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Volume 155, Issue 6

Phosphate and carbon source regulation of two PhoP-dependent glycerophosphodiester phosphodiesterase genes of Free

Abstract

Glycerophosphodiesters are formed by deacylation of phospholipids. and other soil-dwelling actinomycetes utilize glycerophosphodiesters as phosphate and carbon sources by the action of glycerophosphodiester phosphodiesterases (GDPDs). Seven genes encoding putative GDPDs occur in the genome. Two of these genes, and , encoding extracellular GDPDs, showed a PhoP-dependent upregulated profile in response to phosphate shiftdown. Expression studies using the genes as reporter confirmed the PhoP dependence of both and . Footprinting analyses with pure GST-PhoP of the promoter revealed four protected direct repeat units (DRu). PhoP binding affinity to the promoter was lower and revealed a protected region containing five DRu. As expected for regulon genes, inorganic phosphate, and also glycerol 3-phosphate, inhibited the expression from both and . The expression of was also repressed by serine and inositol but expression of was not. In contrast, glucose, fructose and glycerol increased expression of but not that of . In summary, our results suggest an interaction of phosphate control mediated by PhoP and carbon source regulation of the and genes involving complex operator structures.

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  • Accepted:
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  • Published Online:
Keyword(s): CCR, carbon catabolite regulation , DRu, direct repeat unit(s) , EMSA, electrophoretic mobility shift assay , G3P, sn-glycerol 3-phosphate , GDPD, glycerophosphodiester phosphodiesterase , GST, glutathione S-transferase and TSP, transcription start point
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2009-06-01
2024-04-23
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References

  1. 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 Genet 244:135–143
     [Google Scholar]
  2. Antelmann H., Scharf C., Hecker M. 2000; Phosphate starvation-inducible proteins of Bacillus subtilis : proteomics and transcriptional analysis. J Bacteriol 182:4478–4490
     [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
     [Google Scholar]
  4. 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
     [Google Scholar]
  5. Brzoska P., Boos W. 1988; Characteristics of a ugp -encoded and phoB -dependent glycerophosphoryl diester phosphodiesterase which is physically dependent on the Ugp transport system of Escherichia coli . J Bacteriol 170:4125–4135
     [Google Scholar]
  6. Brzoska P., Boos W. 1989; The ugp -encoded glycerophosphoryldiester phosphodiesterase, a transport-related enzyme of Escherichia coli . FEMS Microbiol Rev 5:115–124
     [Google Scholar]
  7. Challis G. L., Hopwood D. A. 2003; Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci U S A 100 :Suppl. 214555–14561
     [Google Scholar]
  8. Díaz M., Esteban A., Fernández-Abalos J. M., Santamaría 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
     [Google Scholar]
  9. Divecha N., Irvine R. F. 1995; Phospholipid signaling. Cell 80:269–278
     [Google Scholar]
  10. 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]
  11. Esteban A., Díaz M., Yepes A., Santamaría R. I. 2008; Expression of the pstS gene of Streptomyces lividans is regulated by the carbon source and is partially independent of the PhoP regulator. BMC Microbiol 8:201
     [Google Scholar]
  12. Kasahara M., Makino K., Amemura M., Nakata A., Shinagawa H. 1991; Dual regulation of the ugp operon by phosphate and carbon starvation at two interspaced promoters. J Bacteriol 173:549–558
     [Google Scholar]
  13. Kieser T., Bibb M. J., Buttner M. J., Chater K. F., Hopwood D. A. 2000 Practical Streptomyces Genetics Norwich, UK: John Innes Foundation;
  14. Kwakman J. H., Postma P. W. 1994; Glucose kinase has a regulatory role in carbon catabolite repression in Streptomyces coelicolor . J Bacteriol 176:2694–2698
     [Google Scholar]
  15. Larson T. J., Ehrmann M., Boos W. 1983; Periplasmic glycerophosphodiester phosphodiesterase of Escherichia coli , a new enzyme of the glp regulon. J Biol Chem 258:5428–5432
     [Google Scholar]
  16. Larson T. J., Ye S. Z., Weissenborn D. L., Hoffmann H. J., Schweizer H. 1987; Purification and characterization of the repressor for the sn -glycerol 3-phosphate regulon of Escherichia coli K12. J Biol Chem 262:15869–15874
     [Google Scholar]
  17. 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
     [Google Scholar]
  18. Martín J. F., Demain A. L. 1980; Control of antibiotic synthesis. Microbiol Rev 44:230–251
     [Google Scholar]
  19. McLoughlin S. Y., Jackson C., Liu J. W., Ollis D. L. 2004; Growth of Escherichia coli coexpressing phosphotriesterase and glycerophosphodiester phosphodiesterase, using paraoxon as the sole phosphorus source. Appl Environ Microbiol 70:404–412
     [Google Scholar]
  20. Nilsson R. P., Beijer L., Rutberg B. 1994; The glpT and glpQ genes of the glycerol regulon in Bacillus subtilis . Microbiology 140:723–730
     [Google Scholar]
  21. Nogusa Y., Fujioka Y., Komatsu R., Kato N., Yanaka N. 2004; Isolation and characterization of two serpentine membrane proteins containing glycerophosphodiester phosphodiesterase, GDE2 and GDE6. Gene 337:173–179
     [Google Scholar]
  22. Oh W. S., Im Y. S., Yeon K. Y., Yoon Y. J., Kim J. W. 2007; Phosphate and carbon source regulation of alkaline phosphatase and phospholipase in Vibrio vulnificus . J Microbiol 45:311–317
     [Google Scholar]
  23. Overduin P., Boos W., Tommassen J. 1988; Nucleotide sequence of the ugp genes of Escherichia coli K-12: homology to the maltose system. Mol Microbiol 2:767–775
     [Google Scholar]
  24. Patton-Vogt J. 2007; Transport and metabolism of glycerophosphodiesters produced through phospholipid deacylation. Biochim Biophys Acta 1771:337–342
     [Google Scholar]
  25. Puri-Taneja A., Paul S., Chen Y., Hulett F. M. 2006; CcpA causes repression of the phoPR promoter through a novel transcription start site, P(A6. J Bacteriol 188:1266–1278
     [Google Scholar]
  26. Rao M., Sockanathan S. 2005; Transmembrane protein GDE2 induces motor neuron differentiation in vivo. Science 309:2212–2215
     [Google Scholar]
  27. 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 Δ phoP mutant. Proteomics 7:2410–2429
     [Google Scholar]
  28. Sage A. E., Vasil M. L. 1997; Osmoprotectant-dependent expression of plcH , encoding the hemolytic phospholipase C, is subject to novel catabolite repression control in Pseudomonas aeruginosa PAO1. J Bacteriol 179:4874–4881
     [Google Scholar]
  29. Santos-Beneit F., Rodríguez-García A., Franco-Domínguez E., Martín J. F. 2008; Phosphate-dependent regulation of the low- and high-affinity transport systems in the model actinomycete Streptomyces coelicolor . Microbiology 154:2356–2370
     [Google Scholar]
  30. Santos-Beneit F., Rodríguez-García A., Sola-Landa A., Martín J. F. 2009; Crosstalk between two global regulators in Streptomyces : PhoP and AfsR interact in the control of afsS, pstS and phoRP transcription. Mol Microbiol 72:53–68
     [Google Scholar]
  31. Schaaf S., Bott M. 2007; Target genes and DNA-binding sites of the response regulator PhoR from Corynebacterium glutamicum . J Bacteriol 189:5002–5011
     [Google Scholar]
  32. Schneider T. D. 1996; Reading of DNA sequence logos: prediction of major groove binding by information theory. Methods Enzymol 274:445–455
     [Google Scholar]
  33. Schneider T. D. 1997a; Information content of individual genetic sequences. J Theor Biol 189:427–441
     [Google Scholar]
  34. Schneider T. D. 1997b; Sequence walkers: a graphical method to display how binding proteins interact with DNA or RNA sequences. Nucleic Acids Res 25:4408–4415
     [Google Scholar]
  35. 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
     [Google Scholar]
  36. 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]
  37. Strohl W. R. 1992; Compilation and analysis of DNA sequences associated with apparent streptomycete promoters. Nucleic Acids Res 20:961–974
     [Google Scholar]
  38. Tommassen J., Eiglmeier K., Cole S. T., Overduin P., Larson T. J., Boos W. 1991; Characterization of two genes, glpQ and ugpQ , encoding glycerophosphoryl diester phosphodiesterases of Escherichia coli . Mol Gen Genet 226:321–327
     [Google Scholar]
  39. van Wezel G. P., König M., Mahr K., Nothaft H., Thomae A. W., Bibb M., Titgemeyer F. 2007; A new piece of an old jigsaw: glucose kinase is activated posttranslationally in a glucose transport-dependent manner in Streptomyces coelicolor A3(2. J Mol Microbiol Biotechnol 12:67–74
     [Google Scholar]
  40. Von Döhren H., Gräfe U. 1997; General aspects of secondary metabolism. In Biotechnology. Products of Secondary Metabolism vol. 7 pp 1–55 Edited by Kleinkauf H., von Doren H. Weinheim, Germany: VCH;
     [Google Scholar]
  41. Wanner B. L., Wilmes M. R., Young D. C. 1988; Control of bacterial alkaline phosphatase synthesis and variation in an Escherichia coli K-12 phoR mutant by adenyl cyclase, the cyclic AMP receptor protein, and the phoM operon. J Bacteriol 170:1092–1102
     [Google Scholar]
  42. Widdick D. A., Dilks K., Chandra G., Bottrill A., Naldrett M., Pohlschröder M., Palmer T. 2006; The twin-arginine translocation pathway is a major route of protein export in Streptomyces coelicolor . Proc Natl Acad Sci U S A 103:17927–17932
     [Google Scholar]
  43. Zheng B., Berrie C. P., Corda D., Farquhar M. G. 2003; GDE1/MIR16 is a glycerophosphoinositol phosphodiesterase regulated by stimulation of G protein-coupled receptors. Proc Natl Acad Sci U S A 100:1745–1750
     [Google Scholar]
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Phosphate and carbon source regulation of two PhoP-dependent glycerophosphodiester phosphodiesterase genes of Streptomyces coelicolor
Microbiology 155, 1800 (2009); https://doi.org/10.1099/mic.0.026799-0
/content/journal/micro/10.1099/mic.0.026799-0
/content/journal/micro/10.1099/mic.0.026799-0
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