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BioMed Research International
Volume 2013 (2013), Article ID 549737, 10 pages
http://dx.doi.org/10.1155/2013/549737
Review Article

Identification and Biotechnological Application of Novel Regulatory Genes Involved in Streptomyces Polyketide Overproduction through Reverse Engineering Strategy

Department of Biological Engineering, Inha University, Incheon 402-751, Republic of Korea

Received 13 November 2012; Revised 15 December 2012; Accepted 5 January 2013

Academic Editor: Sofiane Ghorbel

Copyright © 2013 Ji-Hye Nah et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. H. Baltz, “Molecular engineering approaches to peptide, polyketide and other antibiotics,” Nature Biotechnology, vol. 24, no. 12, pp. 1533–1540, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. D. A. Hopwood, “Soil to genomics: the Streptomyces chromosome,” Annual Review of Genetics, vol. 40, pp. 1–23, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. M. J. Bibb, “Regulation of secondary metabolism in streptomycetes,” Current Opinion in Microbiology, vol. 8, no. 2, pp. 208–215, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. C. Khosla, “Structures and mechanisms of polyketide synthases,” Journal of Organic Chemistry, vol. 74, no. 17, pp. 6416–6420, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. L. Katz and S. Donadio, “Polyketide synthesis: prospects for hybrid antibiotics,” Annual Review of Microbiology, vol. 47, pp. 875–912, 1993. View at Scopus
  6. C. Hertweck, A. Luzhetskyy, Y. Rebets, and A. Bechthold, “Type II polyketide synthases: gaining a deeper insight into enzymatic teamwork,” Natural Product Reports, vol. 24, no. 1, pp. 162–190, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. K. Watanabe, A. P. Praseuth, and C. C. Wang, “A comprehensive and engaging overview of the type III family of polyketide synthases,” Current Opinion in Chemical Biology, vol. 11, no. 3, pp. 279–286, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. H. G. Floss, “Combinatorial biosynthesis-Potential and problems,” Journal of Biotechnology, vol. 124, no. 1, pp. 242–257, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. S. H. Kang, J. Huang, H. N. Lee, Y. A. Hur, S. N. Cohen, and E. S. Kim, “Interspecies DNA microarray analysis identifies wblA as a pleiotropic down-regulator of antibiotic biosynthesis in Streptomyces,” Journal of Bacteriology, vol. 189, no. 11, pp. 4315–4319, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. J. H. Noh, S. H. Kim, H. N. Lee, S. Y. Lee, and E. S. Kim, “Isolation and genetic manipulation of the antibiotic down-regulatory gene, wblA ortholog for doxorubicin-producing Streptomyces strain improvement,” Applied Microbiology and Biotechnology, vol. 86, no. 4, pp. 1145–1153, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. J. H. Nah, S. H. Park, H. M. Yoon, S. S. Choi, C. H. Lee, and E. S. Kim, “Identification and characterization of wblA-dependent tmcT regulation during tautomycetin biosynthesis in Streptomyces sp. CK4412,” Biotechnology Advances, vol. 30, no. 1, pp. 202–209, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. H. Ikeda, J. Ishikawa, A. Hanamoto et al., “Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis,” Nature Biotechnology, vol. 21, no. 5, pp. 526–531, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. Ohnishi, J. Ishikawa, H. Hara et al., “Genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO 13350,” Journal of Bacteriology, vol. 190, no. 11, pp. 4050–4060, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. M. H. Medema, A. Trefzer, A. Kovalchuk, M. van den Berg, U. Muller, W. Heijne, et al., “The sequence of a 1.8-mb bacterial linear plasmid reveals a rich evolutionary reservoir of secondary metabolic pathways,” Genome Biology and Evolution, vol. 2, pp. 212–224, 2010. View at Publisher · View at Google Scholar
  15. M. Rabyk, B. Ostash, Y. Rebets, S. Walker, and V. Fedorenko, “Streptomyces ghanaensis pleiotropic regulatory gene wblAgh influences morphogenesis and moenomycin production,” Biotechnology Letters, vol. 33, no. 12, pp. 2481–2486, 2011. View at Publisher · View at Google Scholar
  16. D. J. Wilson, Y. Xue, K. A. Reynolds, and D. H. Sherman, “Characterization and analysis of the pikD regulatory factor in the pikromycin biosynthetic pathway of Streptomyces venezuelae,” Journal of Bacteriology, vol. 183, no. 11, pp. 3468–3475, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. E. J. Lee, N. Karoonuthaisiri, H. S. Kim et al., “A master regulator σB governs osmotic and oxidative response as well as differentiation via a network of sigma factors in Streptomyces coelicolor,” Molecular Microbiology, vol. 57, no. 5, pp. 1252–1264, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. G. P. Van Wezel and K. J. McDowall, “The regulation of the secondary metabolism of Streptomyces: new links and experimental advances,” Natural Product Reports, vol. 28, no. 7, pp. 1311–1333, 2011. View at Publisher · View at Google Scholar
  19. F. Lombó, A. F. Braña, C. Méndez, and J. A. Salas, “The mithramycin gene cluster of Streptomyces argillaceus contains a positive regulatory gene and two repeated DNA sequences that are located at both ends of the cluster,” Journal of Bacteriology, vol. 181, no. 2, pp. 642–647, 1999. View at Scopus
  20. L. Retzlaff and J. Distler, “The regulator of streptomycin gene expression, StrR, of Streptomyces griseus is a DNA binding activator protein with multiple recognition sites,” Molecular Microbiology, vol. 18, no. 1, pp. 151–162, 1995. View at Scopus
  21. L. Tang, A. Grimm, Y. X. Zhang, and C. R. Hutchinson, “Purification and characterization of the DNA-binding protein Dnrl, a transcriptional factor of daunorubicin biosynthesis in Streptomyces peucetius,” Molecular Microbiology, vol. 22, no. 5, pp. 801–813, 1996. View at Scopus
  22. P. Arias, M. A. Fernández-Moreno, and F. Malpartida, “Characterization of the pathway-specific positive transcriptional regulator for actinorhodin biosynthesis in Streptomyces coelicolor A3(2) as a DNA-binding protein,” Journal of Bacteriology, vol. 181, no. 22, pp. 6958–6968, 1999. View at Scopus
  23. A. Wietzorrek and M. Bibb, “A novel family of proteins that regulates antibiotic production in Streptomycetes appears to contain an OmpR-like DNA-binding fold,” Molecular Microbiology, vol. 25, no. 6, pp. 1181–1184, 1997. View at Scopus
  24. S. D. Bentley, K. F. Chater, A. M. Cerdeno-Tarraga, G. L. Challis, N. R. Thomson, K. D. James, et al., “Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2),” Nature, vol. 417, no. 6885, pp. 141–147, 2002. View at Publisher · View at Google Scholar
  25. J. Huang, C. J. Lih, K. H. Pan, and S. N. Cohen, “Global analysis of growth phase responsive gene expression and regulation of antibiotic biosynthetic pathways in Streptomyces coelicolor using DNA microarrays,” Genes and Development, vol. 15, no. 23, pp. 3183–3192, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. A. M. Lum, J. Huang, C. R. Hutchinson, and C. M. Kao, “Reverse engineering of industrial pharmaceutical-producing actinomycete strains using DNA microarrays,” Metabolic Engineering, vol. 6, no. 3, pp. 186–196, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. W. Lian, K. P. Jayapal, S. Charaniya et al., “Genome-wide transcriptome analysis reveals that a pleiotropic antibiotic regulator, AfsS, modulates nutritional stress response in Streptomyces coelicolor A3(2),” BMC Genomics, vol. 9, article 56, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. J. R. Yang, E. Song, B. G. Kim, E. S. Kim, J. K. Sohng, and M. K. Oh, “Expression profiling of Streptomyces peucetius metabolic genes using DNA microarray analysis,” Biotechnology and Bioprocess Engineering, vol. 13, no. 6, pp. 738–744, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Ochi and T. Hosaka, “New strategies for drug discovery: activation of silent or weakly expressed microbial gene clusters,” Applied Microbiology and Biotechnology, vol. 97, no. 1, pp. 87–98, 2013. View at Publisher · View at Google Scholar
  30. L. Laureti, L. Song, S. Huang et al., “Identification of a bioactive 51-membered macrolide complex by activation of a silent polyketide synthase in Streptomyces ambofaciens,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 15, pp. 6258–6263, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Craney, C. Ozimok, S. M. Pimentel-Elardo, A. Capretta, and J. R. Nodwell, “Chemical perturbation of secondary metabolism demonstrates important links to primary metabolism,” Chemistry & Biology, vol. 19, pp. 1020–1027, 2012. View at Publisher · View at Google Scholar
  32. P. Jakimowicz, M. R. Cheesman, W. R. Bishai, K. F. Chater, A. J. Thomson, and M. J. Buttner, “Evidence that the Streptomyces developmental protein WhiD, a member of the WhiB family, binds a [4Fe-4S] cluster,” Journal of Biological Chemistry, vol. 280, no. 9, pp. 8309–8315, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. J. A. Soliveri, J. Gomez, W. R. Bishai, and K. F. Chater, “Multiple paralogous genes related to the Streptomyces coelicolor developmental regulatory gene whiB are present in Streptomyces and other Actinomycetes,” Microbiology, vol. 146, no. 2, pp. 333–343, 2000. View at Scopus
  34. K. Fowler-Goldsworthy, B. Gust, S. Mouz, G. Chandra, K. C. Findlay, and K. F. Chater, “The actinobacteria-specific gene wblA controls major developmental transitions in Streptomyces coelicolor A3(2),” Microbiology, vol. 157, no. 5, pp. 1312–1328, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. J. S. Kim, H. N. Lee, P. Kim, H. S. Lee, and E. S. Kim, “Negative role of wblA in response to oxidative stress in Streptomyces coelicolor,” Journal of Microbiology and Biotechnology, vol. 22, no. 6, pp. 736–741, 2012. View at Publisher · View at Google Scholar
  36. H. N. Lee, J. Huang, J. H. Im et al., “Putative TetR family transcriptional regulator SCO1712 encodes an antibiotic downregulator in Streptomyces coelicolor,” Applied and Environmental Microbiology, vol. 76, no. 9, pp. 3039–3043, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. N. P. Niraula, S. H. Kim, J. K. Sohng, and E. S. Kim, “Biotechnological doxorubicin production: pathway and regulation engineering of strains for enhanced production,” Applied Microbiology and Biotechnology, vol. 87, no. 4, pp. 1187–1194, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. S. S. Choi, Y. A. Hur, D. H. Sherman, and E. S. Kim, “Isolation of the biosynthetic gene cluster for tautomycetin, a linear polyketide T cell-specific immunomodulator from Streptomyces sp. CK4412,” Microbiology, vol. 153, no. 4, pp. 1095–1102, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. X. C. Cheng, T. Kihara, X. Ying, et al., “A new antibiotic, tautomycetin,” Journal of Antibiotics, vol. 42, no. 1, pp. 141–144, 1989. View at Scopus
  40. J. H. Shim, H. K. Lee, E. J. Chang et al., “Immunosuppressive effects of tautomycetin in vivo and in vitro via T cell-specific apoptosis induction,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 16, pp. 10617–10622, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. J. H. Lee, J. S. Lee, S. E. Kim et al., “Tautomycetin inhibits growth of colorectal cancer cells through p21cip/WAF1 induction via the extracellular signal-regulated kinase pathway,” Molecular Cancer Therapeutics, vol. 5, no. 12, pp. 3222–3231, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. S. H. Kim, H. N. Lee, H. J. Kim, and E. S. Kim, “Transcriptome analysis of an antibiotic downregulator mutant and synergistic actinorhodin stimulation via disruption of a precursor flux regulator in Streptomyces coelicolor,” Applied and Environmental Microbiology, vol. 77, no. 5, pp. 1872–1877, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. I. Borodina, J. Siebring, J. Zhang et al., “Antibiotic overproduction in Streptomyces coelicolor A3(2) mediated by phosphofructokinase deletion,” Journal of Biological Chemistry, vol. 283, no. 37, pp. 25186–25199, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. J. P. Gomez-Escribano and M. J. Bibb, “Engineering Streptomyces coelicolor for heterologous expression of secondary metabolite gene clusters,” Microbial Biotechnology, vol. 4, no. 2, pp. 207–215, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. R. H. Baltz, “Streptomyces and Saccharopolyspora hosts for heterologous expression of secondary metabolite gene clusters,” Journal of Industrial Microbiology and Biotechnology, vol. 37, no. 8, pp. 759–772, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Komatsu, T. Uchiyama, S. Omura, D. E. Cane, and H. Ikeda, “Genome-minimized Streptomyces host for the heterologous expression of secondary metabolism,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 6, pp. 2646–2651, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. H. N. Lee, H. J. Kim, P. Kim, H. S. Lee, and E. S. Kim, “Minimal polyketide pathway expression in an actinorhodin cluster-deleted and regulation-stimulated Streptomyces coelicolor,” Journal of Industrial Microbiology and Biotechnology, vol. 39, no. 5, pp. 805–811, 2012. View at Publisher · View at Google Scholar
  48. E. S. Kim, K. D. Cramer, A. L. Shreve, and D. H. Sherman, “Heterologous expression of an engineered biosynthetic pathway: functional dissection of type II polyketide synthase components in Streptomyces species,” Journal of Bacteriology, vol. 177, no. 5, pp. 1202–1207, 1995. View at Scopus