the oxidase and reductases of Paracoccus denitrificans with cytochromes c550. J Bioenerg Biomembr 23:303–319
    [Google Scholar]
  57. van Spanning R. J. M. 1991 Genes involved in respiration of Paracoccus denitrificans. PhD thesis, Free University of Amsterdam, The Netherlands.
    [Google Scholar]
  58. van Spanning R. J. M., Wansell W. N. M., Harms N., Ras J., Oltmann L. F., Stouthamer A. H. 1990; Mutagenesis of the gene encoding cytochrome c550 of Paracoccus denitrificans and analysis of the resultant physiological effects. J Bacteriol 172:986–996
    [Google Scholar]
  59. van Spanning R. J. M., Wansell C. W., 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, c5511and c553i. J Bacteriol 173:6962–6970
    [Google Scholar]
  60. van Spanning R. J. M., van der Palen C. J. N. M., Slotboom D.-J., Reijnders W. N. M., Stouthamer A. H., Duine J. A. 1995a; Expression of the mau genes involved in methylamine metabolism in Paracoccus denitrificans is under control of a LysR-type transcriptional activator. Eur J Biochem 226:201–210
    [Google Scholar]
  61. van Spanning R. J. M., de Boer A. P. N., Reijnders W. N. M., Spiro S., Westerhoff H. V., Stouthamer A. H., van der Oost J. 1995b; Nitrite and nitric oxide reduction in Paracoccus denitrificansis under the control of NNR, a regulatory protein that belongs to the FNR family of transcriptional activators. FEBS Lett 360:151–154
    [Google Scholar]
  62. Steinrücke P., Ludwig B. 1993; Genetics of Paracoccus denitrificans. FEMS Microbiol Lett 104:83–118
    [Google Scholar]
  63. Steinrücke P., Gerhus E., Jetzek M., Turba A., Ludwig B. 1991; The cytochrome c reductase/oxidase respiratory pathway of Paracoccus denitrificans: genetic and functional studies. J Bioenerg Biomembr 23:227–239
    [Google Scholar]
  64. Stewart V. 1988; Nitrate respiration in relation to facultative metabolism in enterobacteria. Microbiol Rev 52:190–232
    [Google Scholar]
  65. Timkovich R., Dickerson R. E. 1976; The structure of Paracuccm denitrificans c550. J Biol Chem 251:4033–4046
    [Google Scholar]
  66. Turba A., Jetzek M., Ludwig B. 1995; Purification of Paracoccus denitrificans cytochrome c552 and sequence analysis of the gene. Eur J Biochem 231:259–265
    [Google Scholar]
  67. Tzagoloff A., Capitanio N., Nobrega M. P., Gatti D. 1990; Cytochrome oxidase assembly in yeast requires the product of COX11, a homolog of the P. denitrificans protein encoded by ORF3. EMBO J 9:2759–2764
    [Google Scholar]
  68. de Vries G. E., Harms N., Maurer K., Papandrecht A., Stouthamer A. H. 1988; Physiological regulation of Paracoccus denitrificans methanol dehydrogenase. J Bacteriol 170:3731–3737
    [Google Scholar]
  69. de Vries G. E., Harms N., Hoogendijk J., Stoutharner A. H. 1989; Isolation and characterisation of Paracoccus denitrificans mutants with increased conjugation frequencies and pleiotropic loss of a (nGATCn) DNA modifying property. Arch Microbiol 152:52–57
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-142-9-2577
Loading
/content/journal/micro/10.1099/00221287-142-9-2577
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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