Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지

Overexpression of Shinorhizobium meliloti Hemoprotein in Streptomyces lividans to Enhance Secondary Metabolite Production

  • Kim, Yoon-Jung (Department of Chemical and Biomolecular Engineering, Korea Advanced Institute of Science and Technology) ;
  • Sa, Soon-Ok (Department of Chemical and Biomolecular Engineering, Korea Advanced Institute of Science and Technology) ;
  • Chang, Yong-Keun (Department of Chemical and Biomolecular Engineering, Korea Advanced Institute of Science and Technology) ;
  • Hong, Soon-Kwang (Division of Bioscience and Bioinformatics, Myongji University) ;
  • Hong, Young-Soo (Korea Research Institute of Bioscience and Biotechnology)
  • Published : 2007.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

It was found that Shinorhizobium meliloti hemoprotein (SM) was more effective than Vitreoscilla hemoglobin (Vhb) in promoting secondary metabolites production when overexpressed in Streptomyces lividans TK24. The transformant with sm (sm-transformant) produced 2.7-times and 3-times larger amounts of actinorhodin than the vhb-transformant in solid culture and flask culture, respectively. In both solid and flask cultures, a larger amount of undecylprodigiocin was produced by the sm-transformant. It is considered that the overexpression of SM especially has activated the pentose phosphate pathway through oxidative stress, as evidenced by an increased NADPH production observed, and that it has promoted secondary metabolites biosynthesis.

Keywords

References

  1. Alexander, D. F. and P. T. Kallio. 2003. Bacterial hemoglobins and flavohemoglobins: Versatile proteins and their impact on microbiology and biotechnology. FEMS Microbiol. 27: 525-545 https://doi.org/10.1016/S0168-6445(03)00056-1
  2. Aydin, S. 2003. Menadione knocks out Vitreoscilla haemoglobin (Vhb): The current evidence for the role of Vhb in recombinant Escherichia coli. Biotechnol. Appl. Biochem. 38: 71-76 https://doi.org/10.1042/BA20030046
  3. Bollinger, C. J., J. E. Bailey, and P. T. Kallio. 2001. Novel hemoglobins to enhance microaerobic growth and substrate utilization in Escherichia coli. Biotechol. Prog. 17: 798-808 https://doi.org/10.1021/bp010091j
  4. Bruheim, P., M. Butler, and T. E. Ellingsen. 2002. A theoretical analysis of the biosynthesis of actinorhodin in a hyper-producing Streptomyces lividans strain cultivated on various carbon sources. Appl. Microbiol. Biotechnol. 58: 735-742 https://doi.org/10.1007/s00253-002-0969-9
  5. Butler, M. J., P. Bruheim, S. Jovetic, F. Marinelli, P. W. Postma, and M. J. Bibb. 2002. Engineering of primary carbon metabolism for improved antibiotic production in Streptomyces lividans. Appl. Environ. Microbiol. 68: 4731-4739 https://doi.org/10.1128/AEM.68.10.4731-4739.2002
  6. Cho, Y. H., E. J. Lee, and J. H. Roe. 2000. A developmentally regulated catalase required for proper differentiation and osmoprotection of Streptomyces coelicolor. Mol. Microbiol. 35: 150-160 https://doi.org/10.1046/j.1365-2958.2000.01685.x
  7. Choi, E.-Y., E. A. Oh, J.-H. Kim, D.-K. Kang, S. S. Kang, J. Chun, and S.-K. Hong. 2007. Distinct regulation of the sprC gene encoding Streptomyces griseus protease C from other chymotrypsin genes in Streptomyces griseus IFO13350. J. Microbiol. Biotechnol. 17: 81-88
  8. Choi, S.-S., J. H. Kim, J.-H. Kim, D.-K. Kang, S.-S. Kang, and S.-K. Hong. 2006. Functional anaylsis of sprD gene encoding Streptomyces griseus protease D (SGPD) in Streptomyces griseus. J. Microbiol. Biotechnol. 16: 312-317
  9. Cramm, R., R. A. Siddiqui, and B. Friedrich. 1994. Primary sequence and evidence for a physiological function of the flavohemoprotein of Alcaligenes eutrophus. J. Biol. Chem. 269: 7345-7354
  10. Crawford, M. J. and D. E. Goldberg. 1998. Regulation of the Salmonella typhimurium flavohemoglobin gene. A new pathway for bacterial gene expression in response to nitric oxide. J. Biol. Chem. 273: 34028-34032 https://doi.org/10.1074/jbc.273.51.34028
  11. Doumith, M., P. Weingarten, U. F. Wehmeier, K. Salah-bey, B. Benhamou, C. Capdevila, J.-M. Michel, W. Piepersberg, and M.-C. Raynal. 2000. Analysis of genes involved in 6- deoxyhexose biosynthesis and transfer in Saccharopolyspora erythraea. Mol. Gen. Genet. 264: 477-485 https://doi.org/10.1007/s004380000329
  12. Erenler, S. O., S. Gencer, H. Geckil, B. C. Stark, and D. A. Webster. 2004. Cloning and expression of the Vitreoscilla hemoglobin gene in Enterobacter aerogenes: Effect on cell growth and oxygen uptake. Appl. Biochem. Microbiol. 40: 241-248 https://doi.org/10.1023/B:ABIM.0000025945.53332.74
  13. Favey, S., G. Labesse, V. Vouille, and M. Boccara. 1995. Flavohaemoglobin HmpX: A new pathogenicity determinant in Erwinia chrysanthemi strain 3937. Microbiology 141: 863-871 https://doi.org/10.1099/13500872-141-4-863
  14. Geckil, H., S. Gencer, H. Kahraman, and S. O. Erenler. 2003. Genetic engineering of Enterobacter aerogenes with the Vitreoscilla hemoglobin gene: Cell growth, survival, and antioxidant enzyme status under oxidative stress. Res. Microbiol. 154: 425-31
  15. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166: 557-580 https://doi.org/10.1016/S0022-2836(83)80284-8
  16. Hopwood, D. A., M. J. Bibb, K. F. Chater, T. Kieser, C. J. Bruton, H. M. Kieser, D. J. Lydiate, D. P. Smith, and J. M. Ward. 1985. Genetic Manipulation of Streptomyces: A Laboratory Manual. The John Innes Foundation, Norwich, England
  17. Hu, Y., P. D. Butcher, J. A. Mangan, M. A. Rajandream, and A. R. Coates. 1999. Regulation of hmp gene transcription in Mycobacterium tuberculosis: Effects of oxygen limitation and nitrosative and oxidative stress. J. Bacteriol. 181: 3486-3493
  18. Joshi, M., S. Mande, and K. L. Dikshit. 1998. Hemoglobin biosynthesis in Vitreoscilla stercoraria DW: Cloning, expression, and characterization of a new homolog of a bacterial globin gene. Appl. Environ. Microbiol. 64: 2220-2280
  19. Kallio, P. T., D. J. Kim, P. S. Tsai, and J. E. Bailey. 1994. Intracellular expression of Vitreoscilla haemoglobin activates E. coli energy metabolism under oxygen-limited conditions. Eur. J. Biochem. 219: 201-208 https://doi.org/10.1111/j.1432-1033.1994.tb19931.x
  20. Khang, Y.-H., I.-W. Kim, Y.-R. Hah, J.-H. Hwangbo, and K.-K. Kang. 2003. Fusion protein of Vitreoscilla hemoglobin with D-amino acid oxidase enhances activity and stability of biocatalyst in the bioconversion process of cephalosporin C. Biotechnol. Bioeng. 82: 480-488 https://doi.org/10.1002/bit.10592
  21. Khleifat, K. and M. M. Abboud. 2003. Correlation between bacterial haemoglobin gene (vgb) and aeration: Their effect on the growth and a-amylase activity in transformed Enterobacter aerogenes. J. Appl. Microbiol. 94: 1052-1058 https://doi.org/10.1046/j.1365-2672.2003.01939.x
  22. Khosla, C., J. E. Curtis, J. DeModena, U. Rinas, and J. E. Bailey. 1990. Expression of intracellular hemoglobin improves protein synthesis in oxygen-limited Escherichia coli. Biotechnology 8: 49-53
  23. Khosla, C. and J. E. Bailey. 1988. Heterologous expression of a bacterial hemoglobin improves the growth properties of recombinant Escherichia coli. Nature 331: 633-635 https://doi.org/10.1038/331633a0
  24. Khosla, C. and J. E. Bailey. 1988. The Vitreoscilla hemoglobin gene: Molecular cloning, nucleotide sequence and genetic expression in Escherichia coli. Mol. Gen. Genet. 214: 158-161 https://doi.org/10.1007/BF00340195
  25. Kieser, T., M. J. Bibb, M. J. Buttner, K. F. Chater, and D. A. Hopwood. 2000. Practical Streptomyces Genetics. John Innes Foundation, Norwich
  26. Kim, C.-Y., H.-J. Park, and E.-S. Kim. 2006. Functional dissection of sigma-like domain in antibiotic regulatory gene, afsR2, in Streptomyces lividans. J. Microbiol. Biotechnol. 16: 1477-1480
  27. LaCelle, M., M. Kumano, K. Kurita, K. Yamane, P. Zuber, and M. M. Nakano. 1996. Oxygen-controlled regulation of the flavohemoglobin gene in Bacillus subtilis. J. Bacteriol. 178: 3803-380 https://doi.org/10.1128/jb.178.13.3803-3808.1996
  28. 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
  29. Magnolo, S. K., D. L. Leenutaphong, J. A. DeModena, J. E. Curtis, J. E. Bailey, J. L. Galazzo, and D. E. Hughes. 1991. Actinorhodin production by Streptomyces coelicolor and growth of Streptomyces lividans are improved by the expression of a bacterial hemoglobin. Biotechnology 9: 473-476 https://doi.org/10.1038/nbt0591-473
  30. Pandolfi, P. P., F. Sonati, R. Rivi, P. Mason, F. Grosveld, and L. Luzzatto. 1995. Targeted disruption of the housekeeping gene encoding glucose-6-phosphate dehydrogenase (G6PD): G6PD is dispensable for pentose synthesis but essential for defense against oxidative stress. EMBO J. 14: 5209-5215
  31. Sambrook, J. and D. W. Russell. 2001. Molecular Cloning; 3rd Ed., Cold Spring Harbor, New York, U.S.A
  32. Tsai, P. S., V. Hatzimanikatis, and J. E. Bailey. 1996. Effect of Vitreoscilla hemoglobin dosage on microaerobic Escherichia coli carbon and energy metabolism. Biotechnol. Bioeng. 49: 139-150 https://doi.org/10.1002/(SICI)1097-0290(19960120)49:2<139::AID-BIT3>3.0.CO;2-R
  33. Vasudevan, S. G., W. L. Armarego, D. C. Shaw, P. E. Lilley, N. E. Dixon, and R. K. Poole. 1991. Isolation and nucleotide sequence of the hmp gene that encodes a haemoglobin-like protein in Escherichia coli K-12. Mol. Gen. Genet. 226: 49-58 https://doi.org/10.1007/BF00273586
  34. Yang, H.-Y., S.-S. Choi, W.-J. Chi, J.-H. Kim, D.-K. Kang, J. Chun, S.-S. Kang, and S.-K. Hong. 2005. Identification of the sprU gene encoding an additional sprT homologous trypsin-type protease in Streptomyces griseus. J. Microbiol. Biotechnol. 15: 1125-1129