Activation of the SoxR regulon in Streptomyces coelicolor by the extracellular form of the pigmented antibiotic actinorhodin

Journal of Bacteriology

Volumn 193, Issue 1, 2011, Pages 75-81

  Shin, Jung Ho ^a   Singh, Atul K ^a   Cheon, Dong Joo ^a   Roe, Jung Hye ^a  

^a Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ACTINORHODINE; ANTIBIOTIC AGENT; BACTERIAL PROTEIN; GAMMA ACTINORHODINE; SC04266 PROTEIN; SCO1178 PROTEIN; SCO1909 PROTEIN; SCO2478 PROTEIN; SCO7008 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOXR; UNCLASSIFIED DRUG; UNDECYLPRODIGIOSIN; UNSPECIFIC MONOOXYGENASE;

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GROWTH; ESCHERICHIA COLI; GENE ACTIVATION; GENE EXPRESSION; GENE SEQUENCE; GENE TARGETING; MYCELIUM; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN SECRETION; REGULON; SPOROGENESIS; STREPTOMYCES COELICOLOR; WILD TYPE;

ANTHRAQUINONES; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR STRUCTURE; MUTATION; PRODIGIOSIN; PROTEIN BINDING; REGULON; STREPTOMYCES COELICOLOR; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; ESCHERICHIA COLI; STREPTOMYCES COELICOLOR;

EID: 78650114522     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00965-10     Document Type: Article

References (36)

1. Ahn, S. K., K. Tahlan, Z. Yu, and J. Nodwell. 2007. Investigation of transcription repression and small-molecule responsiveness by TetR-like transcription factors using a heterologous Escherichia coli-based assay. J. Bacteriol. 189:6655-6664.
2. Arias, P., M. A. Fernández-Moreno, and F. Malpartida. 1999. Characterization of the pathway-specific positive transcriptional regulator for actinorhodin biosynthesis in Streptomyces coelicolor A3(2) as a DNA-binding protein. J. Bacteriol. 181:6958-6968.
3. Bentley, S. D., K. F. Chater, A. M. Cerdeño-Tárraga, 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.
4. Bierman, M., R. Logan, K. O'Brien, E. T. Seno, R. N. Rao, and B. E. Schoner. 1992. Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116:43-49.
5. Brockmann, H., and E. Hieronimus. 1955. Uber Actinomycetenfarbstoffe, V. Mitteil.: Zur Konstitution des Actinorhodins, III. Mitteil. Chem. Ber. 88:1379-1390.
6. Bystrykh, L. V., M. A. Fernandez-Moreno, J. K. Herrema, F. Malpartida, D. A. Hopwood, and L. Dijkhuizen. 1996. Production of actinorhodin-related blue pigments by Streptomyces coelicolor A3(2). J. Bacteriol. 178:2238-2244.
7. Caballero, J. L., F. Malpartida, and D. A. Hopwood. 1991. Transcriptional organization and regulation of an antibiotic export complex in the producing Streptomyces culture. Mol. Gen. Genet. 228:372-380.
8. Chater, K. F., and D. A. Hopwood. 1993. Streptomyces, p. 83-89. In J. P. Sonenshein (ed.), Bacillus subtilis and other gram-positive bacteria. Biochemistry, physiology and molecular genetics. ASM Press, Washington, DC.
9. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
10. Dietrich, L. E. P., A. Price-Whelan, A. Petersen, M. Whiteley, and D. K. Newman. 2006. The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol. Microbiol. 61:1308-1321.
11. Dietrich, L. E. P., T. K. Teal, A. Price-Whelan, and D. K. Newman. 2008. Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science 321:1203-1206.
12. Floriano, B., and M. J. Bibb. 1996. afsR is a pleiotropic but conditionally required regulatory gene for antibiotic production in Streptomyces coelicolor A3(2). Mol. Microbiol. 21:385-396.
13. Gramajo, H. C., E. Takano, and M. J. Bibb. 1993. Stationary-phase production of the antibiotic actinorhodin in Streptomyces coelicolor A3(2) is transcriptionally regulated. Mol. Microbiol. 7:837-845.
14. Greenberg, J. T., P. Monach, J. H. Chou, P. D. Josephy, and B. Demple. 1990. Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 87:6181-6185.
15. 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. U. S. A. 100:1541-1546.
16. Hidalgo, E., and B. Demple. 1994. An iron-sulfur center essential for transcriptional activation by the redox-sensing SoxR protein. EMBO J. 13:138-146.
17. Kieser, T., M. J. Bibb, M. J. Buttner, K. F. Chater, and D. A. Hopwood. 2000. Practical Streptomyces genetics. The John Innes Foundation, Norwich, United Kingdom.
18. Kim, I. K., C. J. Lee, M. K. Kim, J. M. Kim, J. H. Kim, H. S. Yim, S. S. Cha, and S. O. Kang. 2006. Crystal structure of the DNA-binding domain of BldD, a central regulator of aerial mycelium formation in Streptomyces coelicolor A3(2). Mol. Microbiol. 60:1179-1193.
19. Kobayashi, K., and S. Tagawa. 2004. Activation of SoxR-dependent transcription in Pseudomonas aeruginosa. J. Biochem. 136:607-615.
20. Mazodier, P., R. Petter, and C. Thompson. 1989. Intergeneric conjugation between Escherichia coli and Streptomyces species. J. Bacteriol. 171:3583-3585.
21. Okamoto, S., T. Taguchi, K. Ochi, and K. Ichinose. 2009. Biosynthesis of actinorhodin and related antibiotics: discovery of alternative routes for quinone formation encoded in the act gene cluster. Chem. Biol. 16:226-236.
22. Palma, M., J. Zurita, J. A. Ferreras, S. Worgall, D. H. Larone, L. Shi, F. Campagne, and L. E. N. Quadri. 2005. Pseudomonas aeruginosa SoxR does not conform to the archetypal paradigm for SoxR-dependent regulation of the bacterial oxidative stress adaptive response. Infect. Immun. 73:2958-2966.
23. Park, W., S. Peña-Llopis, Y. H. Lee, and B. Demple. 2006. Regulation of superoxide stress in Pseudomonas putida KT2440 is different from the SoxR paradigm in Escherichia coli. Biochem. Biophys. Res. Commun. 341:51-56.
24. Park, S. S., Y. H. Yang, E. Song, E. J. Kim, W. S. Kim, J. K. Sohng, H. C. Lee, K. K. Liou, and B. G. Kim. 2009. Mass spectrometric screening of transcriptional regulators involved in antibiotic biosynthesis in Streptomyces coelicolor A3(2). J. Ind. Microbiol. Biotechnol. 36:1073-1083.
25. Pomposiello, P. J., and B. Demple. 2001. Redox-operated genetic switches: the SoxR and OxyR transcription factors. Trends Biotechnol. 19:109-114.
26. Rigali, S., F. Titgemeyer, S. Barends, S. Mulder, A. W. Thomae, D. A. Hopwood, and G. P. van Wezel. 2008. Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO reports. 9:670-675.
27. Strauch, E., E. Takano, H. A. Baylis, and M. J. Bibb. 1991. The stringent response in Streptomyces coelicolor A3(2). Mol. Microbiol. 5:289-298.
28. Taguchi, T., Y. Ebizuka, D. A. Hopwood, and K. Ichinose. 2001. A new mode of stereochemical control revealed by analysis of the biosynthesis of dihydrogranaticin in Streptomyces violaceoruber Tu22. J. Am. Chem. Soc. 123:11376-11380.
29. Tahlan, K., S. K. Ahn, A. Sing, T. D. Bodnaruk, A. R. Willems, A. R. Davidson, and J. R. Nodwell. 2007. Initiation of actinorhodin export in Streptomyces coelicolor. Mol. Microbiol. 63:951-961.
30. Tahlan, K., Z. Yu, Y. Xu, A. R. Davidson, and J. R. Nodwell. 2008. Ligand recognition by ActR, a TetR-like regulator of actinorhodin export. J. Mol. Biol. 383:753-761.
31. Takano, E., H. C. Gramajo, E. Strauch, N. Andres, J. White, and M. J. Bibb. 1992. Transcriptional regulation of the redD transcriptional activator gene accounts for growth-phase dependent production of the antibiotic undecyl-prodigiosin in Streptomyces coelicolor A3(2). Mol. Microbiol. 6:2797-2804.
32. Tsaneva, I. R., and B. Weiss. 1990. SoxR, a locus governing a superoxide response regulon in Escherichia coli K-12. J. Bacteriol. 172:4197-4205.
33. Tsao, S. W., B. A. Rudd, X. G. He, C. J. Chang, and H. G. Floss. 1985. Identification of a red pigment from Streptomyces coelicolor A3(2) as a mixture of prodigiosin derivatives. J. Antibiot. 38:128-131.
34. Turner, J. M., and A. J. Messenger. 1986. Occurrence, biochemistry and physiology of phenazine pigment production. Adv. Microb. Physiol. 27:211-275.
35. Uguru, G. C., K. E. Stephens, J. A. Stead, J. E. Towle, S. Baumberg, and K. J. McDowall. 2005. Transcriptional activation of the pathway-specific regulator of the actinorhodin biosynthetic genes in Streptomyces coelicolor. Mol. Microbiol. 58:131-150.
36. Watanabe, S., A. Kita, K. Kobayashi, and K. Miki. 2008. Crystral structure of the [2Fe-2S] oxidative-stress sensor SoxR bound to DNA. Proc. Natl. Acad. Sci. U. S. A. 105:4121-4126.