1887

Abstract

The cell walls of Gram-positive bacteria consist primarily of a macromolecular matrix comprising similar amounts of peptidoglycan and covalently attached anionic polymers. Under most growth conditions the anionic polymers of are principally teichoic acids; in strain 168 these include a polyglycerol teichoic acid and a glucose/galactosamine-containing teichoic acid. However, when cultures are subjected to phosphate stress the bacterium induces a complex series of responses, one of which is the replacement of at least part of the wall teichoic acid with teichuronic acid, a non-phosphate- containing anionic polymer. In this paper the construction of a transcriptional reporter strain that facilitates the monitoring of the promoter region upstream of the operon involved in teichuronic acid synthesis and its controlled expression are reported. The expression of the operon was monitored in both phosphate-starved, non-growing batch cultures and phosphate-limited continuous cultures. We show that the transcription of the operon correlates well with the anionic polymer composition of the cell walls.

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1999-12-01
2020-04-07
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References

  1. Ames B. N.. 1966; Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol8:115–118
    [Google Scholar]
  2. Anagnostopoulos C., Spizizen J.. 1961; Requirements for transformation in Bacillus subtilis. J Bacteriol81:741–746
    [Google Scholar]
  3. Archibald A. R., Hancock I. C., Harwood C. R.. 1993; Cell wall structure, synthesis and turnover. In Bacillus subtilis and Other Gram-positive Bacteria: Biochemistry, Physiology and Molecular Genetics pp. 381–410Edited by Sonenshein A. L., Hock J. A., Losick R.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  4. Blumenkrantz N., Asboe-Hansen G.. 1973; New method for the quantitative determination of uronic acids. Anal Biochem54:484–489[CrossRef]
    [Google Scholar]
  5. Boylan R. J., Mendelson N. H., Brooks D., Young F. E.. 1972; Regulation of the cell wall: analysis of a mutant of Bacillus subtilis defective in biosynthesis of teichoic acid. J Bacteriol110:281–290
    [Google Scholar]
  6. Bron S.. 1990; Plasmids. In Molecular Biological Methods for Bacillus. pp. 75–174Edited by Harwood C. R., Cutting S. M.. Chichester: Wiley;
  7. Chen P. S., Toribara T. Y., Warner H.. 1956; Micro-determination of phosphorus. Anal Chem28:1756–1761[CrossRef]
    [Google Scholar]
  8. Ellwood D. C., Tempest D. W.. 1969; Control of teichoic acid and teichuronic acid biosynthesis in chemostat cultures of Bacillus subtilis var. niger. J Biochem111:1–5
    [Google Scholar]
  9. Eymann C., Mach H., Harwood C. R., Hecker M.. 1996; Phosphate-starvation inducible proteins in Bacillus subtilis: a two-dimensional gel electrophoresis study. Microbiology142:3163–3170[CrossRef]
    [Google Scholar]
  10. Grant W. D.. 1979; Cell wall teichoic acid as a reservoir phosphate source in Bacillus subtilis. J Bacteriol 13735–43
    [Google Scholar]
  11. Hoch J. A.. 1998; Initiation of bacterial development. Curr Opin Microbiol1:170–174[CrossRef]
    [Google Scholar]
  12. Hulett F. M.. 1993; Regulation of phosphorus metabolism. In Bacillus subtilis and Other Gram-positive Bacteria: Biochemistry, Physiology and Molecular Genetics. pp. 229–235Edited by Sonenshein A. L., Hock J. A., Losick R.. Washington, DC: American Society for Microbiology;
  13. Hulett F. M.. 1995; Complex phosphate regulation by sequential switches in Bacillus subtilis. In Two Component Signal Transduction pp. 289–302Edited by Hoch J. A., Silhavy T. J.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  14. Hulett F. M., Lee J., Shi L., Sun G., Chesnut R., Sharkova E., Duggan M. F., Kapp N.. 1994a; Sequential action of two component genetic switches regulates the Pho regulon in Bacillus subtilis. J Bacteriol176:1348–1358
    [Google Scholar]
  15. Hulett F. M., Sun G., Liu W.. 1994b; The Pho regulon of Bacillus subtilis is regulated by sequential action of two genetic switches. In Phosphate in Micro-organisms, Cellular and Molecular Biology pp. 50–54Edited by Torriani-Gorini A., Yogil E., Silver S.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  16. Itoh T., Aiba H., Baba T.. 22 other authors 1996; A 460-kb DNA sequence of the Escherichia coli K-12 genome corresponding to the 40·1–50·0 min region on the linkage map. DNA Res3:379–392[CrossRef]
    [Google Scholar]
  17. Jensen K. K., Sharkova E., Duggan M. F., Qi Y., Koide A., Hoch J. A., Hulett F. M.. 1993; Bacillus subtilis transcription regulator, Spo0A, decreases alkaline phosphatase levels induced by phosphate starvation. J Bacteriol175:3749–3756
    [Google Scholar]
  18. Kunst F., Ogasawara N., Moszer I.. & 148 other authors. 1997; The complete genome sequence of the Gram- positive bacterium Bacillus subtilis. Nature390:249–256[CrossRef]
    [Google Scholar]
  19. Lang W. K., Glassy K., Archibald A. R.. 1982; Influence of phosphate supply on teichoic and teichuronic acid content of Bacillus subtilis walls. J Bacteriol151:367–375
    [Google Scholar]
  20. Lazarevic V., Margot P., Soldo B., Karamata D.. 1992; Sequencing and analysis of the Bacillus subtilis lytRABC divergon: a regulatory unit encompassing the structural genes of the N-acetylmuramoyl-l-alanine amidase and its modifier. J Gen Microbiol138:1949–1961[CrossRef]
    [Google Scholar]
  21. Liu W., Hulett F. M.. 1998; Comparison of PhoP binding to the tuaA promoter with PhoP binding to other Pho regulon promoters establishes a Bacillus subtilis Pho core binding site. Microbiology144:1443–1450[CrossRef]
    [Google Scholar]
  22. Makino K., Shinagawa H., Nakata A.. 1985; Regulation of the phosphate regulon of Escherichia coli K-12: regulation and role of the regulatory gene phoR. J Mol Biol184:231–240[CrossRef]
    [Google Scholar]
  23. Makino K., Shinagawa H., Amemura M., Nakata A.. 1986; Nucleotide sequence of the phoR gene, a regulatory gene of the phosphate regulon of Escherichia coli. J Mol Biol192:549–556[CrossRef]
    [Google Scholar]
  24. Mauël C., Young M., Monsutti-Grecescu A., Marriott S. A., Karamata D.. 1994; Analysis of Bacillus subtilis tag gene expression using transcription fusion. Microbiology140:2279–2288[CrossRef]
    [Google Scholar]
  25. Merad T., Archibald A. R., Hancock I. C., Harwood C. R., Hobot J. A.. 1989; Cell wall assembly in Bacillus subtilis: Visualization of old and new wall material by electron microscopic examination of samples stained selectively for teichoic acid and teichuronic acid. J Gen Microbiol135:645–655
    [Google Scholar]
  26. Miller J. H.. 1972; Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  27. Müller J. P., An Z., Merad T., Hancock I. C., Harwood C. R.. 1997; Influence of Bacillus subtilis phoR on cell wall anionic polymers. Microbiology143947–956[CrossRef]
    [Google Scholar]
  28. Nicholson W. L., Setlow P.. 1990; Sporulation, germination and outgrowth. In Molecular Biological Methods for Bacillus pp. 391–450Edited by Harwood C. R., Cutting S. M.. Chichester: Wiley;
    [Google Scholar]
  29. Qi Y., Hulett F. M.. 1998; Role of PhoP∼P in transcriptional regulation of genes involved in cell wall anionic polymer biosynthesis in Bacillus subtilis. J Bacteriol180:4007–4010
    [Google Scholar]
  30. Qi Y., Kobayashi Y., Hulett F. M.. 1997; The pst operon of Bacillus subtilis has a phosphate-regulated promoter and is involved in phosphate transport but not in regulation of the pho regulon. J Bacteriol179:2534–2539
    [Google Scholar]
  31. Sambrook J., Fritsch E. F., Maniatis T.. 1989; Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  32. Seki T., Yoshikawa H., Takahashi H., Saito H.. 1987; Cloning and nucleotide sequence of phoP, the regulatory gene for alkaline phosphatase and phosphodiesterase in Bacillus subtilis. J Bacteriol169:2913–2916
    [Google Scholar]
  33. Seki T., Yoshikawa H., Takahashi H., Saito H.. 1988; Nucleotide sequence of the Bacillus subtilis phoR gene. J Bacteriol170:5935–5938
    [Google Scholar]
  34. Soldo B., Lazarevic V., Pagni M., Karamata D.. 1999; Teichuronic acid operon of Bacillus subtilis 168. Mol Microbiol31:795–805[CrossRef]
    [Google Scholar]
  35. Spizizen J.. 1958; Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Proc Natl Acad Sci USA44:1072–1078[CrossRef]
    [Google Scholar]
  36. Stevenson G., Andrianopoulos K., Hobbs M., Reeves P. R.. 1996; Organization of the Escherichia coli K-12 gene cluster responsible for production of the extracellular polysaccharide colanic acid. J Bacteriol178:4885–4893
    [Google Scholar]
  37. Takemaru K., Mizuno M., Kobayashi Y.. 1996; A Bacillus subtilis gene cluster similar to the Escherichia coli phosphate-specific transport (pst) operon: evidence for a tandemly arranged pstB gene. Microbiology142:2017–2020[CrossRef]
    [Google Scholar]
  38. Tinoco I., Borer P. N., Dengler B., Levin M. D., Uhlenbeck O. C., Crothers D. M., Bralla J.. 1973; Improved estimation of secondary structure in ribonucleic acids. Nature New Biol246:40–41[CrossRef]
    [Google Scholar]
  39. Tommassen J., de Geus P., Lugtenberg B., Hackett J., Reeves P.. 1982; Regulation of the Pho regulon of Escherichia coli K-12, cloning of the regulatory genes phoB and phoR and identification of their gene products. J Mol Biol 157265–274[CrossRef]
    [Google Scholar]
  40. Vagner V., Dervyn E., Ehrlich S. D.. 1998; A vector for systematic gene inactivation in Bacillus subtilis. Microbiology144:3097–3104[CrossRef]
    [Google Scholar]
  41. Yamane K., Maruo B.. 1978; Alkaline phosphatase possessing alkaline phosphodiesterase activity and other phosphodiesterases in Bacillus subtilis. J Bacteriol134:108–114
    [Google Scholar]
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