EshA accentuates ppGpp accumulation and is conditionally required for antibiotic production in Streptomyces coelicolor A3(2)

Journal of Bacteriology

Volumn 188, Issue 13, 2006, Pages 4952-4961

  Saito, Natsumi ^a   Xu, Jun ^a   Hosaka, Takeshi ^a   Okamoto, Susumu ^a   Aoki, Hiroyuki ^a,b   Bibb, Mervyn J ^c   Ochi, Kozo ^a  

^a NATIONAL FOOD RESEARCH INSTITUTE   (Japan)

^b UNIVERSITY OF TORONTO   (Canada)

^c JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTINORHODINE; ANTIBIOTIC AGENT; BACTERIAL PROTEIN; CYCLIC NUCLEOTIDE; GUANOSINE 3' DIPHOSPHATE 5' DIPHOSPHATE; PROTEIN ESHA; RNA POLYMERASE BETA SUBUNIT; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BINDING SITE; CONTROLLED STUDY; ESHA GENE; ESHB GENE; GENE DISRUPTION; GENE EXPRESSION; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; RELA GENE; RPOB GENE; SIGNAL TRANSDUCTION; STREPTOMYCES COELICOLOR; SYNTHESIS; WILD TYPE;

ANTHRAQUINONES; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CYCLIC AMP; GUANOSINE TETRAPHOSPHATE; MOLECULAR WEIGHT; PROTEIN BINDING; SPORES, BACTERIAL; STREPTOMYCES COELICOLOR;

STREPTOMYCES COELICOLOR; STREPTOMYCINEAE;

EID: 33745444059     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00343-06     Document Type: Article

References (62)

1. Arias, P., M. A. Fernandez-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.
2. Artsimovitch, I, V. Patlan, S. Sekine, M. N. Vassylyeva, T. Hosaka, K. Ochi, S. Yokoyama, and D. G. Vassylyev. 2004. Structural basis for transcription regulation by alarmone ppGpp. Cell 117:299-310.
3. Bibb, M. J. 2005. Regulation of secondary metabolism in streptomycetes. Curr. Opin. Microbiol. 8:208-215.
4. Botsford, J. L., and J. G. Barman. 1992. Cyclic AMP in prokaryotes. Microbiol. Rev. 56:100-122.
5. Cashel, M., D. R. Gentry, V. J. Hernandez, and D. Vinella. 1996. The stringent response, p. 1458-1496. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. American Society for Microbiology, Washington, D. C.
6. Chakraburtty, R., and M. Bibb. 1997. The ppGpp synthetase gene (relA) of Streptomyces coelicolor A3(2) plays a conditional role in antibiotic production and morphological differentiation. J. Bacteriol. 179:5854-5861.
7. Chakraburtty, R., J. White, E. Takano, and M. Bibb. 1996. Cloning, characterization and disruption of a (p)ppGpp synthetase gene (relA) of Streptomyces coelicolor A3(2). Mol. Microbiol. 19:357-368.
8. Chandler, M. S. 1992. The gene encoding cAMP receptor protein is required for competence development in Haemophilus influenzae Rd. Proc. Natl. Acad. Sci. USA 89:1626-1630.
9. Chater, K. F., and M. J. Bibb, 1997. Regulation of bacterial antibiotic production, p. 57-105. In H. Kleinkauf and H. Von Dohren (ed.), Products of secondary metabolism. Biotechnology, vol. 6. VCH, Weinheim, Germany.
10. Chater, K. F., and D. A. Hopwood. 1993. Streptomyces, p. 83-89. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtitis and other gram-positive bacteria: biochemistry, physiology, and molecular genetics. American Society for Microbiology, Washington, D. C.
11. Chen, C. W., C. H. Huang, H. H. Lee, H. H. Tsai, and R. Kirby. 2002. Once the circle has been broken: dynamics and evolution of Streptomyces chromosomes. Trends Genet. 18:522-529.
12. Dworkin, J., and R. Losick. 2001. Linking nutritional status to gene activation and development. Genes Dev. 15:1051-1054.
13. Fuller, R. S., B. E. Funnell, and A. Kornberg. 1984. The dnaA protein complex with the E. coli chromosomal replication origin (oriC) and other DNA sites. Cell 38:889-900.
14. 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.
15. Hesketh, A., J. Sun, and M. Bibb. 2001. Induction of ppGpp synthesis in Streptomyces coelicolor A3(2) grown under conditions of nutritional sufficiency elicits actII-ORF4 transcription and actinorhodin biosynthesis. Mol. Microbiol. 39:136-144.
16. Hu, H., Q. Zhang, and K. Ochi. 2002. Activation of antibiotic biosynthesis by specified mutations in the rpoB gene (encoding the RNA polymerase β subunit) of Streptomyces lividans. J. Bacteriol. 184:3984-3991.
17. Huang, J., C. J. Lih, K. H. Pan, and S. N. Cohen. 2001. Global analysis of growth phase responsive gene expression and regulation of antibiotic biosynthetic pathways in Streptomyces coelicolor using DNA microarrays. Genes Dev. 15:3183-3192.
18. Hughes, P., A. Landoulsi, and M. Kohiyama. 1988. A novel role for cAMP in the control of the activity of the E. coli chromosome replication initiator protein, DnaA. Cell 55:343-350.
19. Hunter, I. S., and S. Baumberg. 1989. Molecular genetics of antibiotic formation, p. 121-162. In S. Baumberg, I. S. Hunter, and P. M. Rhodes (ed.), Microbial products: new approaches. Cambridge University, Cambridge, England.
20. Inaoka, T., and K. Ochi. 2002. RelA protein is involved in induction of genetic competence in certain Bacillus subtilis strains by moderating the level of intracellular GTP. J. Bacteriol. 184:3923-3930.
21. Inaoka, T., K. Takahashi, M. Ohnishi-Kameyama, M. Yoshida, and K. Ochi. 2003. Guanine nucleotides guanosine 5′-diphosphate 3′-diphosphate and GTP co-operatively regulate the production of an antibiotic bacilysin in Bacillus subtilis. J. Biol. Chem. 278:2169-2176.
22. Inaoka, T., K. Takahashi, H. Yada, M. Yoshida, and K. Ochi. 2004, RNA polymerase mutation activates the production of a dormant antibiotic 3, 3′-neotrehalosadiamine via an autoinduction mechanism in Bacillus subtilis. J. Biol. Chem. 279:3885-3892.
23. Jin, D. J., and C. A. Gross. 1988. Mapping and sequencing of mutations in the Escherichia coli rpoB gene that lead to rifampicin resistance. J. Mol. Biol. 202:45-58.
24. Jin, W., Y. G. Ryu, S. G. Kang, S. K. Kim, N. Saito, K. Ochi, S. H. Lee, and K. J. Lee. 2004. Two relA/spoT homologous genes are involved in the morphological and physiological differentiation of Streptomyces clavuligerus. Microbiology 150:1485-1493.
25. Kalderon, D., and G. M. Rubin. 1989. cGMP-dependent protein kinase genes in Drosophila. J. Biol. Chem. 264:10738-10748.
26. Kang, D. K., X. M. Li, K. Ochi, and S. Horinouchi. 1999. Possible involvement of cAMP in aerial mycelium formation and secondary metabolism in Streptomyces griseus. Microbiology 145:1161-1172.
27. Kawamoto, S., H. Watanabe, A. Hesketh, J. C. Ensign, and K. Ochi. 1997. Expression analysis of the ssgA gene product, associated with sporulation and cell division in Streptomyces griseus. Microbiology 143:1077-1086.
28. Kawamoto, S., M. Watanabe, N. Saito, A. Hesketh, K. Vachalova, K. Matsubara, and K. Ochi. 2001. Molecular and functional analyses of the gene (eshA) encoding the 52-kilodalton protein of Streptomyces coelicolor A3(2) required for antibiotic production. J. Bacteriol. 183:6009-6016.
29. Kawamoto, S, D. Zhang, and K. Ochi. 1997. Molecular analysis of the ribosomal L11 protein gene (rplK = relC) of Streptomyces griseus and identification of a deletion allele. Mol. Gen. Genet. 255:549-560.
30. Kim, D.-W., K. F. Chater, K.-J. Lee, and A. Hesketh. 2005. Effect of growth phase and the developmentally significant bldA-specified tRNA on the membrane-associated proteome of Streptomyces coelicolor. Microbiology 151:2707-2720.
31. Kwak, J., L. A. McCue, K. Trczianka, and K. E. Kendrick. 2001. Identification and characterization of a developmentally regulated protein, EshA, required for sporogenic hyphal branches in Streptomyces griseus. J. Bacteriol. 183:3004-3015.
32. Lai, C., J. Xu, Y. Tozawa, Y. Okamoto-Hosoya, X. Yao, and K. Ochi. 2002. Genetic and physiological characterization of rpoB mutations that activate antibiotic production in Streptomyces lividans. Microbiology 148:3365-3373.
33. McCue, L. A., K. A. McDonough, and C. E. Lawrence. 2000. Functional classification of cNMP-binding proteins and nucleotide cyclases with implications for novel regulatory pathways in Mycobacterium tuberculosis. Genome Res. 10:204-219.
34. Nicholson, M. L., M. Gaasenbeek, and D. E. Laudenbach. 1995. Two enzymes together capable of cysteine biosynthesis are encoded on a cyanobacterial plasmid. Mol. Gen. Genet. 247:623-632.
35. Nicholson, M. L., and D. E. Laudenbach. 1995. Genes encoded on a cyanobacterial plasmid are transcriptionally regulated by sulfur availability and CysR. J. Bacteriol. 177:2143-2150.
36. Ochi, K. 1987. Change in nucleotide pools during sporulation of Streptomyces griseus in submerged culture. J. Gen. Microbiol. 133:2787-2795.
37. Ochi, K. 1987. Metabolic initiation of differentiation and secondary metabolism by Streptomyces griseus: significance of the stringent response (ppGpp) and GTP content in relation to A factor. J. Bacteriol. 169:3608-3616.
38. Ochi, K. 1990. A relaxed (rel) mutant of Streptomyces coelicolor A3(2) with a missing ribosomal protein lacks the ability to accumulate ppGpp, A-factor and prodigiosin. J. Gen. Microbiol. 136:2405-2412.
39. Ochi, K. 1990. Streptomyces relC mutants with an altered ribosomai protein ST-L11 and genetic analysis of a Streptomyces griseus relC mutant. J. Bacteriol. 172:4008-4016.
40. Ochi, K., S. Okamoto, Y. Tozawa, T. Inaoka, T. Hosaka, J. Xu, and K. Kurosawa. 2004. Ribosome engineering and secondary metabolite production. Adv. Appl. Microbiol. 56:155-184.
41. Ochi, K., D. Zhang, S. Kawamoto, and A. Hesketh. 1997. Molecular and functional analysis of the ribosomal L11 and S12 protein genes (rplK and rpsL) of Streptomyces coelicolor A3(2). Mol. Gen. Genet. 256:488-498.
42. Okamoto, S., A. Lezhava, T. Hosaka, Y. Okamoto-Hosoya, and K. Ochi. 2003. Enhanced expression of S-adenosylmethionine synthetase causes over-production of actinorhodin in Streptomyces coelicolor A3(2). J. Bacteriol. 185:601-609.
43. Okamoto, S., and K. Ochi. 1998. An essential GTP-binding protein functions as a regulator for differentiation in Streptomyces coelicolor. Mol. Microbiol. 30:107-119.
44. Onaka, H., S. Taniguchi, H. Ikeda, Y. Igarashi, and T. Furumai. 2003. pTOYAMAcos, pTYM18, and pTYM19, actinomycete-Escherichia coli integrating vectors for heterologous gene expression. J. Antibiot. (Tokyo) 56:950-956.
45. Ratnayake-Lecamwasam, M., P. Serror, K. W. Wong, and A. L. Sonenshein. 2001. Bacillus subtilis CodY represses early-stationary-phase genes by sensing GTP levels. Genes Dev. 15:1093-1103.
46. Redenbach, M., H. M. Kieser, D. Denapaite, A. Eichner, J. Cullum, H. Kinashi, and D. A. Hopwood. 1996. A set of ordered cosmids and a detailed genetic and physical map for the 8 Mb Streptomyces coelicolor A3(2) chromosome. Mol. Microbiol. 21:77-96.
47. Saito, N., K. Matsubara, M. Watanabe, F. Kato, and K. Ochi. 2003. Genetic and biochemical characterization of EshA, a protein that forms large multimers and affects developmental processes in Streptomyces griseus. J. Biol. Chem. 278:5902-5911.
48. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
49. Severinov, K., M. Soushko, A. Goldfarb, and V. Nikiforrov. 1994. Rif mutations in the beginning of the Escherichia coli rpoB gene. Mol. Gen. Genet. 244:120-126.
50. Shabb, J. B., and J. D. Corbin. 1992. Cyclic nucleotide-binding domains in proteins having diverse functions. J. Biol. Chem. 267:5723-5726.
51. Singer, M., D. J. Jin, W. A. Walter, and C. A. Gross. 1993. Genetic evidence for the interaction between cluster I and cluster III rifampicin resistant mutations. J. Mol. Biol. 231:1-5.
52. Sun, J., A. Hesketh, and M. Bibb. 2001. Functional analysis of relA and rshA, two relA/spoT homologues of Streptomyces coelicolor A3(2). J. Bacteriol. 183:3488-3498.
53. Sun, J., G. H. Kelemen, J. M. Fernandez-Abalos, and M. J. Bibb. 1999. Green fluorescent protein as a reporter for spatial and temporal gene expression in Streptomyces coelicolor A3(2). Microbiology 145:2221-2227.
54. Susstrunk, U., J. Pidoux, S. Taubert, A. Ullmann, and C. J. Thompson. 1998. Pleiotropic effects of cAMP on germination, antibiotic biosynthesis and morphological development in Streptomyces coelicolor. Mol. Microbiol. 30:33-46.
55. 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 undecylprodigiosin in Streptomyces coelicolor A3(2). Mol. Microbiol. 6:2797-2804.
56. Takio, K., R. D. Wade, S. B. Smith, E. G. Krebs, K. A. Walsh, and K. Titani. 1984. Guanosine cyclic 3′,5′-phosphate dependent protein kinase, a chimeric protein homologous with two separate protein families. Biochemistry 23:4207-4218.
57. Triccas, J. A., N. Winter, P. W. Roche, A. Gilpin, K. E. Kendrick, and W. J. Britton. 1998. Molecular and immunological analyses of the Mycobacterium avium homolog of the immunodominant Mycobacterium leprae 35-kilodalton protein. Infect. Immun. 66:2684-2690.
58. von Meyenbyrg, K., and F. G. Hansen. 1996. Regulation of chromosome replication, p. 1555-1577. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. American Society for Microbiology, Washington, D. C.
59. Wichelhaus, T. A., V. Schafer, V. Brade, and B. Boddinghaus. 1999. Molecular characterization of rpoB mutations conferring cross-resistance to rifamycins on methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 43:2813-2816.
60. Wilchek, M., and Z. Selinger. 1974. The preparation and use of cyclic AMP Sepharose. Methods Enzymol. 38:385-387.
61. Winter, N., J. A. Triccas, B. Rivoire, M. C. Pessolani, K. Eiglmeier, E. M. Lim, S. W. Hunter, P. J. Brennan, and W. J. Britton. 1995. Characterization of the gene encoding the immunodominant 35 kDa protein of Mycobacterium leprae. Mol. Microbiol. 16:865-876.
62. Xu, J., Y. Tozawa, C. Lai, H. Hayashi, and K. Ochi. 2002. A rifampicin resistance mutation in the rpoB gene confers ppGpp-independent antibiotic production in Streptomyces coelicolor A3(2). Mol. Genet. Genomics 268:179-189.