Genetic Characterization of Two S-Adenosylmethionine-induced ABC Transporters Reveals Their Roles in Modulations of Secondary Metabolism and Sporulation in Streptomyces coelicolor M145

  • Shin, Su-Kyoung (Department of Biological Science, Institute of Bioscience and Biotechnology, Myongji University) ;
  • Park, Hyun-Suh (Department of Biological Science, Institute of Bioscience and Biotechnology, Myongji University) ;
  • Kwon, Hyung-Jin (Department of Biological Science, Institute of Bioscience and Biotechnology, Myongji University) ;
  • Yoon, Hyun-Jin (Department of Biological Science, Institute of Bioscience and Biotechnology, Myongji University) ;
  • Suh, Joo-Won (Department of Biological Science, Institute of Bioscience and Biotechnology, Myongji University)
  • Published : 2007.11.30

Abstract

S-Adenosylmethionine (SAM) was previously documented to activate secondary metabolism in a variety of Streptomyces spp. and to promote actinorhodin (ACT) and undecylprodigiosin (RED) in Streptomyces coelicolor. The SAM-induced proteins in S. coelicolor include several ABC transporter components (SCO5260 and SCO5477) including BldKB, the component of a well-known regulatory factor for differentiations. In order to assess the role of these ABC transporter complexes in differentiation of Streptomyces, SCO5260 and SCO5476, the first genes from the cognate complex clusters, were individually inactivated by gene replacement. Inactivation of either SCO5260 or SCO5476 led to impaired sporulation on agar medium, with the more drastic defect in the SCO5260 null mutant (${\Delta}SCO5260$). ${\Delta}SCO5260$ displayed growth retardation and reduced yields of ACT and RED in liquid cultures. In addition, SAM supplementation failed in promoting the production of ACT and RED in ${\Delta}SCO5260$. Inactivation of SCO5476 gave no significant change in growth and production of ACT and RED, but impaired the promoting effect of SAM on ACT production without interfering with the effect on RED production. The present study suggests that SAM induces several ABC transporters to modulate secondary metabolism and morphological development in S. coelicolor.

Keywords

References

  1. Abouhamad, W. N., M. Manson, M. M. Gibson, and C. F. Higgins. 1991. Peptide transport and chemotaxis in Escherichia coli and Salmonella typhimurium: Characterization of the dipeptide permease (Dpp) and the dipeptide-binding protein. Mol. Microbiol. 5: 1035-1047 https://doi.org/10.1111/j.1365-2958.1991.tb01876.x
  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, et al. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417: 141-147 https://doi.org/10.1038/417141a
  3. Chater, K. F. 2001. Regulation of sporulation in Streptomyces coelicolor A3(2): A checkpoint multiplex? Curr. Opin. Microbiol. 4: 667-673 https://doi.org/10.1016/S1369-5274(01)00267-3
  4. Chater, K. F. and G. Chandra. 2006. The evolution of development in Streptomyces analysed by genome comparisons. FEMS Microbiol. Rev. 30: 651-672 https://doi.org/10.1111/j.1574-6976.2006.00033.x
  5. Chong, Y., J. Young, J. Kim, Y. Lee, K. S. Park, J. H. Cho, H. J. Kwon, J. W. Suh, and Y. Lim. 2006. S-Adenosyl-L-methionine analogues to enhance the production of actinorhodin. J. Microbiol. Biotechnol. 16: 1154-1157
  6. Clewell, D. B., F. Y. An, S. E. Flannagan, M. Antiporta, and G. M. Dunny. 2000. Enterococcal sex pheromone precursors are part of signal sequences for surface lipoproteins. Mol. Microbiol. 35: 246-247 https://doi.org/10.1046/j.1365-2958.2000.01687.x
  7. Detmers, F. J., F. C. Lanfermeijer, and B. Poolman. 2001. Peptides and ATP binding cassette peptide transporters. Res. Microbiol. 152: 245-258 https://doi.org/10.1016/S0923-2508(01)01196-2
  8. Dunny, G. M. and B. A. Leonard. 1997. Cell-cell communication in Gram-positive bacteria. Annu. Rev. Microbiol. 51: 557-564
  9. Espartero, J., J. A. Pintor-Toro, and J. M. Pardo. 1994. Differential accumulation of S-adenosylmethionine synthetase transcripts in response to salt stress. Plant Mol. Biol. 25: 217-227 https://doi.org/10.1007/BF00023239
  10. 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
  11. Havarstein, L. S., G. Coomaraswamy, and D. A. Morrison. 1995. An unmodified heptadecapeptide pheromone induces competence for genetic transformation in Streptococcus pneumoniae. Proc. Natl. Acad. Sci. USA 92: 11140-11144
  12. Hillemann, D., A. Pühler, and W. Wohlleben. 1991. Gene disruption and gene replacement in Streptomyces via single stranded DNA transformation of integration vectors. Nucleic Acids Res. 19: 727-731 https://doi.org/10.1093/nar/19.4.727
  13. Hodgson, D. A. 2000. Primary metabolism and its control in streptomycetes: A most unusual group of bacteria. Adv. Microb. Physiol. 42: 47-238 https://doi.org/10.1016/S0065-2911(00)42003-5
  14. Holland, K. A. and I. B. Holland. 2005. Adventures with ABC-proteins: Highly conserved ATP-dependent transporters. Acta Microbiol. Immunol. Hung. 52: 309-322 https://doi.org/10.1556/AMicr.52.2005.3-4.4
  15. Kieser, T., M. J. Bibb, M. J. Buttner, K. F. Chater, and D. A. Hopwood. 2000. Practical Streptomyces Genetics. The John Innes Foundation, Norwich, England
  16. Kim, D. J., J. H. Huh, Y. Y. Yang, C. M. Kang, I. H. Lee, C. G. Hyun, S. K. Hong, and J. W. Suh. 2003. Accumulation of S-adenosyl-L-methionine enhances production of actinorhodin but inhibits sporulation in Streptomyces lividans TK23. J. Bacteriol. 185: 592-600 https://doi.org/10.1128/JB.185.2.592-600.2003
  17. Kim, D. W., K. F. Chater, K. J. Lee, and A. Hesketh. 2005. Effects of growth phase and the developmentally significant bldA-specific tRNA on the membrane-associated proteome of Streptomyces coelicolor. Microbiology 151: 2707-2720 https://doi.org/10.1099/mic.0.28000-0
  18. Lee, Y., J. Young, H. J. Kwon, J. W. Suh, J. Kim, Y. Chong, and Y. Lim. 2006. AdoMet derivatives induce the production of actinorhodin in Streptomyces coelicolor. J. Microbiol. Biotechnol. 16: 965-968
  19. Leonard, B. A. B., A. Podbielski, P. J. Hedberg, and G. M. Dunny. 1996. Enterococcus faecalis pheromone binding protein, PrgZ, recruits a chromosomal oligopeptide permease system to import sex pheromone cCF10 for induction of conjugation. Proc. Natl. Acad. Sci. USA 93: 260-264
  20. Levdikov, V. M., E. V. Blagova, J. A. Brannigan, L. Wright, A. A. Vagin, and A. J. Wilkinson. 2005. The structure of the oligopeptide-binding protein, AppA, from Bacillus subtilis in complex with a nonapeptide. J. Mol. Biol. 345: 879-892 https://doi.org/10.1016/j.jmb.2004.10.089
  21. Linton, K. J. and C. F. Higgins. 1998. The Escherichia coli ATP-binding cassette (ABC) proteins. Mol. Microbiol. 28: 5-13 https://doi.org/10.1046/j.1365-2958.1998.00764.x
  22. Ma, H. and K. Kendall. 1994. Cloning and analysis of a gene cluster from Streptomyces coelicolor that causes accelerated aerial mycelium formation in Streptomyces lividans. J. Bacteriol. 176: 3800-3811 https://doi.org/10.1128/jb.176.12.3800-3811.1994
  23. Magnuson, R., J. Solomon, and A. D. Grossman. 1994. Biochemical and genetic characterization of a competence pheromone from B. subtilis. Cell 77: 207-216 https://doi.org/10.1016/0092-8674(94)90313-1
  24. Nguyen, K. T., J. M. Willey, L. D. Nguyen, L. T. Nguyen, P. H. Viollier, and C. J. Thompson. 2002. A central regulator of morphological differentiation in the multicellular bacterium Streptomyces coelicolor. Mol. Microbiol. 46: 1223-1238 https://doi.org/10.1046/j.1365-2958.2002.03255.x
  25. Nodwell, J. R. and R. Losick. 1998. Purification of an extracellular signaling molecule involved in production of aerial mycelium by Streptomyces coelicolor. J. Bacteriol. 180: 1334-1337
  26. 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 https://doi.org/10.1046/j.1365-2958.1996.01540.x
  27. Nodwell, J. R., M. Yang, D. Kuo, and R. Losick. 1999. Extracellular complementation and the identification of additional genes involved in aerial mycelium formation in Streptomyces coelicolor. Genetics 151: 569-584
  28. Novotna, J., J. Vohradsky, P. Berndt, H. Gramajo, H. Langen, X. M. Li, W. Minas, L. Orsaria, D. Roeder, and C. J. Thompson. 2003. Proteomic studies of diauxic lag in the differentiating prokaryotes Streptomyces coelicolor reveal a regulatory network of stress-induced proteins and central metabolic enzymes. Mol. Microbiol. 48: 1289-1303 https://doi.org/10.1046/j.1365-2958.2003.03529.x
  29. Okamoto, S., A. Lezhava, T. Hosaka, Y. Okamoto-Hosoya, and K. Ochi. 2003. Enhanced expression of Sadenosylmethionine synthetase causes overproduction of actinorhodin in Streptomyces coelicolor A3(2). J. Bacteriol. 185: 601-609 https://doi.org/10.1128/JB.185.2.601-609.2003
  30. Park, H. S., S. K. Shin, Y. Y. Yang, H. J. Kwon, and J. W. Suh. 2005. Accumulation of S-adenosylmethionine induced oligopeptide transporters including BldK to regulate differentiation events in Streptomyces coelicolor M145. FEMS Microbiol. Lett. 249: 199-206 https://doi.org/10.1016/j.femsle.2005.05.047
  31. Podbielski, A., B. Pohl, M. Woischnik, C. Körner, K. H. Schmidt, E. Rozdzinski, and B. A. Leonard. 1996. Molecular characterization of group A streptococcal (GAS) oligopeptide permease (opp) and its effect on cysteine protease production. Mol. Microbiol. 21: 1087-1099 https://doi.org/10.1046/j.1365-2958.1996.661421.x
  32. Rudner, D. Z., J. R. LeDeaux, K. Ireton, and A. D. Grossman. 1991. The spo0K locus of Bacillus subtilis is homologous to the oligopermease locus and is required for sporulation and competence. J. Bacteriol. 173: 1388-1398 https://doi.org/10.1128/jb.173.4.1388-1398.1991
  33. Sanchez-Aguayo, I., J. M. Rodriguez-Galán, R. García, J. Torreblanca, and J. M. Pardo. 2004. Salt stress enhances xylem development and expression of S-adenosyl-L-methionine synthetase in lignifying tissues of tomato plants. Planta 220: 278-285 https://doi.org/10.1007/s00425-004-1350-2
  34. Schroder, G., J. Eichel, S. Breinig, and J. Schroder. 1997. Three differentially expressed S-adenosylmethionine synthetases from Catharanthus roseus: Molecular and functional characterization. Plant Mol. Biol. 33: 211-222 https://doi.org/10.1023/A:1005711720930
  35. Shin, S. K., D. Xu, H. J. Kwon, and J. W. Suh. 2006. S-Adenosylmethionine activates adpA transcription and promotes streptomycin biosynthesis in Streptomyces griseus. FEMS Microbiol. Lett. 259: 53-59 https://doi.org/10.1111/j.1574-6968.2006.00246.x
  36. Stragier, P. and R. Losick. 1996. Molecular genetics of sporulation in Bacillus subtilis. Annu. Rev. Genet. 3: 203-212
  37. 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 https://doi.org/10.1046/j.1365-2958.1998.01033.x
  38. Ueda, K., H. Takano, M. Nishimoto, H. Inaba, and T. Beppu. 2005. Dual transcriptional control of amfTSBA, which regulates the onset of cellular differentiation in Streptomyces griseus. J. Bacteriol. 187: 135-142 https://doi.org/10.1128/JB.187.1.135-142.2005
  39. Van Breusegem, F., R. Dekeyser, J. Gielen, M. Van Montagu, and A. Caplan. 1994. Characterization of a S-adenosylmethionine synthetase gene in rice. Plant Physiol. 105: 1463-1464 https://doi.org/10.1104/pp.105.4.1463
  40. Willey, J. M., A. Willems, S. Kodani, and J. R. Nodwell. 2006. Morphogenetic surfactants and their role in the formation of aerial hyphae in Streptomyces coelicolor. Mol. Microbiol. 59: 731-742 https://doi.org/10.1111/j.1365-2958.2005.05018.x
  41. Yang, Y. Y., X. Q. Zhao, Y. Y. Jin, J. H. Huh, J. H. Cheng, D. Singh, H. J. Kwon, and J. W. Suh. 2006. Novel function of cytokinin: A signaling molecule for promotion of antibiotic production in streptomycetes. J. Microbiol. Biotechnol. 16: 896-900
  42. Zhao, X. Q., Y. Y. Jin, H. J. Kwon, Y. Y. Yang, and J. W. Suh. 2006. S-Adenosylmethionine (SAM) regulates antibiotic biosynthesis in Streptomyces spp. in a mode independent of its role as a methyl donor. J. Microbiol. Biotechnol. 16: 927-932