1887

Abstract

Summary: Intercellular communication is a crucial phenomenon during spore development in . It couples the establishment of a compartment-specific genetic program to the transcriptional activity of a σ factor in the other compartment. It also keeps σ factor activation in register with the morphological process. This study used directed mutagenesis to analyse the pathway that couples σ activation in the mother-cell to activation of σ in the forespore following asymmetric septation. Targets for mutagenesis in SpollGA (the receptor) were chosen based on the predicted topology of the protein when associated with the cell membrane. The results showed that a residue near the N terminus (D6), predicted to be exposed outside the cell, is required for receptor activity, whereas the major extracellular loop (between membrane domains IV and V) is dispensable for function. In contrast, mutations in SpollR (the signal) that partially blocked protein release (but not membrane translocation) had no effect on signal transduction. These results do not rule out the possibility that uncharacterized molecules intervene in the signalling pathway that establishes the mother-cell-specific developmental program during the early stage of sporulation.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-143-8-2753
1997-08-01
2021-03-06
Loading full text...

Full text loading...

/deliver/fulltext/micro/143/8/mic-143-8-2753.html?itemId=/content/journal/micro/10.1099/00221287-143-8-2753&mimeType=html&fmt=ahah

References

  1. Borchert T. V., Nagarajan V. 1991; Effect of signal sequence alterations on export of levansucrase in Bacillus subtilis. . J Bacteriol 173:276–282
    [Google Scholar]
  2. Breitling R., Dubnau D. 1990; A membrane protein with similarity to N-methylphenylalanine pilins is essential for DNA binding by competent Bacillus subtilis. . J Bacteriol 172:1499–1508
    [Google Scholar]
  3. Brickman E., Beckwith J. 1975; Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and ϕ80 transducing phages. J Mol Biol 96:307–316
    [Google Scholar]
  4. Duncan L., Losick R. 1993; SpoIIAB is an anti-σ factor that binds to and inhibits transcription by regulatory protein σF from Bacillus subtilis. . Proc Natl Acad Sci USA 90:2325–2329
    [Google Scholar]
  5. Errington J. 1993; Sporulation in Bacillus subtilis: regulation of gene expression and control of morphogenesis. Microbiol Rev 57:1–33
    [Google Scholar]
  6. Errington J., Mandelstam J. 1986; Use of a lacZ gene fusion to determine the dependence pattern of sporulation operon spoIIA in spo mutants of Bacillus subtilis. . J Gen Microbiol 132:2967–2976
    [Google Scholar]
  7. Field J., Nikawa J.-I., Broek D., MacDonald B., Rogers L., Wilson I. A., Lerner R. A., Wigler M. 1988; Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol Cell Biol 8:2159–2165
    [Google Scholar]
  8. Frandsen N., Stragier P. 1995; Identification and characterization of the Bacillus subtilis spoIIP locus. J Bacteriol 177:716–722
    [Google Scholar]
  9. Guérout-Fleury A.-M., Shazand K., Frandsen N., Stragier P. 1995; Antibiotic-resistance cassettes for Bacillus subtilis. . Gene 167:335–336
    [Google Scholar]
  10. Guérout-Fleury A.-M., Frandsen N., Stragier P. 1996; Plasmids for ectopic integration in Bacillus subtilis. . Gene 180:57–61
    [Google Scholar]
  11. Gutierrez C., Devedjian J.-C. 1989; A plasmid facilitating in vitro construction of phoA gene fusions in Escherichia coli. . Nucleic Acids Res 17:3999
    [Google Scholar]
  12. Haldenwang W. G. 1995; The sigma factors of Bacillus subtilis. . Microbiol Rev 59:1–30
    [Google Scholar]
  13. Hofmeister A. E. M., Londoño-Vallejo A., Harry E., Stragier P., Losick R. 1995; Extracellular signal protein triggering the proteolytic activation of a developmental transcription factor in B. . subtilis. Cell 83:219–226
    [Google Scholar]
  14. Illing N., Errington J. 1991; Genetic regulation of morphogenesis in Bacillus subtilis:. roles of σE and σ F in prespore engulfment. J Bacteriol 173:3159–3169
    [Google Scholar]
  15. Jonas R. M., Weaver E. A., Kenney T. J., Moran C. P., Jr & Haldenwang W. G. 1988; The Bacillus subtilis spoIIG operon encodes both σE and a gene necessary for σE activation. J Bacteriol 170:507–511
    [Google Scholar]
  16. Karow M., L, Glaser P., Piggot P. J. 1995; Identification of a gene, spoIIR, which links the activation of σE to the transcriptional activity of σ F during sporulation in Bacillus subtilis. . Proc Natl Acad Sci USA 92:2012–2016
    [Google Scholar]
  17. Londoño-Vallejo J.-A., Stragier P. 1995; Cell-cell signaling pathway activating a developmental transcription factor in Bacillus subtilis. . Genes Dev 9:503–508
    [Google Scholar]
  18. Londoño-Vallejo J.-A., Fréhel C., Stragier P. 1997; spoIIQ, a forespore expressed gene required for engulfment in Bacillus subtilis. . Mol Microbiol 24:29–39
    [Google Scholar]
  19. Losick R., Stragier P. 1992; Crisscross regulation of cell-type specific gene expression during development in Bacillus subtilis. . Nature 355:601–604
    [Google Scholar]
  20. Masuda E. S., Anaguchi H., Sato T., Takeuchi M., Kobayashi Y. 1990; Nucleotide sequence of the sporulation gene SpoIIGA from Bacillus subtilis. . Nucleic Acids Res 18:657
    [Google Scholar]
  21. Miller J. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  22. Nagarajan V. 1993; Protein secretion. . In Bacillus subtilis and other Gram-positive bacteria: Biochemistry, Physiology and Molecular Genetics pp 713–726 . Edited by Sonenshein A. L., Hoch J. A., Losick R. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  23. Peters H. K., III & Haldenwang W. G. 1991; Synthesis and fractionation properties of spoIIGA, a protein essential for pro-σE processing in Bacillus subtilis. . J Bacteriol 173:7821–7827
    [Google Scholar]
  24. Peters H. K., Haldenwang W. G. 1994; Isolation of a Bacillus subtilis spoIIGA allele that suppresses processing-negative mutations in the Pro-σE gene (sigE). J Bacteriol 176:7763–7766
    [Google Scholar]
  25. Petit-Glatron M. F., Monteil I., Benyahai F., Chambert R. 1990; Bacillus subtilis levansucrase: amino acid substitutions at one site affect secretion efficiency and refolding kinetics mediated by metals. Mol Microbiol 4:2063–2070
    [Google Scholar]
  26. Picard V., Ersdal-Badju E., Lu A., Clark Bock S. 1994; A rapid and efficient one-tube PCR-based mutagenesis technique using Pfu DNA polymerase. Nucleic Acids Res 22:2587–2591
    [Google Scholar]
  27. Rong S., Rosenkrantz M. S., Sonenshein A. L. 1986; Transcriptional control of the Bacillus subtilis spoIID gene. J Bacteriol 165:771–779
    [Google Scholar]
  28. Schaeffer P., Millet J., Auber J.-P. 1965; Catabolite repression of bacterial sporulation. Proc Natl Acad Sci USA 54:704–711
    [Google Scholar]
  29. Shazand K., Frandsen N., Stragier P. 1995; Cell-type specificity during development in Bacillus subtilis: the molecular and morphological requirements for σ E activation. EMBO J 14:1439–1445
    [Google Scholar]
  30. Stragier P., Bonamy C., Karmazyn-Campelli C. 1988; Processing of a sporulation sigma factor in Bacillus subtilis: how morphological structure could control gene expression. Cell 52:697–704
    [Google Scholar]
  31. Wong J., Sass C., Bennett G. N. 1995; Sequence and arrangement of genes encoding sigma factors in Clostridium acetobutylicum ATCC 824. Gene 153:89–92
    [Google Scholar]
  32. Wu J.-J., Piggot P. J., Tatti K. M., Moran C. P. J. 1991; Transcription of the Bacillus subtilis spoIIA operon. Gene 101:113–116
    [Google Scholar]
  33. Yansura D. G., Henner D. J. 1984; Use of the Escherichia coli lac repressor and operator to control gene expression in Bacillus subtilis. . Proc Natl Acad Sci USA 81:439–443
    [Google Scholar]
  34. Zhang L., Higgings M. L., Piggot P. J., Karow M. L. 1996; Analysis of the role of prespore gene expression in the compartmentalization of mother cell-specific gene expression during sporulation of Bacillus subtilis. . J Bacterial 178:2813–2817
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-143-8-2753
Loading
/content/journal/micro/10.1099/00221287-143-8-2753
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