Identification of two-component system AfsQ1/Q2 regulon and its cross-regulation with GlnR in Streptomyces coelicolor

Molecular Microbiology

Volumn 87, Issue 1, 2013, Pages 30-48

  Wang, Rui ^a,b   Mast, Yvonne ^c   Wang, Jin ^a   Zhang, Weiwen ^d   Zhao, Guoping ^a   Wohlleben, Wolfgang ^c   Lu, Yinhua ^a   Jiang, Weihong ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d TIANJIN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACTINORHODINE; ANTIBIOTIC AGENT; CALCIUM DEPENDENT ANTIBIOTIC; NITROGEN; UNCLASSIFIED DRUG; UNDECYLPRODIGIOSIN;

ACTII GENE; AFSQ1 GENE; AFSQ2 GENE; AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BINDING SITE; BLDM GENE; CDAR GENE; CONTROLLED STUDY; DEVELOPMENTAL GENE; DRUG SYNTHESIS; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; GLNA GENE; GLNR GENE; NIRB GENE; NITROGEN METABOLISM; NONHUMAN; OPEN READING FRAME; PREDICTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN MOTIF; PSTS GENE; REDZ GENE; REGULON; SIGQ GENE; SITE DIRECTED MUTAGENESIS; STREPTOMYCES COELICOLOR; WHID GENE;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DEOXYRIBONUCLEASE I; DNA FOOTPRINTING; DNA, BACTERIAL; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, BACTERIAL; GLUTAMIC ACID; MUTAGENESIS, SITE-DIRECTED; MUTATION; NITROGEN; PROMOTER REGIONS, GENETIC; REGULON; STREPTOMYCES COELICOLOR; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

STREPTOMYCES COELICOLOR;

EID: 84871404801     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12080     Document Type: Article

References (49)

1. Allenby, N.E., Laing, E., Bucca, G., Kierzek, A.M., and Smith, C.P. (2012) Diverse control of metabolism and other cellular processes in Streptomyces coelicolor by the PhoP transcription factor: genome-wide identification of in vivo targets. Nucleic Acids Res 40: 9543-9556.
2. Amin, R., Reuther, J., Bera, A., Wohlleben, W., and Mast, Y. (2012) Novel GlnR-target gene nnaR is involved in nitrate/nitrite assimilation in Streptomyces coelicolor. Microbiology 158: 1172-1182.
3. Apel, A.K., Sola-Landa, A., Rodriguez-Garcia, A., and Martin, 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.
4. Bentley, S.D., Chater, K.F., Cerdeno-Tarraga, A.M., Challis, G.L., Thomson, N.R., James, K.D., etal. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417: 141-147.
5. Bibb, M.J., Molle, V., and Buttner, M.J. (2000) sigma (BldN), an extracytoplasmic function RNA polymerase sigma factor required for aerial mycelium formation in Streptomyces coelicolor A3(2). J Bacteriol 182: 4606-4616.
6. Chang, H.M., Chen, M.Y., Shieh, Y.T., Bibb, M.J., and Chen, C.W. (1996) The cutRS signal transduction system of Streptomyces lividans represses the biosynthesis of the polyketide antibiotic actinorhodin. Mol Microbiol 21: 1075-1085.
7. Colson, S., Stephan, J., Hertrich, T., Saito, A., van Wezel, G.P., Titgemeyer, F., and Rigali, S. (2007) Conserved cis-acting elements upstream of genes composing the chitinolytic system of streptomycetes are DasR-responsive elements. J Mol Microbiol Biotechnol 12: 60-66.
8. Dancer, B.N., and Mandelstam, J. (1975) Production and possible function of serine protease during sporulation of Bacillus subtilis. J Bacteriol 121: 406-410.
9. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
10. Fink, D., Weissschuh, N., Reuther, J., Wohlleben, W., and Engels, A. (2002) Two transcriptional regulators GlnR and GlnRII are involved in regulation of nitrogen metabolism in Streptomyces coelicolor A3(2). Mol Microbiol 46: 331-347.
11. Gust, B., Challis, G.L., Fowler, K., Kieser, T., and 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 USA 100: 1541-1546.
12. den Hengst, C.D., Tran, N.T., Bibb, M.J., Chandra, G., Leskiw, B.K., and Buttner, M.J. (2010) Genes essential for morphological development and antibiotic production in Streptomyces coelicolor are targets of BldD during vegetative growth. Mol Microbiol 78: 361-379.
13. Herrmann, S., Siegl, T., Luzhetska, M., Petzke, L., Jilg, C., Welle, E., etal. (2012) Site-specific recombination strategies for engineering actinomycete genomes. Appl Environ Microbiol 78: 1804-1812.
14. Hiard, S., Maree, R., Colson, S., Hoskisson, P.A., Titgemeyer, F., van Wezel, G.P., etal. (2007) PREDetector: a new tool to identify regulatory elements in bacterial genomes. Biochem Biophys Res Commun 357: 861-864.
15. Hopwood, D.A., Chater, K.F., and Bibb, M.J. (1995) Genetics of antibiotic production in Streptomyces coelicolor A3(2), a model streptomycete. Biotechnology 28: 65-102.
16. Hutchings, M.I., Hoskisson, P.A., Chandra, G., and Buttner, M.J. (2004) Sensing and responding to diverse extracellular signals? Analysis of the sensor kinases and response regulators of Streptomyces coelicolor A3(2). Microbiology 150: 2795-2806.
17. Ishizuka, H., Horinouchi, S., Kieser, H.M., Hopwood, D.A., and Beppu, T. (1992) A putative two-component regulatory system involved in secondary metabolism in Streptomyces spp. J Bacteriol 174: 7585-7594.
18. Kieser, T., Bibb, M.J., Buttner, M.J., Chater, K.F., and Hopwood, D.A. (2000) Practical Streptomyces Genetics. Norwich: John Innes Foundation.
19. Kudo, N., Kimura, M., Beppu, T., and Horinouchi, S. (1995) Cloning and characterization of a gene involved in aerial mycelium formation in Streptomyces griseus. J Bacteriol 177: 6401-6410.
20. Lee, P.C., Umeyama, T., and Horinouchi, S. (2002) afsS is a target of AfsR, a transcriptional factor with ATPase activity that globally controls secondary metabolism in Streptomyces coelicolor A3(2). Mol Microbiol 43: 1413-1430.
21. Livak, K.J., and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
22. Lu, Y., Wang, W., Shu, D., Zhang, W., Chen, L., Qin, Z., etal. (2007) Characterization of a novel two-component regulatory system involved in the regulation of both actinorhodin and a type I polyketide in Streptomyces coelicolor. Appl Microbiol Biotechnol 77: 625-635.
23. Lu, Y., He, J., Zhu, H., Yu, Z., Wang, R., Chen, Y., etal. (2011) An orphan histidine kinase, OhkA, regulates both secondary metabolism and morphological differentiation in Streptomyces coelicolor. J Bacteriol 193: 3020-3032.
24. McKenzie, N.L., and Nodwell, J.R. (2007) Phosphorylated AbsA2 negatively regulates antibiotic production in Streptomyces coelicolor through interactions with pathway-specific regulatory gene promoters. J Bacteriol 189: 5284-5292.
25. Mascher, T., Helmann, J.D., and Unden, G. (2006) Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 70: 910-938.
26. Molle, V., and Buttner, M.J. (2000) Different alleles of the response regulator gene bldM arrest Streptomyces coelicolor development at distinct stages. Mol Microbiol 36: 1265-1278.
27. Molle, V., Palframan, W.J., Findlay, K.C., and Buttner, M.J. (2000) WhiD and WhiB, homologous proteins required for different stages of sporulation in Streptomyces coelicolor A3(2). J Bacteriol 182: 1286-1295.
28. Nieselt, K., Battke, F., Herbig, A., Bruheim, P., Wentzel, A., Jakobsen, O.M., etal. (2010) The dynamic architecture of the metabolic switch in Streptomyces coelicolor. BMC Genomics 11: 10.
29. Perez-Redondo, R., Rodriguez-Garcia, A., Botas, A., Santamarta, I., Martin, J.F., and Liras, P. (2012) ArgR of Streptomyces coelicolor is a versatile regulator. PLoS ONE 7: e32697.
30. Rigali, S., Titgemeyer, F., Barends, S., Mulder, S., Thomae, A.W., Hopwood, D.A., and van Wezel, G.P. (2008) Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep 9: 670-675.
31. Rodriguez-Garcia, A., Sola-Landa, A., Apel, K., Santos-Beneit, F., and Martin, J.F. (2009) Phosphate control over nitrogen metabolism in Streptomyces coelicolor: direct and indirect negative control of glnR, glnA, glnII and amtB expression by the response regulator PhoP. Nucleic Acids Res 37: 3230-3242.
32. Santos-Beneit, F., Rodriguez-Garcia, A., Sola-Landa, A., and Martin, J.F. (2009) Cross-talk between two global regulators in Streptomyces: PhoP and AfsR interact in the control of afsS, pstS and phoRP transcription. Mol Microbiol 72: 53-68.
33. Santos-Beneit, F., Rodriguez-Garcia, A., and Martin, J.F. (2012) Overlapping binding of PhoP and AfsR to the promoter region of glnR in Streptomyces coelicolor. Microbiol Res 167: 532-535.
34. Shu, D., Chen, L., Wang, W., Yu, Z., Ren, C., Zhang, W., etal. (2009) afsQ1-Q2-sigQ is a pleiotropic but conditionally required signal transduction system for both secondary metabolism and morphological development in Streptomyces coelicolor. Appl Microbiol Biotechnol 81: 1149-1160.
35. Sola-Landa, A., Rodriguez-Garcia, A., Franco-Dominguez, E., and Martin, J.F. (2005) Binding of PhoP to promoters of phosphate-regulated genes in Streptomyces coelicolor: identification of PHO boxes. Mol Microbiol 56: 1373-1385.
36. Sola-Landa, A., Rodriguez-Garcia, A., Apel, A.K., and Martin, 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.
37. Stock, A.M., Robinson, V.L., and Goudreau, P.N. (2000) Two-component signal transduction. Annu Rev Biochem 69: 183-215.
38. Strohl, W.R. (1992) Compilation and analysis of DNA sequences associated with apparent streptomycete promoters. Nucleic Acids Res 20: 961-974.
39. Takano, E., Kinoshita, H., Mersinias, V., Bucca, G., Hotchkiss, G., Nihira, T., etal. (2005) A bacterial hormone (the SCB1) directly controls the expression of a pathway-specific regulatory gene in the cryptic type I polyketide biosynthetic gene cluster of Streptomyces coelicolor. Mol Microbiol 56: 465-479.
40. Tiffert, Y., Supra, P., Wurm, R., Wohlleben, W., Wagner, R., and Reuther, J. (2008) The Streptomyces coelicolor GlnR regulon: identification of new GlnR targets and evidence for a central role of GlnR in nitrogen metabolism in actinomycetes. Mol Microbiol 67: 861-880.
41. Tiffert, Y., Franz-Wachtel, M., Fladerer, C., Nordheim, A., Reuther, J., Wohlleben, W., and Mast, Y. (2011) Proteomic analysis of the GlnR-mediated response to nitrogen limitation in Streptomyces coelicolor M145. Appl Microbiol Biotechnol 89: 1149-1159.
42. Uguru, G.C., Stephens, K.E., Stead, J.A., Towle, J.E., Baumberg, S., and McDowall, K.J. (2005) Transcriptional activation of the pathway-specific regulator of the actinorhodin biosynthetic genes in Streptomyces coelicolor. Mol Microbiol 58: 131-150.
43. Wang, J., and Zhao, G.P. (2009) GlnR positively regulates nasA transcription in Streptomyces coelicolor. Biochem Biophys Res Commun 386: 77-81.
44. Wang, W., Shu, D., Chen, L., Jiang, W., and Lu, Y. (2009) Cross-talk between an orphan response regulator and a noncognate histidine kinase in Streptomyces coelicolor. FEMS Microbiol Lett 294: 150-156.
45. van Wezel, G.P., and McDowall, K.J. (2011) The regulation of the secondary metabolism of Streptomyces: new links and experimental advances. Nat Prod Rep 28: 1311-1333.
46. Xu, G., Wang, J., Wang, L., Tian, X., Yang, H., Fan, K., etal. (2010) 'Pseudo' gamma-butyrolactone receptors respond to antibiotic signals to coordinate antibiotic biosynthesis. J Biol Chem 285: 27440-27448.
47. Yang, H., Wang, L., Xie, Z., Tian, Y., Liu, G., and Tan, H. (2007) The tyrosine degradation gene hppD is transcriptionally activated by HpdA and repressed by HpdR in Streptomyces coelicolor, while hpdA is negatively autoregulated and repressed by HpdR. Mol Microbiol 65: 1064-1077.
48. Yepes, A., Rico, S., Rodriguez-Garcia, A., Santamaria, R.I., and Diaz, M. (2011) Novel two-component systems implied in antibiotic production in Streptomyces coelicolor. PLoS ONE 6: e19980.
49. Yu, Z., Zhu, H., Dang, F., Zhang, W., Qin, Z., Yang, S., etal. (2012) Differential regulation of antibiotic biosynthesis by DraR-K, a novel two-component system in Streptomyces coelicolor. Mol Microbiol 85: 535-556.