1887

Abstract

The operon of has previously been shown to be involved in the maturation of cytochrome , possibly by its involvement in the covalent attachment of haem to the apoprotein. Mutations in the genes abolish symbiotic nitrogen fixation. Here, we show that mutants are pleiotropically defective. They have lost a high affinity iron acquisition system due to their failure to make or to export siderophores. They also accumulate protoporphyrin IX, the immediate precursor of haem. A model to account for these phenotypes is presented. Immediately upstream of is a gene, , which is predicted to encode an outer-membrane lipoprotein. Further upstream of , there are two other genes, whose products are similar in sequence to the widespread family of two-component transcriptional regulators. These two genes, and , did not affect the transcription of , or of the operon. However, a mutation in also led to the loss of the high affinity iron uptake system, although siderophores were still produced.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-143-1-127
1997-01-01
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/143/1/mic-143-1-127.html?itemId=/content/journal/micro/10.1099/00221287-143-1-127&mimeType=html&fmt=ahah

References

  1. Albright L.M., Huala E., Ausubel F.M. 1989; Prokaryotic signal transduction mediated by sensor and regulator pairs.. Annu Rev Genet 23:311–336
    [Google Scholar]
  2. Beckman D.L., Trawick D.R., Kranz R.G. 1992; Bacterial cytochrome c biogenesis.. Genes Dev 6:268–283
    [Google Scholar]
  3. Beringer J.E. 1974; R factor transfer in Rhizobium leguminosarum. . J Gen Microbiol 84:188–198
    [Google Scholar]
  4. Beringer J.E., Hoggan S.A., Johnston A.W.B. 1978; Linkage mapping in Rhizobium leguminosarum by means of R plasmid- mediated recombination.. J Gen Microbiol 104:201–207
    [Google Scholar]
  5. Beynon J.L., Beringer J.E., Johnston A.W.B. 1980; Plasmids and host-range in Rhizobium leguminosarum and Rhizobium phaseoli. . J Gen Microbiol 120:421–429
    [Google Scholar]
  6. Buchanan-Woliaston A.V., Beringer J.E., Brewin N.J., Hirsch P.R., Johnston A.W.B. 1980; Isolation of symbiotically defective mutations in Rhizobium leguminosarum by insertion of the transposon Tn5 into a transmissible plasmid.. Mol Gen Genet 178:185–190
    [Google Scholar]
  7. Crosa J.H. 1989; Genetics and microbiology of siderophore- mediated iron transport in bacteria.. Microbiol Rev 53:517–530
    [Google Scholar]
  8. Delgado M.J., Yeoman K.H., Wu G., Vargas C., Davies A.E., Poole R.K., Johnston A.W.B., Downie J.A. 1995; Charac-terisation of the cycHJKL genes involved in cytochrome c biogenesis and symbiotic nitrogen fixation in Rhizobium leguminosarum. . J Bacteriol 177:4927–4934
    [Google Scholar]
  9. Downie J.A., Hombrecher G., Ma Q.S., Knight C.D., Wells B., Johnston A.W.B. 1983; Cloned nodulation genes of Rhizobium leguminosarum determine host-range specificity.. Mol Gen Genet 190:359–365
    [Google Scholar]
  10. Figurski D.H., Helinski D.R. 1979; Replication of an origin- containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. . Proc Natl Acad Sci USA 761648–1652
    [Google Scholar]
  11. Fischer H.M. 1994; Genetic regulation of nitrogen fixation in rhizobia.. Microbiol Rev 58:352–386
    [Google Scholar]
  12. Gilles-Gonzalez M.A., Ditta G.S., Helinski D.R. 1991; A haemoprotein with kinase activity encoded by the oxygen sensor of Rhizobium meliloti. . Nature 350:170–172
    [Google Scholar]
  13. Guerinot M.L. 1991; Iron uptake and metabolism in the rhizobia/legume symbiosis.. Plant Soil 130:199–209
    [Google Scholar]
  14. Johnston A.W.B., Brightwell G., Tibertius A., Yeoman K.H. 1994; Exopolysaccharide synthesis and haem production in Agrobacterium and Rhizobium - an unexpected link.. In Proceedings of the First European Nitrogen Fixation Conference pp. 91–94 Edited by Kiss G. B., Endre G. Szeged, Hungary: Officiana Press;
    [Google Scholar]
  15. Jones C.W., Poole R.K. 1985; Analysis of cytochromes.. Methods Microbiol 18:285–328
    [Google Scholar]
  16. Keen N.T., Tamaki S., Kobayashi D., Trollinger D. 1988; Improved broad-host range plasmids for DNA cloning in Gramnegative bacteria.. Gene 70:191–197
    [Google Scholar]
  17. Kereszt A., Slaska-Kiss K., Putnoky P., Banfalvi Z., Kondorosi A. 1995; 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 247:39–47
    [Google Scholar]
  18. Kondorosi A., Vincz E., Johnston A.W.B., Beringer J.E. 1980; A comparison of three Rhizobium linkage groups.. Mol Gen Genet 178:403–408
    [Google Scholar]
  19. Maniatis T., Fritsch E.F., Sambrook J. 1982 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  20. Miyamoto K., Nishimura K., Musuda T., Tsuji H., Inokuchioo H. 1992; Accumulation of protoporphyrin IX in light-sensitive mutants of Escherichia coli. . FEBS Lett 310:246–248
    [Google Scholar]
  21. Monson E.K., Ditta G.S., Helinski D.R. 1995; The oxygen sensor protein, FixL, of Rhizobium meliloti. . J Biol Chem 270:5243–5250
    [Google Scholar]
  22. Nadler K.D., Johnston A.W.B., Chen J.W., John T.R. 1990; A Rhizobium leguminosarum mutant defective in symbiotic iron acquisition.. J Bacteriol 172:670–677
    [Google Scholar]
  23. Ohyama K., Fukuzawa T., Kohchi T., Sano T., Sano S., Shirai H. 1988; Structure and organisation of Marchantia polymorpha chloroplast genome.. J Mol Biol 203:281–298
    [Google Scholar]
  24. Osteras M., Stanley J., Finan T.M. 1995; Identification of Rhizobium-specific intergenic mosaic elements within an essential two-component regulatory system of Rhizobium species.. J Bacteriol 177:5485–5494
    [Google Scholar]
  25. Page M.D., Ferguson S.J. 1995; Cloning and sequence analysis of the cycH gene from Paracoccus denitrificans; the cycH gene product is required for assembly of all c-type cytochromes, including cytochrome c1. . Mol Microbiol 15:307–318
    [Google Scholar]
  26. Parkinson J.S., Kofoid E.C. 1992; Communication modules in bacterial signalling proteins.. Annu Rev Genet 26:71–112
    [Google Scholar]
  27. Pritchard A.E., Seilhamer J.J., Mahalingam R., Sable C.L., Venuti S.E., Cummings D.J. 1990; Nucleotide sequence of the mitochondrial genome of Paramecium. . Nucleic Acids Res 18:173–180
    [Google Scholar]
  28. Reigh G., O’Connell M. 1993; Siderophore-mediated iron transport correlates with the presence of specific iron-regulated proteins in the outer membrane of Rhizobium meliloti. . J Bacteriol 175:94–102
    [Google Scholar]
  29. Ritz D., Thöny-Meyer L., Hennecke H. 1995; The cycHJKL gene cluster plays an essential role in the biogenesis of c-type cytochromes in Bradyrhizobium japonicum. . Mol Gen Genet 247:27–38
    [Google Scholar]
  30. Rossen L., Shearman C.A., Johnston A.W.B., Downie J.A. 1985; The nodD gene of Rhizobium leguminosarum is autoregulatory and in the presence of plant root exudate induces the nod ABC genes.. EMBO J 4:3369–3374
    [Google Scholar]
  31. Ruvkun G.B., Ausubel F.M. 1981; A general method for site- directed mutagenesis in prokaryotes.. Nature 289:85–88
    [Google Scholar]
  32. Schwyn B., Neilands J.B. 1987; Universal chemical assay for the detection and determination of siderophores.. Anal Biochem 160:47–56
    [Google Scholar]
  33. Simon R., Quamlt J., Klipp W. 1989; New derivatives of transposon Tn5 suitable for mobilisation of replicons, generation of operon fusions and induction of genes in Gram-negative bacteria.. Gene 80:161–169
    [Google Scholar]
  34. Smith M.J., Shoolery J.N., Schwyn B., Holden I., Neilands J.B. 1985; Rhizobactin, a structurally novel siderophore from Rhizobium meliloti. . J Am Chem Soc 107:1739–1743
    [Google Scholar]
  35. Spaink H.P., Okker R.J.H., Wijffelman C.A., Pees E., Lugtenberg B.J.J. 1985; Promoters in the nodulation region of the Rhizobium leguminosarum symbiotic plasmid pRL1JI.. Plant Mol Biol 9:27–39
    [Google Scholar]
  36. Staskawicz B., Dahlbeck D., Keen N.T., Napoli C.A. 1987; Molecular characterisation of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv glycinae. . J Bacteriol 169:5789–5794
    [Google Scholar]
  37. Stock J.B., Ninfa A.J., Stock A.M. 1989; Protein phos-phorylation and regulation of adaptive responses in bacteria.. Microbiol Rev 53:450–490
    [Google Scholar]
  38. Thöny-Meyer L., Fischer F., Kunzler P., Ritz D., Hennecke H. 1995; Escherichia coli genes required for cytochrome c maturation.. J Bacteriol 177:4321–4326
    [Google Scholar]
  39. Vargas G, McEwan A.G., Downie J.A. 1993; Detection of c- type cytochromes using enhanced chemiluminescence.. Anal Biochem 209:323–326
    [Google Scholar]
  40. Woese GR. 1987; Bacterial evolution.. Microbiol Rev 51:221–271
    [Google Scholar]
  41. Wu H.G, Tokunaga M. 1986; Biogenesis of lipoproteins in bacteria.. Curr Top Microbiol Immunol 125:127–157
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-143-1-127
Loading
/content/journal/micro/10.1099/00221287-143-1-127
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