Complex transcriptional control of the antibiotic regulator afsS in Streptomyces: PhoP and AfsR are overlapping, competitive activators

Journal of Bacteriology

Volumn 193, Issue 9, 2011, Pages 2242-2251

  Santos Beneit, Fernando ^a   Rodríguez García, Antonio ^a,b   Martín, Juan F ^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

ACTINORHODINE; LUCIFERASE; S ADENOSYLMETHIONINE;

ARTICLE; BIOSYNTHESIS; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STREPTOMYCES;

ANTHRAQUINONES; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; POINT MUTATION; PRODIGIOSIN; PROMOTER REGIONS, GENETIC; STREPTOMYCES; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

STREPTOMYCES; STREPTOMYCES COELICOLOR;

EID: 79955531028     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01462-10     Document Type: Article

References (44)

1. Bentley, S. D., et al. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141-147.
2. Bibb, M. J. 2005. Regulation of secondary metabolism in streptomycetes. Curr. Opin. Microbiol. 8:208-215.
3. Browning, D. F., and S. J. Busby. 2004. The regulation of bacterial transcription initiation. Nat. Rev. Microbiol. 2:57-65.
4. Chiu, J., P. E. March, R. Lee, and D. Tillett. 2004. Site-directed, ligaseindependent mutagenesis (SLIM): a single-tube methodology approaching 100% efficiency in 4 h. Nucleic Acids Res. 32:e174-e179.
5. Doull, J. L., and L. C. Vining. 1991. Culture conditions promoting dispersed growth and biphasic production of actinorhodin in shaken cultures of Streptomyces coelicolor A3(2). FEMS Microbiol. Lett. 65:265-268.
6. Floriano, B., and M. Bibb. 1996. afsR is a pleiotropic but conditionally required regulatory gene for antibiotic production in Streptomyces coelicolor A3(2). Mol. Microbiol. 21:385-396.
7. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
8. Horinouchi, S., O. Hara, and T. Beppu. 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. 155:1238-1248.
9. Horinouchi, S., F. Malpartida, D. A. Hopwood, and T. Beppu. 1989. afsB stimulates transcription of the actinorhodin biosynthetic pathway in Streptomyces coelicolor A3(2) and Streptomyces lividans. Mol. Gen. Genet. 215:355-357.
10. Horinouchi, S. 2003. AfsR as an integrator of signals that are sensed by multiple serine/threonine kinases in Streptomyces coelicolor A3(2). J. Ind. Microbiol. Biotechnol. 30:462-467.
11. Huang, J., et al. 2005. Cross-regulation among disparate antibiotic biosynthetic pathways of Streptomyces coelicolor. Mol. Microbiol. 58:1276-1287.
12. 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.
13. Kim, E. S., H. J. Hong, C. Y. Choi, and S. N. Cohen. 2001. Modulation of actinorhodin biosynthesis in Streptomyces lividans by glucose repression of afsR2 gene transcription. J. Bacteriol. 183:2198-2203. (Erratum, 183: 2969.).
14. Lee, J., Y. Hwang, S. Kim, E. Kim, and C. Choi. 2000. Effect of a global regulatory gene, afsR2, from Streptomyces lividans on avermectin production in Streptomyces avermitilis. J. Biosci. Bioeng. 89:606-608.
15. Lee, P.-C., T. Umeyama, and S. Horinouchi. 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.
16. Lee, Y., K. Kim, J.-W. Suh, S. Rhee, and Y. Lim. 2007. Binding study of AfsK, a Ser/Thr kinase from Streptomyces coelicolor A3(2) and S-adenosyl-Lmethionine. FEMS Microbiol. Lett. 266:236-240.
17. Lian, W., et al. 2008. Genome-wide transcriptome analysis reveals that a pleiotropic antibiotic regulator, AfsS, modulates nutritional stress response in Streptomyces coelicolor A3(2). BMC Genomics 9:56-60.
18. MacNeil, D. J., et al. 1992. Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene 111: 61-68.
19. Maharjan, S., T.-J. Oh, H. C. Lee, and J. K. Sohng. 2009. Identification and functional characterization of an afsR homolog regulatory gene from Streptomyces venezuelae ATCC 15439. J. Microbiol. Biotechnol. 19:121-127.
20. Makitrynskyy, R., et al. 2010. Genetic factors that influence moenomycin production in streptomycetes. J. Ind. Microbiol. Biotechnol. 37:559-566.
21. Martín, J. F., and P. Liras. 2010. Engineering of regulatory cascades and networks controlling antibiotic biosynthesis in Streptomyces. Curr. Opin. Microbiol. 13:263-273.
22. Martín, J. F., et al. 2010. Cross-talk of global nutritional regulators in the control of primary and secondary metabolism in Streptomyces. Microb. Biotechnol. doi:10.1111/j.1751-7915.2010.00235.x.
23. Martínez-Hackert, E., and A. M. Stock. 1997. The DNA-binding domain of OmpR: crystal structures of a winged helix transcription factor. Structure 5:109-124.
24. Matsumoto, A., S. K. Hong, H. Ishizuka, S. Horinouchi, and T. Beppu. 1994. Phosphorylation of the AfsR protein involved in secondary metabolism in Streptomyces species by a eukaryotic-type protein kinase. Gene 146:47-56.
25. Matsumoto, A., H. Ishizuka, T. Beppu, and S. Horinouchi. 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.
26. Parajuli, N., et al. 2005. Identification and characterization of the afsR homologue regulatory gene from Streptomyces peucetius ATCC 27952. Res. Microbiol. 156:707-712.
27. Peeters, E., P. N. Le Minh, M. Foulquie-Moreno, and D. Charlier. 2009. Competitive activation of the Escherichia coli argO gene coding for an arginine exporter by the transcriptional regulators Lrp and ArgP. Mol. Microbiol. 74:1513-1526.
28. Pérez-Redondo, R., I. Santamarta, R. Bovenberg, J. F. Martín, and P. Liras. 2010. The enigmatic lack of glucose utilization in Streptomyces clavuligerus is due to inefficient expression of the glucose permease gene. Microbiology 156:1527-1537.
29. Rajkarnikar, A., H.-J. Kwon, Y.-W. Ryu, and J.-W. Suh. 2006. Catalytic domain of AfsKav modulates both secondary metabolism and morphologic differentiation in Streptomyces avermitilis ATCC 31272. Curr. Microbiol. 53:204-208.
30. Rajkarnikar, A., H.-J. Kwon, Y.-W. Ryu, and J.-W. Suh. 2007. Two threonine residues required for the role of AfsKav in controlling morphogenesis and avermectin production in Streptomyces avermitilis. J. Microbiol. Biotechnol. 17:1563-1567.
31. Rodríguez-García, A., C. Barreiro, F. Santos-Beneit, A. Sola-Landa, and J. F. Martín. 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.
32. Rodríguez-García, A., A. Sola-Landa, K. Apel, F. Santos-Beneit, and J. F. Martín. 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.
33. Santos-Beneit, F., A. Rodríguez-García, E. Franco-Domínguez, and J. F. Martín. 2008. Phosphate-dependent regulation of the low- and high-affinity transport systems in the model actinomycete Streptomyces coelicolor. Microbiology 154:2356-2370.
34. Santos-Beneit, F., A. Rodríguez-García, A. Sola-Landa, and J. F. Martín. 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.
35. Sawai, R., A. Suzuki, Y. Takano, P. C. Lee, and S. Horinouchi. 2004. Phosphorylation of AfsR by multiple serine/threonine kinases in Streptomyces coelicolor A3(2). Gene 334:53-61.
36. Sola-Landa, A., R. S. Moura, and J. F. Martín. 2003. The two-component PhoR-PhoP system controls both primary metabolism and secondary metabolite biosynthesis in Streptomyces lividans. Proc. Natl. Acad. Sci. U. S. A. 100:6133-6138.
37. Sola-Landa, A., A. Rodríguez-García, E. Franco-Domínguez, and J. F. Martín. 2005. Binding of PhoP to promoters of phosphate-regulated genes in Streptomyces coelicolor: identification of PHO boxes. Mol. Microbiol. 56: 1373-1385.
38. Sola-Landa, A., A. Rodríguez-García, A. K. Apel, and J. F. Martín. 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.
39. Tanaka, A., Y. Takano, Y. Ohnishi, and S. Horinouchi. 2007. AfsR recruits RNA polymerase to the afsS promoter: a model for transcriptional activation by SARPs. J. Mol. Biol. 369:322-333.
40. Umeyama, T., P. C. Lee, K. Ueda, and S. Horinouchi. 1999. An AfsK/AfsR system involved in the response of aerial mycelium formation to glucose in Streptomyces griseus. Microbiology 145:2281-2292.
41. Umeyama, T., and S. Horinouchi. 2001. Autophosphorylation of a bacterial serine/threonine kinase, AfsK, is inhibited by KbpA, an AfsK-binding protein. J. Bacteriol. 183:5506-5512.
42. Umeyama, T., P. C. Lee, and S. Horinouchi. 2002. Protein serine/threonine kinases in signal transduction for secondary metabolism and morphogenesis in Streptomyces. Appl. Microbiol. Biotechnol. 59:419-425.
43. Vögtli, M., P. C. Chang, and S. N. Cohen. 1994. afsR2: a previously undetected gene encoding a 63-amino-acid protein that stimulates antibiotic production in Streptomyces lividans. Mol. Microbiol. 14:643-653.
44. Wietzorrek, A., and M. Bibb. 1997. A novel family of proteins that regulates antibiotic production in streptomycetes appears to contain an OmpR-like DNA-binding fold. Mol. Microbiol. 25:1181-1184.