Cross-talk of global nutritional regulators in the control of primary and secondary metabolism in Streptomyces

Microbial Biotechnology

Volumn 4, Issue 2, 2011, Pages 165-174

  Martín, Juan F ^a,b   Sola Landa, Alberto ^a   Santos Beneit, Fernando ^a   Fernández Martínez, Lorena T ^a   Prieto, Carlos ^a   Rodríguez García, Antonio ^a,b  

^a Institute of Biotechnology INBIOTEC Parque Científico de León   (Spain)

^b UNIVERSITY OF LEÓN   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; N ACETYLGLUCOSAMINE; NITROGEN; NITROGEN REGULATORY PROTEIN; PERMEASE; PHOP PROTEIN; PHOSPHATE; PHOSPHOTRANSFERASE;

BACTERIAL METABOLISM; BINDING SITE; CARBON METABOLISM; GENE CONTROL; GENE EXPRESSION; HOMEOSTASIS; NONHUMAN; NUTRITION; PROMOTER REGION; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; REVIEW; STREPTOMYCES; STREPTOMYCES COELICOLOR;

BACTERIAL PROTEINS; CARBON; GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; GENES, REGULATOR; NITROGEN; PHOSPHATES; STREPTOMYCES;

STREPTOMYCES; STREPTOMYCES COELICOLOR;

EID: 79951818857     PISSN: 17517907     EISSN: 17517915     Source Type: Journal    
DOI: 10.1111/j.1751-7915.2010.00235.x     Document Type: Review

References (70)

1. Apel, A.K., Sola-Landa, A., Rodríguez-García, A., and 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.
2. Borodina, I., Siebring, J., Zhang, J., Smith, C.P., van Keulen, G., Dijkhuizen, L., and Nielsen, J. (2008) Antibiotic overproduction in Streptomyces coelicolor A3(2) mediated by phosphofructokinase deletion. J Biol Chem 283: 25186-25199.
3. Brzoska, P., and 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.
4. Champness, W., Riggle, P., Adamidis, T., and Vandervere, P. (1992) Identification of Streptomyces coelicolor genes involved in regulation of antibiotic synthesis. Gene 115: 55-60.
5. Chang, S.A., Bralley, P., and Jones, G.H. (2005) The absB gene encodes a double-strand specific endoribonuclease that cleaves the readthrough transcript of the rspO-pnp operon in Streptomyces coelicolor. J Biol Chem 280: 33213-33219.
6. Choi, S.-K., and Saier, M.H. (2005) Regulation of pho regulon gene expression by the carbon control protein A, CcpA, in Bacillus subtilis. J Mol Microbiol Biotechnol 10: 40-50.
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. Commichau, F.M., Forchhammer, K., and Stülke, J. (2006) Regulatory links between carbon and nitrogen metabolism. Curr Opin Microbiol 9: 167-172.
9. Díaz, M., Esteban, A., Fernández-Ábalos, J.M., and 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.
10. Esteban, A., Díaz, M., Yepes, A., and 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: 201-213.
11. 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.
12. Fisher, S.H., and Wray, L.V., Jr. (1989) Regulation of glutamine synthetase in Streptomyces coelicolor. J Bacteriol 171: 2378-2383.
13. Floriano, B., and Bibb, M. (1996) afsR is a pleiotropic but conditionally required regulatory gene for antibiotic production in Streptomyces coelicolor A3(2). Mol Microbiol 21: 385-396.
14. Ghorbel, S., Kormanec, J., Artus, A., and Virolle, M.-J. (2006a) Transcriptional studies and regulatory interactions between the phoR-phoP operon and the phoU, mtpA, and ppk genes of Streptomyces lividans TK24. J Bacteriol 188: 677-686.
15. Ghorbel, S., Smirnov, A., Chouayekh, H., Sperandio, B., Esnault, C., Kormanec, J., and Virolle, M.-J. (2006b) Regulation of ppk expression and in vivo function of Ppk in Streptomyces lividans TK24. J Bacteriol 188: 6269-6276.
16. Hesketh, A., Fink, D., Gust, B., Rexer, H.-U., Scheel, B., Chater, K., etal. (2002) The GlnD and GlnK homologues of Streptomyces coelicolor A3(2) are functionally dissimilar to their nitrogen regulatory system counterparts from enteric bacteria. Mol Microbiol 46: 319-330.
17. Hobbs, G., Frazer, C.M., Gardner, D.C.J., Flett, F., and Oliver, S.G. (1990) Pigmented antibiotic production by Streptomyces coelicolor A3(2): kinetics and the influence of nutrients. J Gen Microbiol 136: 2291-2296.
18. Hoi, L.T., Voigt, B., Jürgen, B., Ehrenreich, A., Gottschalk, G., Evers, S., etal. (2006) The phosphate-starvation response of Bacillus licheniformis. Proteomics 6: 3582-3601.
19. Horinouchi, S., Hara, O., and Beppu, T. (1983) Cloning of a pleiotropic gene that positively controls biosynthesis of A-factor, actinorhodin, and prodigiosin in Streptomyces coelicolor A3(2) and Streptomyces lividans. J Bacteriol 162: 406-412.
20. Iwasaki, Y., Nakano, H., and Yamane, T. (1994) Phospholipase D from Streptomyces antibioticus: cloning, sequencing, expression, and relationship to other phospholipases. Appl Microbiol Biotechnol 42: 290-299.
21. Kasahara, M., Makino, K., Amemura, M., Nakata, A., and Shinagawa, H. (1991) Dual regulation of the ugp operon by phosphate and carbon starvation at two interspaced promoters. J Bacteriol 173: 549-558.
22. Kezuka, T., Ohishi, M., Itoh, Y., Watanabe, J., Mitsutomi, M., Watanabe, T., and Nonaka, T. (2006) Structural studies of a two-domain chitinase from Streptomyces griseus HUT6037. J Mol Biol 358: 472-484.
23. Krol, E., and Becker, A. (2004) Global transcriptional analysis of the phosphate starvation response in Sinorhizobium meliloti strains 1021 and 2011. Mol Genet Genomics 272: 1-17.
24. Larson, T.J., Ehrmann, M., and Boos, W. (1983) Periplasmic glycerophosphodiester phosphodiesterase of Escherichia coli, a new enzyme of the glp regulon. J Biol Chem 258: 5428-5432.
25. 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.
26. Lu, Y.H., Wang, W.H., Shu, D., Zhang, W.W., Chen, L., Qin, Z.J., 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.
27. Makarewicz, O., Dubrac, S., Msadek, T., and 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.
28. Martín, J.F. (2004) Phosphate control of the biosynthesis of antibiotics and other secondary metabolites is mediated by the PhoR-PhoP system: an unfinished story. J Bacteriol 186: 5197-5201.
29. Martín, J.F., and Demain, A.L. (1980) Control of antibiotic synthesis. Microbiol Rev 44: 230-251.
30. Martín, J.F., and Liras, P. (2010) Engineering of regulatory cascades and networks controlling antibiotic biosynthesis in Streptomyces. Curr Opin Microbiol 13: 263-273.
31. Masayama, A., Takahashi, T., Tsukada, K., Nishikawa, S., Takahashi, R., Adachi, M., etal. (2008) Streptomyces phospholipase D mutants with altered substrate specificity capable of phophatidylinositol synthesis. Chembiochem 9: 974-981.
32. Matsumoto, A., Ishizuka, H., Beppu, T., and Horinouchi, S. (1995) Involvement of a small ORF downstream of the afsR gene in the regulation of secondary metabolism in Streptomyces coelicolor A3(2). Actinomycetologica 9: 37-43.
33. Mendes, M.V., Tunca, S., Antón, N., Recio, E., Sola-Landa, A., Aparicio, J.F., and 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.
34. Merrick, M.J., and Edwards, R.A. (1995) Nitrogen control in bacteria. Microbiol Rev 59: 604-622.
35. Moura, R.S., Martín, J.F., Martín, A., and Liras, P. (2001) Substrate analysis and molecular cloning of the extracellular alkaline phosphatase of Streptomyces griseus. Microbiology 147: 1525-1533.
36. 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: 10-19.
37. Nilsson, R.P., Beijer, L., and Rutberg, B. (1994) The glpT and glpQ genes of the glycerol regulon in Bacillus subtilis. Microbiology 140: 724-730.
38. Nothaft, H., Rigali, S., Boomsma, B., Swiatek, M., McDowall, K.J., van Wezel, G.P., and Titgemeyer, F. (2010) The permease gene nagE2 is the key to N-acetylglucosamine sensing and utilization in Streptomyces coelicolor and is subject to multi-level control. Mol Microbiol 75: 1133-1144.
39. Oh, W.-S., Im, Y.-S., Yeon, K.-Y., Yoon, Y.-J., and Kim, J.-W. (2007) Phosphate and carbon source regulation of alkaline phosphatase and phospholipase in Vibrio vulnificus. J Microbiol 45: 311-317.
40. Overduin, P., Boos, W., and Tommassen, J. (1988) Nucleotide sequence of the ugp genes of Escherichia coli K-12: homology to the maltose system. Mol Microbiol 2: 767-775.
41. Parker, J.L., Jones, A.M.E., Serazetdinova, L., Saalbach, G., Bibb, M.J., and Naldrett, M.J. (2010) Analysis of the phosphoproteome of the multicellular bacterium Streptomyces coelicolor A3(2) by protein/peptide fractionation, phosphopeptide enrichment and high-accuracy mass spectrometry. Proteomics 10: 2486-2497.
42. Price, B., Adamidis, T., Kong, R., and Champness, W. (1999) A Streptomyces coelicolor antibiotic regulatory gene, absB, encodes an RNase III homolog. J Bacteriol 181: 6142-6151.
43. Puri-Taneja, A., Paul, S., Chen, Y., and Hulett, F.M. (2006) CcpA causes repression of the phoPR promoter through a novel transcription start site, PA6. J Bacteriol 188: 1266-1278.
44. Quiquampoix, H., and Mousain, D. (2005) Enzymatic hydrolysis of organic phosphorus. In Organic Phosphorus in the Environment. Turner, B.L., Frossard, E., and Baldwin, D.S. (eds). Cambridge, MA, USA: CABI Publishing, pp. 89-112.
45. Rao, N.N., and Torriani, A. (1990) Molecular aspects of phosphate transport in Escherichia coli. Mol Microbiol 4: 1083-1090.
46. Reuther, J., and Wohlleben, W. (2007) Nitrogen metabolism in Streptomyces coelicolor: transcriptional and post-translational regulation. J Mol Microbiol Biotechnol 12: 139-146.
47. 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.
48. Rodríguez-García, A., Barreiro, C., Santos-Beneit, F., Sola-Landa, A., and 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.
49. Rodríguez-García, A., Sola-Landa, A., Apel, K., Santos-Beneit, F., and Martín, J.F. (2009) Phosphate control over nitrogen metabolism in Streptomyces coelicolor: direct and indirect negative control of glnR, glnA, glnII and amtBexpression by the response regulator PhoP. Nucleic Acids Res 37: 3230-3242.
50. Saito, A., and Schrempf, H. (2004) Mutational analysis of the binding affinity and transport activity for N-acetylglucosamine of the novel ABC transporter Ngc in the chitin-degrader Streptomyces olivaceoviridis. Mol Genet Genomics 271: 545-553.
51. Santos-Beneit, F., Rodríguez-García, A., Franco-Domínguez, E., and 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.
52. Santos-Beneit, F., Rodríguez-García, A., Sola-Landa, A., and Martín, J.F. (2009a) 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.
53. Santos-Beneit, F., Rodríguez-García, A., Apel, A.K., and Martín, J.F. (2009b) Phosphate and carbon source regulation of two PhoP-dependent glycerophosphodiester phosphodiesterase genes of Streptomyces coelicolor. Microbiology 155: 1800-1811.
54. Scheu, A.K., Martínez, E., Soliveri, J., and Malpartida, F. (1997) abaB, a putative regulator for secondary metabolism in Streptomyces. FEMS Microbiol Lett 147: 29-36.
55. Schrempf, H. (2001) Recognition and degradation of chitin by streptomycetes. Antonine Van Leewenhoek 79: 285-289.
56. 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.
57. Sola-Landa, A., Moura, R.S., and 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 USA 100: 6133-6138.
58. Sola-Landa, A., Rodríguez-García, A., Franco-Domínguez, E., and 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.
59. Sola-Landa, A., Rodríguez-García, A., Apel, A.K., and 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.
60. Sonenshein, A.L. (2007) Control of key metabolic intersections in Bacillus subtilis. Nat Rev Microbiol 5: 917-927.
61. 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.
62. Titball, R.W. (1993) Bacterial phospholipases C. Microbiol Rev 57: 347-366.
63. Torriani, A. (1990) From cell membrane to nucleotides: the phosphate regulon in Escherichia coli. Bioessays 12: 371-376.
64. Uesugi, Y., and Hatanaka, T. (2009) Phospholipase D mechanism using Streptomyces PLD. Biochim Biophys Acta 1791: 962-969.
65. VanBogelen, R.A., Olson, E.R., Wanner, B.L., and Neidhardt, F.C. (1996) Global analysis of proteins synthesized during phosphorus restriction in Escherichia coli. J Bacteriol 178: 4344-4366.
66. Vögtli, M., Chang, P.C., and Cohen, S.N. (1994) afsR2: a previously undetected gene encoding a 63-amino acid protein that stimulates antibiotic production in Streptomyces lividans. Mol Microbiol 14: 643-653.
67. Wang, F., Xiao, X., Saito, A., and Schrempf, H. (2002) Streptomyces olivaceoviridis possesses a phosphotransferase system that mediates specific, phosphoenolpyruvate-dependent uptake of N-acetylglucosamine. Mol Genet Genomics 268: 344-351.
68. Wanner, B.L. (1996) Phosphorus assimilation and control of the phosphate regulon. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt, F.C., Curtiss, R., III, Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., etal. (eds). Washington, DC, USA: American Society for Microbiology, pp. 1357-1381.
69. Wray, L.V., and Fisher, S.H. (1993) The Streptomyces coelicolor glnR gene encodes a protein similar to other bacterial response regulators. Gene 130: 145-150.
70. Wray, L.V., Jr, Atkinson, M.R., and Fisher, S.H. (1991) Identification and cloning of the glnR locus, which is required for transcription of the glnA gene in Streptomyces coelicolor A3(2). J Bacteriol 173: 7351-7360.