1887

Abstract

The transport of inorganic phosphate (P) is essential for the growth of all organisms. The metabolism of soil-dwelling species, and their ability to produce antibiotics and other secondary metabolites, are strongly influenced by the availability of phosphate. The transcriptional regulation of the SCO4138 and SCO1845 genes of was studied. These genes encode the two putative low-affinity P transporters PitH1 and PitH2, respectively. Expression of these genes and that of the high-affinity transport system follows a sequential pattern in response to phosphate deprivation, as shown by coupling their promoters to a luciferase reporter gene. Expression of , but not that of (a bicistronic transcript), is dependent upon the response regulator PhoP. PhoP binds to specific sequences consisting of direct repeats of 11 nt in the promoter of , but does not bind to the promoter, which lacks these direct repeats for PhoP recognition. The transcription start point of the promoter was identified by primer extension analyses, and the structure of the regulatory sequences in the PhoP-protected DNA region was established. It consists of four central direct repeats flanked by two other less conserved repeats. A model for PhoP regulation of this promoter is proposed based on the four promoter DNA–PhoP complexes detected by electrophoretic mobility shift assays and footprinting studies.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2008/019539-0
2008-08-01
2019-10-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/8/2356.html?itemId=/content/journal/micro/10.1099/mic.0.2008/019539-0&mimeType=html&fmt=ahah

References

  1. Altermann, E., Klein, J. R. & Henrich, B. ( 1999; ). Synthesis and automated detection of fluorescently labeled primer extension products. Biotechniques 26, 96–101.
    [Google Scholar]
  2. Álvarez, S. & Jerez, C. A. ( 2004; ). Copper ions stimulate polyphosphate degradation and phosphate efflux in Acidithiobacillus ferrooxidans. Appl Environ Microbiol 70, 5177–5182.[CrossRef]
    [Google Scholar]
  3. Apel, A. K., Sola-Landa, A., Rodríguez-García, A. & Martín, J. F. ( 2007; ). Phosphate control of phoA, phoC and phoD gene expression in Streptomyces coelicolor reveals significant differences in binding of PhoP to their promoter regions. Microbiology 153, 3527–3537.[CrossRef]
    [Google Scholar]
  4. Bardin, S. D. & Finan, T. M. ( 1998; ). Regulation of phosphate assimilation in Rhizobium (Sinorhizobium) meliloti. Genetics 148, 1689–1700.
    [Google Scholar]
  5. Bardin, S. D., Voegele, R. T. & Finan, T. M. ( 1998; ). Phosphate assimilation in Rhizobium (Sinorhizobium) meliloti: identification of a pit-like gene. J Bacteriol 180, 4219–4226.
    [Google Scholar]
  6. Beard, S. J., Hashim, R., Wu, G., Binet, M. R., Hughes, M. N. & Poole, R. K. ( 2000; ). Evidence for the transport of zinc(II) ions via the Pit inorganic phosphate transport system in Escherichia coli. FEMS Microbiol Lett 184, 231–235.[CrossRef]
    [Google Scholar]
  7. Bendtsen, J. D., Nielsen, H., von Heijne, G. & Brunak, S. ( 2004; ). Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340, 783–795.[CrossRef]
    [Google Scholar]
  8. Bentley, S. D., Chater, K. F., Cerdeno-Tarraga, A. M., Challis, G. L., Thomson, N. R., James, K. D., Harris, D. E., Quail, M. A., Kieser, H. & other authors ( 2002; ). Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417, 141–147.[CrossRef]
    [Google Scholar]
  9. Bérdy, J. ( 2005; ). Bioactive microbial metabolites. J Antibiot (Tokyo) 58, 1–26.[CrossRef]
    [Google Scholar]
  10. Braibant, M., Lefevre, P., de Wit, L., Ooms, J., Peirs, P., Huygen, K., Wattiez, R. & Content, J. ( 1996; ). Identification of a second Mycobacterium tuberculosis gene cluster encoding proteins of an ABC phosphate transporter. FEBS Lett 394, 206–212.[CrossRef]
    [Google Scholar]
  11. Chater, K. F. & Bibb, M. J. ( 1997; ). Regulation of Bacterial Antibiotic Production. In Biotechnology, vol. 7: Products of Secondary Metabolism, pp 57–105. Edited by H. Kleinkauf & H. von Döhren. Weinheim, Germany: VCH.
  12. Claros, M. G. & von Heijne, G. ( 1994; ). TopPred II: an improved software for membrane protein structure predictions. Comput Appl Biosci 10, 685–686.
    [Google Scholar]
  13. Desper, R. & Gascuel, O. ( 2002; ). Fast and accurate phylogeny reconstruction algorithms based on the minimum-evolution principle. J Comput Biol 9, 687–705.[CrossRef]
    [Google Scholar]
  14. Díaz, M., Esteban, A., Fernandez-Abalos, J. M. & Santamaria, R. I. ( 2005; ). The high-affinity phosphate-binding protein PstS is accumulated under high fructose concentrations and mutation of the corresponding gene affects differentiation in Streptomyces lividans. Microbiology 151, 2583–2592.[CrossRef]
    [Google Scholar]
  15. Doull, J. L. & Vining, L. C. ( 1989; ). Culture conditions promoting dispersed growth and biphasic production of actinorhodin in shaken cultures of Streptomyces coelicolor A3(2). FEMS Microbiol Lett 53, 265–268.
    [Google Scholar]
  16. Eder, S., Liu, W. & Hulett, F. M. ( 1999; ). Mutational analysis of the phoD promoter in Bacillus subtilis: implications for PhoP binding and promoter activation of Pho regulon promoters. J Bacteriol 181, 2017–2025.
    [Google Scholar]
  17. Elvin, C. M., Dixon, N. E. & Rosenberg, H. ( 1986; ). Molecular cloning of the phosphate (inorganic) transport (pit) gene of Escherichia coli K12. Identification of the pit+ gene product and physical mapping of the pit–gor region of the chromosome. Mol Gen Genet 204, 477–484.[CrossRef]
    [Google Scholar]
  18. Fekete, R. A., Miller, M. J. & Chattoraj, D. K. ( 2003; ). Fluorescently labeled oligonucleotide extension, a rapid and quantitative protocol for primer extension. Biotechniques 35, 90–98.
    [Google Scholar]
  19. Gebhard, S., Tran, S. L. & Cook, G. M. ( 2006; ). The Phn system of Mycobacterium smegmatis: a second high-affinity ABC-transporter for phosphate. Microbiology 152, 3453–3465.[CrossRef]
    [Google Scholar]
  20. Ghorbel, S., Smirnov, A., Chouayekh, H., Sperandio, B., Esnault, C., Kormanec, J. & Virolle, M. J. ( 2006; ). Regulation of ppk expression and in vivo function of Ppk in Streptomyces lividans TK24. J Bacteriol 188, 6269–6276.[CrossRef]
    [Google Scholar]
  21. Hahn, M. Y., Bae, J. B., Park, J. H. & Roe, J. H. ( 2003; ). Isolation and characterization of Streptomyces coelicolor RNA polymerase, its sigma, and antisigma factors. Methods Enzymol 370, 73–82.
    [Google Scholar]
  22. Hanahan, D. ( 1983; ). Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166, 557–580.[CrossRef]
    [Google Scholar]
  23. Harris, R. M., Webb, D. C., Howitt, S. M. & Cox, G. B. ( 2001; ). Characterization of PitA and PitB from Escherichia coli. J Bacteriol 183, 5008–5014.[CrossRef]
    [Google Scholar]
  24. Hidalgo, E. & Demple, B. ( 1997; ). Spacing of promoter elements regulates the basal expression of the soxS gene and converts SoxR from a transcriptional activator into a repressor. EMBO J 16, 1056–1065.[CrossRef]
    [Google Scholar]
  25. Higgens, C. E., Hamill, R. L., Sands, T. H., Hoehn, M. M. & Davis, N. E. ( 1974; ). Letter: the occurrence of deacetoxycephalosporin C in fungi and streptomycetes. J Antibiot (Tokyo) 27, 298–300.[CrossRef]
    [Google Scholar]
  26. 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 Bacteriol 183, 4659–4663.[CrossRef]
    [Google Scholar]
  27. Hofmann, K. & Stoffel, W. ( 1993; ). TMbase: a database of membrane spanning proteins segments. Biol Chem Hoppe Seyler 374, 166
    [Google Scholar]
  28. Ikeda, H., Ishikawa, J., Hanamoto, A., Shinose, M., Kikuchi, H., Shiba, T., Sakaki, Y., Hattori, M. & Omura, S. ( 2003; ). Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21, 526–531.[CrossRef]
    [Google Scholar]
  29. Kanehisa, M., Goto, S., Hattori, M., Aoki-Kinoshita, K. F., Itoh, M., Kawashima, S., Katayama, T., Araki, M. & Hirakawa, M. ( 2006; ). From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34, ((database issue)), D354–D357.[CrossRef]
    [Google Scholar]
  30. Keasling, J. D. ( 1997; ). Regulation of intracellular toxic metals and other cations by hydrolysis of polyphosphate. Ann N Y Acad Sci 829, 242–249.[CrossRef]
    [Google Scholar]
  31. Kieser, T., Bibb, M. J., Buttner, M. J., Chater, K. F. & Hopwood, D. A. ( 2000; ). Practical Streptomyces Genetics. Norwich, UK: The John Innes Foundation.
  32. Lanzetta, P. A., Álvarez, L. J., Reinach, P. S. & Candia, O. A. ( 1979; ). Improved assay for nanomole amounts of inorganic phosphate. Anal Biochem 100, 95–97.[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 Microbiol 28, 119–130.
    [Google Scholar]
  34. MacNeil, D. J., Gewain, K. M., Ruby, C. L., Dezeny, G., Gibbons, P. H. & MacNeil, T. ( 1992; ). Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene 111, 61–68.[CrossRef]
    [Google Scholar]
  35. Makarewicz, O., Dubrac, S., Msadek, T. & Borriss, R. ( 2006; ). Dual role of the PhoP-P response regulator: Bacillus amyloliquefaciens FZB45 phytase gene transcription is directed by positive and negative interactions with the phyC promoter. J Bacteriol 188, 6953–6965.[CrossRef]
    [Google Scholar]
  36. Marcos, A. T., Gutirrrez, S., Diez, B., Fernfindez, F. J., Oguiza, J. A. & Martin, J. F. ( 1995; ). Three genes hrdB, hrdD and hrdT of Streptomyces griseus IMRU 3570, encoding sigma factor-like proteins, are differentially expressed under specific nutritional conditions. Gene 153, 41–48.[CrossRef]
    [Google Scholar]
  37. Martín, J. F. & Demain, A. L. ( 1977; ). Cleavage of adenosine 5′-monophosphate during uptake by Streptomyces griseus. J Bacteriol 132, 590–595.
    [Google Scholar]
  38. Martín, J. F. & Demain, A. L. ( 1980; ). Control of antibiotic synthesis. Microbiol Rev 44, 230–251.
    [Google Scholar]
  39. Martín, J. F., Marcos, A. T., Martín, A., Asturias, J. A. & Liras, P. ( 1994; ). Phosphate control of antibiotic biosynthesis at the transcriptional level. In Phosphate in Microorganisms: Cellular and Molecular Biology, pp. 140–147. Edited by A. Torriani-Gorini, E. Yagil & S. Silver. Washington, DC: American Society for Microbiology.
  40. Mendes, M. V., Tunca, S., Antón, N., Recio, E., Sola-Landa, A., Aparicio, J. F. & Martín, J. F. ( 2007; ). The two-component phoR–phoP system of Streptomyces natalensis: Inactivation or deletion of phoP reduces the negative phosphate regulation of pimaricin biosynthesis. Metab Eng 9, 217–227.[CrossRef]
    [Google Scholar]
  41. Minnig, K., Lazarevic, V., Soldo, B. & Mauël, C. ( 2005; ). Analysis of teichoic acid biosynthesis regulation reveals that the extracytoplasmic function sigma factor σ M is induced by phosphate depletion in Bacillus subtilis W23. Microbiology 151, 3041–3049.[CrossRef]
    [Google Scholar]
  42. Nikata, T., Sakai, Y., Shibat, K., Kato, J., Kuroda, A. & Ohtake, H. ( 1996; ). Molecular analysis of the phosphate-specific transport (pst) operon of Pseudomonas aeruginosa. Mol Gen Genet 250, 692–698.
    [Google Scholar]
  43. Omura, S., Ikeda, H., Ishikawa, J., Hanamoto, A., Takahashi, C., Shinose, M., Takahashi, Y., Horikawa, H., Nakazawa, H. & other authors ( 2001; ). Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc Natl Acad Sci U S A 98, 12215–12220.[CrossRef]
    [Google Scholar]
  44. Paul, S., Birkey, S., Liu, W. & Hulett, F. M. ( 2004; ). Autoinduction of Bacillus subtilis phoPR operon transcription results from enhanced transcription from Eσ A- and Eσ E-responsive promoters by phosphorylated PhoP. J Bacteriol 186, 4262–4275.[CrossRef]
    [Google Scholar]
  45. Rao, N. N. & Torriani, A. ( 1990; ). Molecular aspects of phosphate transport in Escherichia coli. Mol Microbiol 4, 1083–1090.[CrossRef]
    [Google Scholar]
  46. Rice, P., Longden, I. & Bleasby, A. ( 2000; ). EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16, 276–277.[CrossRef]
    [Google Scholar]
  47. Rodríguez-García, A., Ludovice, M., Martín, J. F. & Liras, P. ( 1997; ). Arginine boxes and the argR gene in Streptomyces clavuligerus: evidence for a clear regulation of the arginine pathway. Mol Microbiol 25, 219–228.[CrossRef]
    [Google Scholar]
  48. Rodríguez-García, A., Barreiro, C., Santos-Beneit, F., Sola-Landa, A. & Martín, J. F. ( 2007; ). Genome-wide transcriptomic and proteomic analysis of the primary response to phosphate limitation in Streptomyces coelicolor M145 and in a ΔphoP mutant. Proteomics 7, 2410–2429.[CrossRef]
    [Google Scholar]
  49. Rosenberg, H., Gerdes, R. G. & Chegwidden, K. ( 1977; ). Two systems for the uptake of phosphate in Escherichia coli. J Bacteriol 131, 505–511.
    [Google Scholar]
  50. Rosenberg, H., Gerdes, R. G. & Harold, F. M. ( 1979; ). Energy coupling to the transport of inorganic phosphate in Escherichia coli K12. Biochem J 178, 133–137.
    [Google Scholar]
  51. Russell, L. M. & Rosenberg, H. ( 1980; ). The nature of the link between potassium transport and phosphate transport in Escherichia coli. Biochem J 188, 715–723.
    [Google Scholar]
  52. Saier, M. H., Jr, Eng, B. H., Fard, S., Garg, J., Haggerty, D. A., Hutchinson, W. J., Jack, D. L., Lai, E. C., Liu, H. J. & other authors ( 1999; ). Phylogenetic characterization of novel transport protein families revealed by genome analyses. Biochim Biophys Acta 1422, 1–56.[CrossRef]
    [Google Scholar]
  53. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  54. Schaaf, S. & Bott, M. ( 2007; ). Target genes and DNA-binding sites of the response regulator PhoR from Corynebacterium glutamicum. J Bacteriol 189, 5002–5011.[CrossRef]
    [Google Scholar]
  55. Schneider, T. D. ( 1996; ). Reading of DNA sequence logos: prediction of major groove binding by information theory. Methods Enzymol 274, 445–455.
    [Google Scholar]
  56. Schneider, T. D. ( 1997; ). Sequence walkers: a graphical method to display how binding proteins interact with DNA or RNA sequences. Nucleic Acids Res 25, 4408–4415.[CrossRef]
    [Google Scholar]
  57. Schneider, T. D. & Stephens, R. M. ( 1990; ). Sequence logos: a new way to display consensus sequences. Nucleic Acids Res 18, 6097–6100.[CrossRef]
    [Google Scholar]
  58. Sola-Landa, A., Moura, R. S. & Martín, 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 A 100, 6133–6138.[CrossRef]
    [Google Scholar]
  59. Sola-Landa, A., Rodríguez-García, A., Franco-Dominguez, E. & Martín, J. F. ( 2005; ). Binding of PhoP to promoters of phosphate-regulated genes in Streptomyces coelicolor: identification of PHO boxes. Mol Microbiol 56, 1373–1385.[CrossRef]
    [Google Scholar]
  60. Sola-Landa, A., Rodríguez-García, A., Apel, A. K. & Martín, J. F. ( 2008; ). Target genes and structure of the direct repeats in the DNA-binding sequences of the response regulator PhoP in Streptomyces coelicolor. Nucleic Acids Res 36, 1358–1368.
    [Google Scholar]
  61. Strohl, W. R. ( 1992; ). Compilation and analysis of DNA sequences associated with apparent streptomycete promoters. Nucleic Acids Res 20, 961–974.[CrossRef]
    [Google Scholar]
  62. van Veen, H. W. ( 1997; ). Phosphate transport in prokaryotes: molecules, mediators and mechanisms. Antonie Van Leeuwenhoek 72, 299–315.[CrossRef]
    [Google Scholar]
  63. van Veen, H. W., Abee, T., Kortstee, G. J., Konings, W. N. & Zehnder, A. J. ( 1993; ). Characterization of two phosphate transport systems in Acinetobacter johnsonii 210A. J Bacteriol 175, 200–206.
    [Google Scholar]
  64. van Veen, H. W., Abee, T., Kortstee, G. J., Konings, W. N. & Zehnder, A. J. ( 1994a; ). Translocation of metal phosphate via the phosphate inorganic transport system of Escherichia coli. Biochemistry 33, 1766–1770.[CrossRef]
    [Google Scholar]
  65. van Veen, H. W., Abee, T., Kortstee, G. J., Konings, W. N. & Zehnder, A. J. ( 1994b; ). Substrate specificity of the two phosphate transport systems of Acinetobacter johnsonii 210A in relation to phosphate speciation in its aquatic environment. J Biol Chem 269, 16212–16216.
    [Google Scholar]
  66. van Veen, H. W., Abee, T., Kortstee, G. J., Pereira, H., Konings, W. N. & Zehnder, A. J. ( 1994c; ). Generation of a proton motive force by the excretion of metal-phosphate in the polyphosphate-accumulating Acinetobacter johnsonii strain 210A. J Biol Chem 269, 29509–29514.
    [Google Scholar]
  67. Voegele, R. T., Bardin, S. & Finan, T. M. ( 1997; ). Characterization of the Rhizobium (Sinorhizobium) meliloti high- and low-affinity phosphate uptake systems. J Bacteriol 179, 7226–7232.
    [Google Scholar]
  68. von Mering, C., Jensen, L. J., Kuhn, M., Chaffron, S., Doerks, T., Kruger, B., Snel, B. & Bork, P. ( 2007; ). STRING 7 – recent developments in the integration and prediction of protein interactions. Nucleic Acids Res 35, (database issue), D358–D362.[CrossRef]
    [Google Scholar]
  69. Whitworth, D. E., Holmes, A. B., Irvine, A. G., Hodgson, D. A. & Scanlan, D. J. ( 2008; ). Phosphate acquisition components of the Myxococcus xanthus Pho regulon are regulated by both phosphate availability and development. J Bacteriol 190, 1997–2003.[CrossRef]
    [Google Scholar]
  70. Yuan, Z. C., Zaheer, R. & Finan, T. M. ( 2006a; ). Regulation and properties of PstSCAB, a high-affinity, high-velocity phosphate transport system of Sinorhizobium meliloti. J Bacteriol 188, 1089–1102.[CrossRef]
    [Google Scholar]
  71. Yuan, Z. C., Zaheer, R., Morton, R. & Finan, T. M. ( 2006b; ). Genome prediction of PhoB regulated promoters in Sinorhizobium meliloti and twelve proteobacteria. Nucleic Acids Res 34, 2686–2697.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2008/019539-0
Loading
/content/journal/micro/10.1099/mic.0.2008/019539-0
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