A new GntR family transcriptional regulator in Streptomyces coelicolor is required for morphogenesis and antibiotic production and controls transcription of an ABC transporter in response to carbon source

Journal of Bacteriology

Volumn 188, Issue 21, 2006, Pages 7477-7487

  Hillerich, Brandan ^a   Westpheling, Janet ^a  

^a University of Georgia ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ALPHA GLUCOSIDASE; ANTIBIOTIC AGENT; BACTERIAL PROTEIN; CARBOHYDRATE; GLUCOSE; GLYCEROL; LACTOSE; MELIBIOSE; PROTEIN GNTR; TREHALOSE; UNCLASSIFIED DRUG;

AGL3E GENE; AGL3F GENE; AGL3G GENE; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; CARBOHYDRATE TRANSPORT; CARBON SOURCE; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; GENE CONTROL; GENE DELETION; GENE INSERTION; GENE ISOLATION; GENE MUTATION; GENE REPRESSION; MORPHOGENESIS; MUTANT; NOMENCLATURE; NONHUMAN; NUTRITION; OPEN READING FRAME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; SIGNAL TRANSDUCTION; STREPTOMYCES COELICOLOR; TRANSCRIPTION REGULATION; TRANSPOSON;

ANTI-BACTERIAL AGENTS; ARTIFICIAL GENE FUSION; ATP-BINDING CASSETTE TRANSPORTERS; CARBOHYDRATE METABOLISM; DNA, BACTERIAL; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ESCHERICHIA COLI PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REGULATOR; GENES, REPORTER; GLUCOSIDES; MORPHOGENESIS; PROTEIN BINDING; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, BACTERIAL; RNA, MESSENGER; STREPTOMYCES COELICOLOR; SYMPORTERS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

STREPTOMYCES; STREPTOMYCES COELICOLOR;

EID: 33750435588     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00898-06     Document Type: Article

References (47)

1. Angell, S., C. G. Lewis, M. J. Buttner, and M. J. Bihb. 1994. Glucose repression in Streptomyces coelicolor A3(2): a likely regulatory role for glucose kinase. Mol. Gen. Genet. 244:135-143.
2. Bentley, S. D., K. F. Chater, A. M. Cerdeno-Tarraga, G. L. Challis, N. R. Thomson, K. D. James, D. E. Harris, M. A. Quail, H. Kieser, D. Harper, A. Bateman, S. Brown, G. Chandra, C. W. Chen, M. Collins, A. Cronin, A. Fraser, A. Goble, J. Hidalgo, T. Hornsby, S. Howarth, C. H. Huang, T. Kieser, L. Larke, L. Murphy, K. Oliver, S. O'Neil, E. Rabbinowitsch, M. A. Rajandream, K. Rutherford, S. Rutter, K. Seeger, D. Saunders, S. Sharp, R. Squares, S. Squares, K. Taylor, T. Warren, A. Wietzorrek, J. Woodward, B. G. Barrell, J. Parkhill, and D. A. Hopwood. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141-147.
3. Bertram, R., M. Schlicht, K. Mahr, H. Nothaft, M. H. Saier, Jr., and F. Titgemeyer. 2004. In silico and transcriptional analysis of carbohydrate uptake systems of Streptomyces coelicolor A3(2). J. Bacteriol. 186:1362-1373.
4. 54-RNA polymerase holoenzyme. J. Bacteriol. 186:4535-4542.
5. Champness, W. 1988. New loci required for Streptomyces coelicolor morphological and physiological differentiation. J. Bacteriol. 170:1168-1174.
6. Champness, W. C., and K. F. Chater. 1994. Regulation and integration of antibiotic production and morphological differentiation in Streptomyces spp., p. 61-93. In P. J. Piggot, C. P. Moran, and P. Youngman (ed.). Regulation of bacterial development. American Society for Microbiology. Washington, D.C.
7. Chater, K. 1975. Construction and phenotypes of double sporulation deficient mutants in Streptomyces coelicolor A3(2). J. Gen. Microbiol. 87:312-325.
8. Chater, K. F. 1972. A morphological and genetic mapping study of white colony mutants of Streptomyces coelicolor. J. Gen. Microbiol. 72:9-28.
9. Chater, K. F. 2001. Regulation of sporulation in Streptomyces coelicolor A3(2): a checkpoint multiplex? Curr. Opin. Microbiol. 4:667-673.
10. Deronaux, A., D. Dehareng, E. Lecocq, S. Halici, H. Nothaft, F. Giannotta, G. Montzonrelis, J. Dusart, H. Devreese, F. Titgemeyer, J. Van Beeumen, and S. Rigali. 2004. Crp of Streptomyces coelicolor is the third transcription factor of the large CRP-FNR superfamily able to bind cAMP. Biochem. Biophys. Res. Commun. 325:983-990.
11. Deronaux, A., S. Halici, H. Nothaft, T. Nentelings, G. Montzourelis, J. Dusart, F. Titgemeyer, and S. Rigali. 2004. Deletion of a cyclic AMP receptor protein homologue diminishes germination and affects morphological development of Streptomyces coelicolor. J. Bacteriol. 186:1893-1897.
12. DiRusso, C., A. Metzger, and T. Heimert. 1993. Regulation of transcription of genes required for fatty acid transport and unsaturated fatty acid biosynthesis in Escherichia coli by FadR. Mol. Microbiol. 7:311-322.
13. Flardh, K., K. C. Findlay, and K. F. Chater. 1999. Association of early sporulation genes with suggested developmental decision points in Streptomyces coelicolor A3(2). Microbiology 145:2229-2243.
14. Gust, B., G. L. Challis, K. Fowler, T. Kieser, and K. F. Chater. 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.
15. Guzman, S., A. Carmona, L. Escalante, I. Imriskova, R. Lopez, R. Rodriguez-Sanoja, B. Ruiz, L. Servin-Gonzalez, S. Sanchez, and E. Langley, 2005. Pleiotropic effect of the SCO2127 gene on the glucose uptake, glucose kinase activity and carbon catabolite repression in Streptomyces peucetiuss var. caesius. Microbiology 151:1717-1713.
16. Haydon, D. J., and J. R. Guest. 1991. A new family of bacterial regulatory proteins. FEMS Microbiol. Lett. 63:291-295.
17. Hopwood, D. A., M. J. Bibb, K. F. Chater, T. Kieser, C. J. Bruton, H. M. Kieser, D. J. Lydiate, C. P. Smith, J. M. Ward, and H. Schrempf. 1985. Genetic manipulation of Streptomyces: a laboratory manual. 1st ed. The John Innes Foundation, Norwich, United Kingdom.
18. Hurtubise, Y., F. Sareck, D. Kluepfel, and R. Morosoli. 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. Microbiol. 17:367-377.
19. Ingram, C., M. Brawner, P. Youngman, and J. Westpheling. 1989. xylE functions as an efficient reporter gene in Streptomyces spp.: use for the study of galpl, a catabolite-controlled promoter. J. Bacteriol. 171:6617-6624.
20. Ingram, C., I. Delic, and J. Westpheling. 1995. ccrAl: a mutation in Streptomyces coelicolor that affects the control of catabolite repression. J. Bacteriol. 177:3579-3586.
21. Kamionka, A., S. Parche, H. Nothaft, J. Siepelmeyer, K. Jahreis, and F. Titgemeyer. 2002. The phosphotransferase system of Streptomyces coelicolor. Eur. J.Biochem. 269:2143-2150.
22. Kelemen, G. H., P. Brian, K. Flärdh, L. Chamberlin, K. Chater, and M. Buttner. 1996. Developmental regulation of the transcription of whiE, a locus specifying the polyketide spore pigment in Streptomyces coelicolor A3(2). J. Bacteriol. 180:2515-2521.
23. Kieser, T., M. J. Bibb, M. J. Buttner, K. F. Cbater, and D. A. Hopwood. 2000. Practical Streptomyces genetics. The John Innes Foundation. Norwich, United Kingdom.
24. Kodani, S., M. E. Hudson, M. C. Durrant, M. J. Buttner, J. R. Nodwell, and J. M. Willey. 2004. The SapB morphogen is a lantibiotic-like peptide derived from the product of the developmental gene ramS in Streptomyces caelicolor. Proc. Natl. Acad. Sci. USA 101:11448-11453.
25. Kormanec, J. 2001. Analyzing the developmental expression of sigma factors with S1-nuclease mapping. Methods Mol. Biol. 160:481-494.
26. Kwakman, J. H., and P. W. Postma. 1994. Glucose kinase has a regulatory role in carbon catabolite repression in Streptomyces coelicolor. J. Bacteriol. 176:2694-2698.
27. Merrick, M. J. 1976. A morphological and genetic mapping study of bald colony mutants of Streptomyces coelicolor. J. Gen. Microbiol. 96:299-315.
28. Nodwell, J. R., K. McGovern, and R. Losick. 1996. An oligopeptide permease responsible for the import of an extracellular signal governing aerial mycelium formation in Streptomyces coelicolor. Mol. Microbiol. 22:881-893.
29. Parche, S., R. Schmid, and F. Titgemeyer. 1999. The phosphotransferase system (PTS) of Streptomyces coelicolor: identification and biochemical analysis of a histidine phosphocarrier protein HPr encoded by the gene ptsH. Eur. J. Biochem. 265:308-317.
30. Pope, M. K., B. D. Green, and J. Westpheling. 1996. The bld mutants of Streptomyces coelicolor are defective in the regulation of carbon utilization, morphogenesis and cell-cell signalling. Mol. Microbiol. 19:747-756.
31. Rigali, S., A. Derouanx, K. Giannotta, and J. Dusart. 2002. Subdivision of the helix-turn-helix GntR family of bacterial regulators in the FadR, HutC, MocR, and YtrA subfamilies. J. Biol. Chem. 277:12507-12515.
32. Ryding, N. J., M. J. Bibb, V. Molle, K. C. Findlay, K. F. Chater, and M. J. Buttner. 1999. New sporulation loci in Streptomyces coelicolor A3(2). J. Bacteriol. 181:5419-5425.
33. Ryding, N. J., G. H. Kelemen, C. A. Whatling, K. Flardh, M. J. Buttner, and K. F. Chater. 1998. A developmentally regulated gene encoding a repressor-like protein is essential for sporulation in Streptomyces coelicolor A3(2). Mol. Microbiol. 29:343-357.
34. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual. 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
35. Saurin, W., W. Koster, and E. Dassa. 1985. Bacterial binding protein-dependent permeases: characterization of distinctive signatures for functionally related integral cytoplasmic membrane proteins. Mol. Microbiol. 12:993-1004.
36. Schlosser, A. 2000. MsiK-dependent trehalose uptake in Streptomyces reticuli. FEMS Microbiol. Lett. 184:187-192.
37. Schlosser, A., J. Jantos, K. Hackmann, and H. Schrempf. 1999. Characterization of the binding protein-dependent cellobiose and cellotriose transport system of the cellulose degrader Streptomyces reticuli. Appl. Environ. Microbiol. 65:2636-2643.
38. Schlosser, A., A. Weber, and H. Schrempl. 2001. Synthesis of the Streptomyces lividans maltodextrin ABC transporter depends on the presence of the regulator MalR. FEMS Microbiol. Lett. 196:77-83.
39. Schmitt, L., and R. Tampe. 2002. Structure and mechanism of ABC transporters. Curr. Opin. Struct. Biol. 12:754-760.
40. Seo, J. W., Y. Ohnishi, A. Hirata, and S. Horinouchi. 2002. ATP-binding cassette transport system involved in regulation of morphological differentiation in response to glucose in Streptomyces griseus. J. Bacteriol. 184:91-103.
41. Sprusausky, O., L. Zhou, S. Jordan, J. White, and J. Westpheling. 2003. Identification of three new genes involved in morphogenesis and antibiotic production in Streptomyces coelicolor. J. Bacteriol. 185:6147-6157.
42. Sutcliffe, I., L. Tao, J. Ferretti, and R. Russell. 1993. MsmE, a lipoprotein involved in sugar transport in Streptococcus mutans. J. Bacteriol. 175:1853-1855.
43. van Veen, H. W., A. Margolles, M. Muller, C. F. Higgins, and W. N. Konings. 2000. The homodimeric ATP-binding cassette transporter LmrA mediates multidrug transport by an alternating two-site (two-cylinder engine) mechanism. EMBO J. 19:2503-2514.
44. van Wezel, G. P., K. Mahr, M. Konig, B. A. Traag, E. F. Pimentel-Schmitt, A. Willimek, and F. Titgemeyer. 2005. GlcP constitutes the major glucose uptake system of Streptomyces coelicolor A3(2). Mol. Microbiol. 55:624-636.
45. van Wezel, G. P., J. White, M. J. Bibb, and P. W. Postma. 1997. The malEFG gene cluster of Streptomyces coelicolor A3(2): characterization, disruption and transcriptional analysis. Mol. Gen. Genet. 254:604-608.
46. Willey, J. W., R. Santamaria, J. Gnijarro, M. Geislich, and R. Losick. 1991. Extracellular complementation of a developmental mutation implicates a small sporulation protein in aerial mycelium formation by Streptomyces coelicolor. Cell 65:641-650.
47. Yu, T. W., and D. A. Hopwood. 1995. Ectopic expression of the Streptomyces coelicolor whiE genes for polykelide spore pigment synthesis and their interaction with the act genes for actinorhodin biosynthesis. Microbiology 141:2779-2791.