1887

Abstract

The secreted protein pattern of depends on the carbon source present in the culture media. One protein that shows the most dramatic change is the high-affinity phosphate-binding protein PstS, which is strongly accumulated in the supernatant of liquid cultures containing high concentrations (>3 %) of certain sugars, such as fructose, galactose and mannose. The promoter region of this gene and that of its homologue were used to drive the expression of a xylanase in that was accumulated in the culture supernatant when grown in the presence of fructose. PstS accumulation was dramatically increased in a polyphosphate kinase null mutant (Δ) and was impaired in a deletion mutant lacking , the transcriptional regulator gene of the two-component system that controls the Pho regulon. Deletion of the genes in and impaired phosphate transport and accelerated differentiation and sporulation on solid media. Complementation with a single copy in a null mutant returned phosphate transport and sporulation to levels similar to those of the wild-type strain. The present work demonstrates that carbon and phosphate metabolism are linked in the regulation of genes and that this can trigger the genetic switch towards morphogenesis.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27983-0
2005-08-01
2020-07-09
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/8/mic1512583.html?itemId=/content/journal/micro/10.1099/mic.0.27983-0&mimeType=html&fmt=ahah

References

  1. Adham S. A., Honrubia P., Gil J. A, Díaz, M., Fernández-Ábalos, J. M., Santamaría, R. I.. 2001; Expression of the genes coding for the xylanase Xys1 and the cellulase Cel1 from the straw-decomposing. Streptomyces halstedii. JM8 cloned into the amino-acid producer Brevibacterium lactofermentum ATCC13869. Arch Microbiol 17791–97[CrossRef]
    [Google Scholar]
  2. Aguena M., Yagil E., Spira B. 2002; Transcriptional analysis of the pst operon of Escherichia coli. Mol Genet Genomics268:518–524[CrossRef]
    [Google Scholar]
  3. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res25:3389–3402[CrossRef]
    [Google Scholar]
  4. Angell S., Lewis C. G., Buttner M. J., Bibb M. J. 1994; Glucose repression in Streptomyces coelicolor A3(2): a likely regulatory role for glucose kinase. Mol Gen Genet244:135–143
    [Google Scholar]
  5. Antelmann H., Scharf C., Hecker M. 2000; Phosphate starvation-inducible proteins of Bacillus subtilis: proteomics and transcriptional analysis. J Bacteriol182:4478–4490[CrossRef]
    [Google Scholar]
  6. Atalla A., Schumann W. 2003; The pst operon of Bacillus subtilis is specifically induced by alkali stress. J Bacteriol185:5019–5022[CrossRef]
    [Google Scholar]
  7. Bertram R., Schlicht M., Mahr K., Nothaft H., Saier M. H. Jr, Titgemeyer F. 2004; In silico and transcriptional analysis of carbohydrate uptake systems of Streptomyces coelicolor A3(2). J Bacteriol186:1362–1373[CrossRef]
    [Google Scholar]
  8. Blanco A. G., Sola M., Gomis-Ruth F. X., Coll M. 2002; Tandem DNA recognition by PhoB, a two-component signal transduction transcriptional activator. Structure (Camb)10:701–713[CrossRef]
    [Google Scholar]
  9. Chang Z., Choudhary A., Lathigra R., Quiocho F. A. 1994; The immunodominant 38-kDa lipoprotein antigen of Mycobacterium tuberculosis is a phosphate-binding protein. J Biol Chem269:1956–1958
    [Google Scholar]
  10. Chouayekh H., Virolle M. J. 2002; The polyphosphate kinase plays a negative role in the control of antibiotic production in Streptomyces lividans. Mol Microbiol43:919–930[CrossRef]
    [Google Scholar]
  11. Daza A., Gil J. A, Martín J. F., Domínguez A.. 1989; Sporulation of several species of Streptomyces in submerged cultures after nutritional downshift. J Gen Microbiol135:2483–2491
    [Google Scholar]
  12. D'Souza S., Rosseels V., Denis O. & 8 other authors. 2002; Improved tuberculosis DNA vaccines by formulation in cationic lipids. Infect Immun70:3681–3688[CrossRef]
    [Google Scholar]
  13. Duwat P., Ehrlich S. D., Gruss A. 1999; Effects of metabolic flux on stress response pathways in Lactococcus lactis. Mol Microbiol31:845–858[CrossRef]
    [Google Scholar]
  14. Espitia C., Elinos M., Hernandez-Pando R., Mancilla R. 1992; Phosphate starvation enhances expression of the immunodominant 38-kilodalton protein antigen of Mycobacterium tuberculosis: demonstration by immunogold electron microscopy. Infect Immun60:2998–3001
    [Google Scholar]
  15. Fernández-Abalos J. M., Reviejo V, Leal F, Díaz, M., Rodríguez S., Santamaría R. I. 2003; Posttranslational processing of the xylanase Xys1L from Streptomyces halstedii JM8 is carried out by secreted serine proteases. Microbiology149:1623–1632[CrossRef]
    [Google Scholar]
  16. Ghorbel S., Virolle M. 2003; Regulation of the expression of the ppk gene from Streptomyces lividans encoding a polyphosphate kinase activity. Talk 18 in Biology of Streptomycetes and Related Actinomycetes. Symposium organized by H Schrempf at the University of Osnabrück;
    [Google Scholar]
  17. Gil J. A., Campelo-Diez A. B. 2003; Candicidin biosynthesis in Streptomyces griseus. Appl Microbiol Biotechnol60:633–642[CrossRef]
    [Google Scholar]
  18. Gust B., Challis G. L., Fowler K., Kieser T., Chater K. F. 2003; PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci U S A100:1541–1546[CrossRef]
    [Google Scholar]
  19. Hantke K. 2001; Bacterial zinc transporters and regulators. Biometals14:239–249[CrossRef]
    [Google Scholar]
  20. Harris R. M., Webb D. C., Howitt S. M., Cox G. B. 2001; Characterization of PitA and PitB from. Escherichia coli. J Bacteriol183:5008–5014[CrossRef]
    [Google Scholar]
  21. Hodgson D. A. 2000; Primary metabolism and its control in streptomycetes: a most unusual group of bacteria. Adv Microb Physiol42:47–238
    [Google Scholar]
  22. Hoffer S. M., Schoondermark P., van Veen H. W., Tommassen J. 2001; Activation by gene amplification of. pitB, encoding a third phosphate transporter of Escherichia coli. K-12. J Bacteriol183:4659–4663[CrossRef]
    [Google Scholar]
  23. Hopwood D. A. 1967; Genetic analysis and genome structure in Streptomyces coelicolor. Bacteriol Rev31:373–403
    [Google Scholar]
  24. Hulett F. M. 2002; The Pho regulon. In Bacillus subtilis and its Closest Relatives: from Genes to Cells pp193–201 Edited by Sonenshein A. L., Hoch J. A., Losick R.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  25. Hurtubise Y., Shareck F., Kluepfel D., Morosoli R. 1995; A cellulase/xylanase-negative mutant of Streptomyces lividans 1326 defective in cellobiose and xylobiose uptake is mutated in a gene encoding a protein homologous to ATP-binding proteins. Mol Microbiol17:367–377[CrossRef]
    [Google Scholar]
  26. Hutchings M. I., Hoskisson P. A., Chandra G., Buttner M. J. 2004; Sensing and responding to diverse extracellular signals? Analysis of the sensor kinases and response regulators of. Streptomyces coelicolor. A3(2). Microbiology150:2795–2806[CrossRef]
    [Google Scholar]
  27. Kieser T., Bibb M. J., Buttner M. J., Chater K. F., Hopwood D. A. 2000; Practical Streptomyces Genetics Norwich: John Innes Foundation;
    [Google Scholar]
  28. Kuhstoss S., Richardson M. A., Rao R. N. 1991; Plasmid cloning vectors that integrate site-specifically in Streptomyces spp. Gene97:143–146[CrossRef]
    [Google Scholar]
  29. Lanzetta P. A., Alvarez L. J., Reinach P. S., Candia O. A. 1979; An improved assay for nanomole amounts of inorganic phosphate. Anal Biochem100:95–97[CrossRef]
    [Google Scholar]
  30. Lefevre P., Braibant M, de Wit L..8 other authors 1997; Three different putative phosphate transport receptors are encoded by the Mycobacterium tuberculosis genome and are present at the surface of. Mycobacterium bovis. BCG. J Bacteriol179:2900–2996
    [Google Scholar]
  31. Licha I., Benes I., Janda S., Host'alek Z., Janacek K. 1997; Characterization of phosphate transport in Streptomyces granaticolor. Biochem Mol Biol Int41:431–437
    [Google Scholar]
  32. Liras P., Asturias J. A., Martin J. F. 1990; Phosphate control sequences involved in transcriptional regulation of antibiotic biosynthesis. Trends Biotechnol8:184–189[CrossRef]
    [Google Scholar]
  33. Liu W., Qi Y., Hulett F. M. 1998; Sites internal to the coding regions of phoA and pstS bind PhoP and are required for full promoter activity. Mol Microbiol28:119–130
    [Google Scholar]
  34. Marck C. 1988; ‘DNA Strider’: a ‘C’ program for the fast analysis of DNA and protein sequences on the Apple Macintosh family of computers. Nucleic Acids Res16:1829–1836[CrossRef]
    [Google Scholar]
  35. Martin J. F., Demain A. L. 1980; Control of antibiotic biosynthesis. Microbiol Rev44:230–251
    [Google Scholar]
  36. Martin J. F., McDaniel L. E. 1975; Specific inhibition of candicidin biosynthesis by the lipogenic inhibitor cerulenin. Biochim Biophys Acta411:186–194[CrossRef]
    [Google Scholar]
  37. Matsuzaki M., Abe M., Hara S., Iwasaki Y., Yamamoto I., Satoh T. 2003; An abundant periplasmic protein of the denitrifying phototroph Rhodobacter sphaeroides f. sp. denitrificans is PstS, a component of an ABC phosphate transport system. Plant Cell Physiol44:212–216[CrossRef]
    [Google Scholar]
  38. Nothaft H., Dresel D., Willimek A., Mahr K., Niederweis M., Titgemeyer F. 2003a; The phosphotransferase system of Streptomyces coelicolor is biased for N-acetylglucosamine metabolism. J Bacteriol185:7019–7023[CrossRef]
    [Google Scholar]
  39. Nothaft H., Parche S., Kamionka A., Titgemeyer F. 2003b; In vivo analysis of HPr reveals a fructose-specific phosphotransferase system that confers high-affinity uptake in. Streptomyces coelicolor. J Bacteriol185:929–937[CrossRef]
    [Google Scholar]
  40. Pearson W. R., Lipman D. J. 1988; Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A85:2444–2448[CrossRef]
    [Google Scholar]
  41. Qi Y., Hulett F. M. 1998; PhoP-P and RNA polymerase sigmaA holoenzyme are sufficient for transcription of Pho regulon promoters in Bacillus subtilis: PhoP-P activator sites within the coding region stimulate transcription in vitro. Mol Microbiol28:1187–1197[CrossRef]
    [Google Scholar]
  42. 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]
  43. Rallu F., Gruss A., Ehrlich S. D., Maguin E. 2000; Acid- and multistress-resistant mutants of Lactococcus lactis: identification of intracellular stress signals. Mol Microbiol35:517–528
    [Google Scholar]
  44. Ruiz-Arribas A., Fernandez-Abalos J. M., Sanchez P., Garda A. L., Santamaria R. I. 1995; Overproduction, purification, and biochemical characterization of a xylanase (Xys1) from. Streptomyces halstedii. JM8. Appl Environ Microbiol61:2414–2419
    [Google Scholar]
  45. Ruiz-Arribas A., Calvete J. J., Raida M, Sánchez P., Fernández-Abalos J. M., Santamaría R. I. 1997; Analysis of xysA, a gene from Streptomyces halstedii. JM8 that encodes a 45-kilodalton modular xylanase, Xys1. Appl Environ Microbiol632983–2988
    [Google Scholar]
  46. Runyen-Janecky L. J., Payne S. M. 2002; Identification of chromosomal Shigella flexneri genes induced by the eukaryotic intracellular environment. Infect Immun70:4379–4388[CrossRef]
    [Google Scholar]
  47. Sambrook J., Fritsch E., Maniatis T. 1989; Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  48. Santamaría R. I., Leal F, Díaz M., Fernández-Abalos J. M. 2002; Morphological and physiological changes in Streptomyces lividans induced by different yeasts. Arch Microbiol177:259–266[CrossRef]
    [Google Scholar]
  49. Schlösser A., Jantos J., Hackmann K., Schrempf H. 1999; Characterization of the binding protein-dependent cellobiose and cellotriose transport system of the cellulose degrader. Streptomyces reticuli. Appl Environ Microbiol65:2636–2643
    [Google Scholar]
  50. Slater H., Crow M., Everson L., Salmond G. P. 2003; Phosphate availability regulates biosynthesis of two antibiotics, prodigiosin and carbapenem, in Serratia via both quorum-sensing-dependent and -independent pathways. Mol Microbiol47:303–320
    [Google Scholar]
  51. Sola-Landa A., Moura R. S., Martin J. F. 2003; The two-component PhoR-PhoP system controls both primary metabolism and secondary metabolite biosynthesis in Streptomyces lividans. Proc Natl Acad Sci U S A100:6133–6138[CrossRef]
    [Google Scholar]
  52. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res22:4673–4680[CrossRef]
    [Google Scholar]
  53. Torriani A. 1990; From cell membrane to nucleotides: the phosphate regulon in Escherichia coli. Bioessays12:371–376[CrossRef]
    [Google Scholar]
  54. Trujillo M. E., Kroppenstedt R. M., Schumann P., Mateos P. F, Martínez-Molina E, Fernández-Molinero C., Velázquez E.. 2005; Micromonospora mirobrigensis sp. nov. Int J Syst Evol Microbiol55877–880[CrossRef]
    [Google Scholar]
  55. VanBogelen R. A., Olson E. R., Wanner B. L., Neidhardt F. C. 1996; Global analysis of proteins synthesized during phosphorus restriction in. Escherichia coli. J Bacteriol178:4344–4366
    [Google Scholar]
  56. van Helden J., Andre B., Collado-Vides J. 2000; A web site for the computational analysis of yeast regulatory sequences. Yeast16:177–187[CrossRef]
    [Google Scholar]
  57. van Wezel G. P., White J., Bibb M. J., Postma P. W. 1997; The malEFG gene cluster of Streptomyces coelicolor A3(2): characterization, disruption and transcriptional analysis. Mol Gen Genet254:604–608[CrossRef]
    [Google Scholar]
  58. van Wezel G. P., Mahr K., Konig M., Traag B. A., Pimentel-Schmitt E. F., Willimek A., Titgemeyer F. 2005; GlcP constitutes the major glucose uptake system of. Streptomyces coelicolor. A3(2). Mol Microbiol55:624–636
    [Google Scholar]
  59. Wang F., Xiao X., Saito A., Schrempf H. 2002; Streptomyces olivaceoviridis possesses a phosphotransferase system that mediates specific, phosphoenolpyruvate-dependent uptake of N-acetylglucosamine. Mol Genet Genomics268:344–351[CrossRef]
    [Google Scholar]
  60. Wanner B. L. 1993; Gene regulation by phosphate in enteric bacteria. J Cell Biochem51:47–54[CrossRef]
    [Google Scholar]
  61. Wanner B. L. 1996; Phosphorus assimilation and control of the phosphate regulon. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. pp1357–1381 Edited by Neidhardt F. C..others Washington, DC: American Society for Microbiology;
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27983-0
Loading
/content/journal/micro/10.1099/mic.0.27983-0
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