1887

Microbiology Society logo

Volume 141, Issue 10

In 168, teichoic acid of the cross-wall may be different from that of the cylinder: a hypothesis based on transcription analysis of genes Free

Abstract

Summary: Five of the genes known to encode the enzymes for the synthesis of poly(glycerol phosphate), the major teichoic acid of 168, are organized in two divergently transcribed operons, and and transcriptional fusions to the first genes of these operons revealed that: (i) in media of different richness, higher growth rates were paralleled by lower transcription levels; (ii) upon transition to stationary phase, the transcription per unit mass of both operons increased abruptly by a factor of about two; and (iii) a rise in temperature was accompanied by decreased transcription of and increased transcription of . Mapping of transcription start points revealed two divergent a-controlled promoters. Although and the neighbouring downstream gene are transcribed from the same promoter, the latter was expressed at a much lower level than the former. Moreover, expression of , and of the translationally coupled , did not increase at the onset of the stationary phase, indicating that additional regulatory signals may act in the intergenic - region. Optimal transcription of these operons appears to require the entire regulatory region, suggesting that gene expression may, among other factors, be regulated by the three-dimensional configuration of this segment. The biological implications of these results are discussed.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): Bacillus subtilis 168 , cross-wall , poly(glycerol phosphate) , tag gene transcription and teichoic acids
© Society for General Microbiology 1995
Loading

Article metrics loading...

/content/journal/micro/10.1099/13500872-141-10-2379
1995-10-01
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/141/10/mic-141-10-2379.html?itemId=/content/journal/micro/10.1099/13500872-141-10-2379&mimeType=html&fmt=ahah

References

  1. Aldea M., Garrido T., Pla J., Vicente M. 1990; Division genes in Escherichia coli are expressed coordinately to cell septum requirements by gearbox promoters.. EMBO J 9:3787–3794
     [Google Scholar]
  2. Antoniewski C., Savelli B., Stragier P. 1990; The spoIIJ gene, which regulates early developmental steps in Bacillus subtilis, belongs to a class of environmentally responsive genes.. J Bacteriol 172:86–93
     [Google Scholar]
  3. Araki Y., Ito E. 1989; Linkage units in cell walls of grampositive bacteria.. Crit Rev Microbiol 17:121–135
     [Google Scholar]
  4. Baddiley J. 1970; Structure, biosynthesis and function of teichoic acids.. Account Chem Res 3:98–105
     [Google Scholar]
  5. Barr K., Ward S., Meier-Dieter U., Mayer H., Rick P.D. 1988; Characterization of an Escherichia coli rff mutant defective in transfer of N-acetylmannosaminuronic acid (ManNacA) from UDP-ManNacA to a lipid-linked intermediate involved in enterobacterial common antigen synthesis.. J Bacteriol 170:228–233
     [Google Scholar]
  6. Beck C.F., Warren R.A.J. 1988; Divergent promoters, a common form of gene organization.. Microbiol Rev 52:318–326
     [Google Scholar]
  7. Brehm J.K., Oultram J.D., Thompson D.E., Swinfield T.J., Peck H., Young M., Minton N.P. 1988; Construction of plasmid vector systems for Clostridium acetobutylicum.. In Genetics and Biotechnology of Bacilli 2 pp. 409–414 Edited by Ganesan A. T., Hoch J. A. San Diego: Academic Press;
     [Google Scholar]
  8. Brooks D., Mays L.L., Hatefi Y., Young F.E. 1971; Glucosylation of teichoic acid: solubilisation and partial characterization of the uridine diphosphoglucose: polyglycerol- teichoic acid glucosyl transferase from membranes of Bacillus subtilis.. J Bacteriol 107:223–229
     [Google Scholar]
  9. Carter H.L. III Wang L.-F., Doi R.H., Moran C.P. Jr 1988; rpoD operon promoter used by σH-RNA polymerase in Bacillus subtilis.. J Bacteriol 170:1617–1621
     [Google Scholar]
  10. Chung C.T., Miller R.H. 1988; A rapid and convenient method for the preparation and storage of competent bacterial cells.. Nucleic Acids Res 16:3580
     [Google Scholar]
  11. Clarke-Sturman A.J., Archibald A.R., Hancock I.C., Harwood C.R., Merad T., Hobot J.A. 1989; Cell wall assembly in Bacillus subtilis-. partial conservation of polar wall material and the effect of growth conditions on the pattern of incorporation of new material at the polar caps.. J Gen Microbiol 135:657–665
     [Google Scholar]
  12. Del Sal G., Manfioletti G., Schneider C. 1988; A one-tube plasmid DNA minipreparation suitable for sequencing.. Nucleic Acids Res 16:9878
     [Google Scholar]
  13. Dubnau E.J., Weir J., Nair G., Carter H.L. III Moran C.P. Jr Smith I. 1988; Bacillus sporulation gene spo0H codes for σ30 (σH).. J Bacteriol 170:1054–1062
     [Google Scholar]
  14. Ellwood D.C., Tempest D.W. 1972; Effects of environment on bacterial wall content and composition.. Adv Microb Physiol 7:83–117
     [Google Scholar]
  15. Fan D.P., Pelvit M.C., Cunningham W.P. 1972; Structural difference between walls from ends and sides of the rod-shaped bacterium Bacillus subtilis.. J Bacteriol 114:790–797
     [Google Scholar]
  16. Gonzy-Tr#x00E9;boul G., Karmazyn-Campelli C., Stragier P. 1992; Developmental regulation of transcription of the Bacillus subtilis ftsAZ operon.. J Mol Biol 224:967–979
     [Google Scholar]
  17. Graham L.L., Beveridge T.J. 1994; Structural differentiation of the Bacillus subtilis 168 cell wall.. J Bacteriol 176:1413–1421
     [Google Scholar]
  18. Hanahan D. 1983; Studies on transformation of Escherichia coli with plasmids.. J Mol Biol 166:557–580
     [Google Scholar]
  19. Heery D.M., Gannon F., Powell R. 1990; A simple method for subcloning DNA fragments from gel slices.. Trends Genet 6:173
     [Google Scholar]
  20. Honeyman A.L., Stewart G.C. 1989; The nucleotide sequence of the rodC operon in Bacillus subtilis.. Mol Microbiol 3:1257–1268
     [Google Scholar]
  21. Jefferson R.A., Burgess S.M., Hirsh D. 1986; β-Glucuronidase from Escherichia coli as a gene fusion marker.. Proc Natl Acad Sci USA 838447–8451
     [Google Scholar]
  22. Karamata D., Gross J. 1970; Isolation and genetic analysis of temperature sensitive mutants of Bacillus subtilis defective in DNA synthesis.. Mol & Gen Genet 108:277–287
     [Google Scholar]
  23. Karamata D., Pooley H.M., Monod M. 1987; Expression of heterologous genes for wall teichoic acids in Bacillus subtilis 168.. Mol & Gen Genet 207:73–81
     [Google Scholar]
  24. Karow M., Piggot P. 1993; The use of gus and lacZ fusions as a double reporter system to study gene expression during B. subtilis sporulation.. In Abstracts of Posters, Seventh International Conference on Bacillus, Paris, Trance p. 95
     [Google Scholar]
  25. Karow M.L, Glaser Ph., Piggot P.J. 1995; Identification of a gene, spoIIR, that links the activation of σE to the transcriptional activity of σF during sporulation in Bacillus subtilis.. Proc Natl Acad Sci USA 922012–2016
     [Google Scholar]
  26. Kellenberger E., Kellenberger-van der Kamp C. 1995; Unstained and in vivo fluorescently stained bacterial nucleoids and plasmolysis observed by a new specimen preparation method for high power light microscopy of metabolically active cells.. J Microsc 176:132–142
     [Google Scholar]
  27. Lazarevic V., Karamata D. 1995; The tagGH operon of Bacillus subtilis 168 encodes a two-component ABC transporter involved in the metabolism of two teichoic acids.. Mol Microbiol 16:345–355
     [Google Scholar]
  28. Lazarevic V., Margot Ph., Soldo B., Karamata D. 1992; Sequencing and analysis of the Bacillus subtilis lytRABCdivergon: a regulatory unit encompassing the structural genes of the N-acetylmuramoyl-l-alanine amidase and its modifier.. J Gen Microbiol 138:1949–1961
     [Google Scholar]
  29. Lazarevic V., Mauël C., Soldo B., Freymond P.-Ph., Margot Ph., Karamata D. 1995; Sequence analysis of the 308° to 311° segment of the Bacillus subtilis 168 chromosome, a region devoted to cell wall metabolism comprising non-coding grey holes which reveal chromosomal rearrangements.. Microbiology 141:329–335
     [Google Scholar]
  30. Lutkenhaus J. 1993; FtsZ ring in bacterial cytokinesis.. Mol Microbiol 9:403–409
     [Google Scholar]
  31. Maniatis T., Fritsch E.F., Sambrook J. 1982 Molecular Cloning: a Eaboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  32. Mauël C., Young M., Margot Ph., Karamata D. 1989; The essential nature of teichoic acids in Bacillus subtilis as revealed by insertional mutagenesis.. Mol & Gen Genet 215:388–394
     [Google Scholar]
  33. Mauel C., Young M., Karamata D. 1991; Genes concerned with synthesis of poly(glycerol phosphate), the essential teichoic acid in Bacillus subtilis strain 168, are organized in two divergent transcription units.. J Gen Microbiol 137:929–941
     [Google Scholar]
  34. Mauel C., Young M., Monsutti-Grecescu A., Marriot S.A., Karamata D. 1994; Analysis of Bacillus subtilis tag gene expression using transcriptional fusions.. Microbiology 140:2279–2288
     [Google Scholar]
  35. Meier-Dieter U., Starman R., Barr K., Mayer H., Rick P.D. 1990; Biosynthesis of enterobacterial common antigen in Escherichia coli. Biochemical characterization of Tn 10 insertion mutants defective in enterobacterial common antigen synthesis.. J Biol Chem 265:13490–13497
     [Google Scholar]
  36. Miller J. 1972 Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  37. Mobley H.L.T., Koch A.L., Doyle R.J., Streips U. N. 1984; Insertion and fate of the cell wall in Bacillus subtilis.. J Bacteriol 158:169–179
     [Google Scholar]
  38. Moran C.P. Jr Lang N., LeGrice S.F.J., Lee G., Stephens M. 1982; Nucleotide sequences that signal the initiation of transcription and translation in Bacillus subtilis.. Mol & Gen Genet 186:339–346
     [Google Scholar]
  39. O´Kane G, Stephens M.A., McConnel D. 1986; Integrable α-amylase plasmid for generating random transcriptional fusions in Bacillus subtilis.. J Bacteriol 168:973–981
     [Google Scholar]
  40. P#x00E9;rez-Martin J., Rojo F., de Lorenzo V. 1994; Promoters responsive to DNA bending: a common theme in prokaryotic gene expression.. Microbiol Rev 58:268–290
     [Google Scholar]
  41. Pooley H.M., Abelian F.-X., Karamata D. 1991; A conditional-lethal mutant of Bacillus subtilis 168 with a thermosensitive glycerol-3-phosphate cytidylyl transferase, an enzyme specific for the synthesis of the major wall teichoic acid.. J Gen Microbiol 137:921–928
     [Google Scholar]
  42. Pooley H.M., Abellan F.-X., Karamata D. 1992; CDP-glycerol: poly(glycerophosphate) glycerophosphotransferase, which is involved in the synthesis of the major wall teichoic acid in Bacillus subtilis 168, is encoded by tagF (rodC).. J Bacteriol 174:646–649
     [Google Scholar]
  43. Schaechter M., Maaloe O., Kjeldgaard N.O. 1958; Dependency on medium and temperature of cell size and chemical composition during balanced growth of Salmonella typhimurium.. J Gen Microbiol 19:592–606
     [Google Scholar]
  44. Schlaeppi J.-M., Pooley H.M., Karamata D. 1982; Identification of cell wall subunits in Bacillus subtilis and analysis of their cosegregation during growth.. J Bacteriol 149:329–337
     [Google Scholar]
  45. Soldo B, Lazarevic V., Margot Ph., Karamata D. 1993; Sequencing and analysis of the divergon comprising gtaB, the structural gene of UDP-glucose pyrophosphorylase of Bacillus subtilis 168.. J Gen Microbiol 139:3185–3195
     [Google Scholar]
  46. Tatti K.M., Carter H.L. III Moir A., Moran C.P. Jr 1989; Sigma H-directed transcription of citG in Bacillus subtilis.. J Bacteriol 171:5928–5932
     [Google Scholar]
  47. Trieu-Cuot P., Courvalin P. 1983; Nucleotide sequence of the Streptococcusfaecalis plasmid gene encoding the 3´,5´-aminoglycoside phosphotransferase type III.. Gene 23:331–341
     [Google Scholar]
  48. Vicente M., Kuschner S.R., Garrido T., Aldea M. 1991; The role of the ‘gearbox’ in the transcription of essential genes.. Mol Microbiol 5:2085–2091
     [Google Scholar]
  49. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mpl8 and pUC19 vectors.. Gene 33:103–119
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/13500872-141-10-2379
Loading
In Bacillus subtilis 168, teichoic acid of the cross-wall may be different from that of the cylinder: a hypothesis based on transcription analysis of tag genes
Microbiology 141, 2379 (1995); https://doi.org/10.1099/13500872-141-10-2379
/content/journal/micro/10.1099/13500872-141-10-2379
/content/journal/micro/10.1099/13500872-141-10-2379
Loading

Data & Media loading...

Most cited 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