Accumulation ofS-Adenosyl-l-Methionine Enhances Production of Actinorhodin but Inhibits Sporulation inStreptomyces lividansTK23
10.1128/jb.185.2.592-600.2003
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

ABSTRACTS-Adenosyl-l-methionine synthetase (SAM-s) catalyzes the biosynthesis of SAM from ATP andl-methionine. Despite extensive research with many organisms, its role inStreptomycessp. remains unclear. In the present study, the putative SAM-s gene was isolated from a spectinomycin producer,Streptomyces spectabilis. The purified protein from the transformedEscherichia coliwith the isolated gene synthesized SAM froml-methionine and ATP in vitro, strongly indicating that the isolated gene indeed encoded the SAM-s protein. The overexpression of the SAM-s gene inStreptomyces lividansTK23 inhibited sporulation and aerial mycelium formation but enhanced the production of actinorhodin in both agar plates and liquid media. Surprisingly, the overexpressed SAM was proven by Northern analysis to increase the production of actinorhodin through the induction ofactII-ORF4, a transcription activator of actinorhodin biosynthetic gene clusters. In addition, we found that a certain level of intracellular SAM is critical for the induction of antibiotic biosynthetic genes, since the control strain harboring only the plasmid DNA did not show any induction ofactII-ORF4 until it reached a certain level of SAM in the cell. From these results, we concluded that the SAM plays important roles as an intracellular factor in both cellular differentiation and antibiotic production inStreptomycessp.

Bibliography

Kim, D.-J., Huh, J.-H., Yang, Y.-Y., Kang, C.-M., Lee, I.-H., Hyun, C.-G., Hong, S.-K., & Suh, J.-W. (2003). Accumulation ofS-Adenosyl-l-Methionine Enhances Production of Actinorhodin but Inhibits Sporulation inStreptomyces lividansTK23. Journal of Bacteriology, 185(2), 592–600.

Authors 8
  1. Dong-Jin Kim (first)
  2. Jung-Hyun Huh (additional)
  3. Young-Yell Yang (additional)
  4. Choong-Min Kang (additional)
  5. In-Hyung Lee (additional)
  6. Chang-Gu Hyun (additional)
  7. Soon-Kwang Hong (additional)
  8. Joo-Won Suh (additional)
References 42 Referenced 88
  1. 10.1038/417141a
  2. Brian, A., M. Rudd, and D. A. Hopwood. 1979. Genetics of actinorhodin biosynthesis by Streptomyces coelicolor A3(2). J. Gen. Microbiol.114:35-43. (10.1099/00221287-114-1-35) / J. Gen. Microbiol. (1979)
  3. Cantoni G. L. 1977. The biochemistry of adenosylmethionine p. 557-577. In F. Salvatore E. Vorek V. Zappia H. G. Williams-Ashman and F. Schlenk (ed.) S -Adenosylmethionine. Columbia University Press New York N.Y.
  4. 10.1128/jb.179.18.5854-5861.1997
  5. Champness W. C. and K. F. Chater. 1994. Regulation and integration of antibiotic production and morphological differentiation in Streptomyces spp. p. 61-93. In C. P. Piggot J. Moran and P. Youngman (ed.) Regulation of bacterial differentiation. American Society for Microbiology Washington D.C.
  6. Champness, W., P. Riggle, T. Adamidis, and P. Vandervere. 1992. Identification of Streptomyces coelicolor genes involved in regulation of antibiotic synthesis. Gene115:55-60. (10.1016/0378-1119(92)90540-6) / Gene (1992)
  7. Chater, K. F. 1989. Multilevel regulation of Streptomyces differentiation. Trends Genet.5:372-377. (10.1016/0168-9525(89)90172-8) / Trends Genet. (1989)
  8. Chater, K. F. 1993. Genetics of differentiation in Streptomyces. Annu. Rev. Microbiol.47:685-713. (10.1146/annurev.mi.47.100193.003345) / Annu. Rev. Microbiol. (1993)
  9. Chater K. F. and D. A. Hopwood. 1993. Streptomyces p. 83-89. In A. L. Sonenshein J. A. Hoch and R. Losick (ed.) Bacillus subtilis and other gram-positive bacteria: biochemistry physiology and molecular genetics. American Society for Microbiology Washington D.C. (10.1128/9781555818388.ch6)
  10. Chater, K. F., and M. J. Bibb. 1997. Regulation of bacterial antibiotic production. Bio/Technology7:57-105. / Bio/Technology (1997)
  11. Coco, E. A., K. E. Narva, and J. S. Feitelson. 1991. New classes of Streptomyces coelicolor A3(2) mutants blocked in undecylprodigiosin (Red) biosynthesis. Mol. Gen. Genet.227:28-32. (10.1007/BF00260702) / Mol. Gen. Genet. (1991)
  12. Fernandez-Moreno, M. A., J. L. Caballero, D. A. Hopwood, and F. Malpartida. 1991. The act cluster contains regulatory and antibiotic export genes, direct targets for translational control by the bldA tRNA gene of Streptomyces. Cell66:769-780. (10.1016/0092-8674(91)90120-N) / Cell (1991)
  13. Gross, A., S. Geresh, and G. M. Whitesides. 1983. Enzymatic synthesis of S-adenosyl-l-methionine from l-methionine and ATP. Appl. Biochem. Biotechnol.8:415-422. (10.1007/BF02779914) / Appl. Biochem. Biotechnol. (1983)
  14. Hara, O., and T. Beppu. 1982. Induction of streptomycin inactivating enzyme by A-factor in Streptomyces griseus. J. Antibiot.35:1208-1215. (10.7164/antibiotics.35.1208) / J. Antibiot. (1982)
  15. Hara, O., and T. Beppu. 1982. Mutants blocked in streptomycin production in Streptomyces griseus: the role of A-factor. J. Antibiot.35:349-358. (10.7164/antibiotics.35.349) / J. Antibiot. (1982)
  16. Hilti, N., R. Graub, M. Jorg, P. Arnold, A. Schweingruber, and M. E. Schweingruber. 2000. Gene SAM1 encoding adenosylmethionine synthetase: effects of its expression in the fission yeast Schizosaccharomyces pombe. Yeast16:1-10. (10.1002/(SICI)1097-0061(20000115)16:1<1::AID-YEA501>3.0.CO;2-K) / Yeast (2000)
  17. Hopwood, D. A. 1988. Towards an understanding of gene switching in Streptomyces, the basis of sporulation and antibiotic production. Proc. R. Soc. Lond. Ser. B235:121-138. (10.1098/rspb.1988.0067) / Proc. R. Soc. Lond. Ser. B (1988)
  18. 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. John Innes Foundation Norwich England.
  19. Hunter H. I. 1995. Gene cloning in Streptomyces p. 19-44. In D. M. Glover (ed.) Gene cloning volume: a practical approach 2nd ed. IRL Press Oxford United Kingdom.
  20. Hyun, C. G., S. S. Kim, J. K. Sohng, J. J. Hahn, J. W. Kim, and J. W. Suh. 2000. An efficient approach for cloning the dNDP-glucose synthetase gene from actinomycins and its application in Streptomyces spectabilis, a spectinomycin producer. FEMS Microbiol. Lett.183:183-189. (10.1111/j.1574-6968.2000.tb08955.x) / FEMS Microbiol. Lett. (2000)
  21. Kelemen, G. H., P. H. Viollier, J. Tenor, L. Marri, M. J. Buttner, and C. J. Thompson. 2001. A connection between stress and development in the multicellular prokaryote Streptomyces coelicolor A3(2). Mol. Microbiol.40:804-814. (10.1046/j.1365-2958.2001.02417.x) / Mol. Microbiol. (2001)
  22. Kieser T. M. J. Bibb K. F. Chater and D. A. Hopwood. 2000. Practical Streptomyces genetics p. 10-16. John Innes Foundation Norwich England.
  23. 10.1128/jb.177.5.1202-1207.1995
  24. Kwon, H. J., S. Y. Lee, S. K. Hong, U. M. Park, and J. W. Suh. 1999. Heterologous expression of Streptomyces albus genes linked to an integrating element and activation of antibiotic production. J. Microbiol. Biotechnol.9:488-497. / J. Microbiol. Biotechnol. (1999)
  25. Liao, X., L. C. Vining, and J. L. Doull. 1995. Physiological control of trophophase-idiophase separation in streptomycete cultures producing secondary metabolites. Can. J. Microbiol.41:309-315. (10.1139/m95-043) / Can. J. Microbiol. (1995)
  26. Malpartida, F., and D. A. Hopwood. 1986. Physical and genetic characterization of the gene cluster for the antibiotic actinorhodin in Streptomyces coelicolor A3(2). Mol. Gen. Genet.205:66-73. (10.1007/BF02428033) / Mol. Gen. Genet. (1986)
  27. Mato, J. M., L. Alvarez, P. Ortiz, and M. A. Pajares. 1997. S-adenosylmethionine synthesis: molecular mechanisms and clinical implications. Pharmacol. Ther.73:265-280. (10.1016/S0163-7258(96)00197-0) / Pharmacol. Ther. (1997)
  28. 10.1128/jb.169.8.3608-3616.1987
  29. 10.1128/jb.152.1.400-410.1982
  30. Okamoto S. L. Alexander T. Hosaka Y. Okamoto-Hosoya and K. Ochi. 2002. Enhanced expression of S -adenosylmethionine synthetase causes overproduction of actinorhodin in Streptomyces coelicolor A3(2). J. Bacteriol. 185: 601-609. (10.1128/JB.185.2.601-609.2003)
  31. 10.1046/j.1365-2958.1996.6191336.x
  32. Romero, M. N., and R. P. Mellado. 1995. Activation of the actinorhodin biosynthetic pathway in Streptomyces lividans. FEMS Microbiol. Lett.127:79-84. (10.1111/j.1574-6968.1995.tb07453.x) / FEMS Microbiol. Lett. (1995)
  33. Rudd, B. A., and D. A. Hopwood. 1980. A pigmented mycelial antibiotic in Streptomyces coelicolor: control by a chromosomal gene cluster. J. Gen. Microbiol.119:333-340. / J. Gen. Microbiol. (1980)
  34. 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.
  35. Scarpa, S., L. Narzi, M. Lucarelli, L. Orru, and R. Strom. 2001. Erythroid differentiation and regulatory gene expression are modulated by adenosine derivatives interfering with S-adenosylmethionine metabolic pathway. J. Cell Biochem.81:401-412. (10.1002/1097-4644(20010601)81:3<401::AID-JCB1054>3.0.CO;2-U) / J. Cell Biochem. (2001)
  36. Shapiro S. 1989. Regulation of secondary metabolism in Actinomycetes p. 50-64. CRC Press Inc. Boca Raton Fla.
  37. Shelly, C. L. 2000. S-adenosylmethionine. Int. J. Biochem. Cell Biol.32:391-395. (10.1016/S1357-2725(99)00139-9) / Int. J. Biochem. Cell Biol. (2000)
  38. Tabor, C. W., and H. Tabor. 1984. Methionine adenosyltransferase (S-adenosylmethionine synthetase) and S-adenosylmethionine decarboxylase. Adv. Enzymol.56:251-282. / Adv. Enzymol. (1984)
  39. Usin E. R. T. Borchardt and C. R. Creveling. 1982. Biochemistry of S -adenosylmethionine and related compounds. Macmillan Press London England.
  40. 10.1128/jb.171.11.5872-5881.1989
  41. Wei, Y., and E. B. Newman. 2002. Studies on the role of the metK gene product of Escherichia coli K-12. Mol. Microbiol.43:1651-1656. (10.1046/j.1365-2958.2002.02856.x) / Mol. Microbiol. (2002)
  42. Yijun, Z., Q. Chao, C. Wen-Qing, V. Anjana, M. Yeldandi, R. Samvasiva, and K. R. Janadan. 2001. Cloning and characterization of PIMT, a protein with a methyltransferase domain, which interacts with and enhances nuclear receptor coactivator PRIP function. Proc. Natl. Acad. Sci. USA98:10380-10385. (10.1073/pnas.181347498) / Proc. Natl. Acad. Sci. USA (2001)
Dates
Type When
Created 22 years, 7 months ago (Jan. 2, 2003, 2:30 p.m.)
Deposited 2 years, 4 months ago (April 25, 2023, 1:47 p.m.)
Indexed 1 day, 16 hours ago (Aug. 26, 2025, 2:57 a.m.)
Issued 22 years, 7 months ago (Jan. 15, 2003)
Published 22 years, 7 months ago (Jan. 15, 2003)
Published Print 22 years, 7 months ago (Jan. 15, 2003)
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@article{Kim_2003, title={Accumulation ofS-Adenosyl<scp>-l-</scp>Methionine Enhances Production of Actinorhodin but Inhibits Sporulation inStreptomyces lividansTK23}, volume={185}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.185.2.592-600.2003}, DOI={10.1128/jb.185.2.592-600.2003}, number={2}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Kim, Dong-Jin and Huh, Jung-Hyun and Yang, Young-Yell and Kang, Choong-Min and Lee, In-Hyung and Hyun, Chang-Gu and Hong, Soon-Kwang and Suh, Joo-Won}, year={2003}, month=jan, pages={592–600} }