Advertisement

Biotechnology and Bioprocess Engineering

, Volume 24, Issue 2, pp 366–374 | Cite as

Enzymatic and Microbial Biosynthesis of Novel Violacein Glycosides with Enhanced Water Solubility and Improved Anti-nematode Activity

  • Yu Jeong Lee
  • Puspalata Bashyal
  • Ramesh Prasad PandeyEmail author
  • Jae Kyung SohngEmail author
Research Paper
  • 4 Downloads

Abstract

Violacein, a microbial metabolite with multiple applications, was produced in Escherichia coli, and glycodiversified using purified Bacillus glycosyltransferase (YjiC) enzyme with glucose, galactose, and N-acetylglucosamine, to generate five novel O-glycoside derivatives. One of the glucose-conjugated derivatives, violacein 5′-O-glucoside, was produced from engineered E. coli harboring entire violacein biosynthetic gene cluster (VioABCDE) and a glycosyltransferase gene (yjiC) in tryptophan supplemented TB medium. Violacein 5′-O-glucoside gained anti-nematodal activity against pine wood nematode Bursaphelenchus xylophilus, a causative agent of pine wilt disease. Moreover, the conjugation of sugar moieties in violacein enhanced water solubility. Violacein 5′-O-diglucoside was completely retained in water fraction, while its aglycone parent molecule was completely insoluble in water.

Keywords

violacein glycodiversification anti-nematode novel glycosides 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgment

This work was supported by a grant from the Next-Generation BioGreen 21 Program (SSAC, grant#: PJ013137), Rural Development Administration, Republic of Korea.

Supplementary material

12257_2018_466_MOESM1_ESM.pdf (1.8 mb)
Supplementary material, approximately 1.78 MB.

References

  1. 1.
    Tobie, W. C. (1934) The pigment of Bacillus violaceus I. The production, extraction, and purification of violacein. J. Bacteriol. 29: 223–227.Google Scholar
  2. 2.
    Nakamura, Y., C. Asada, and T. Sawada (2003) Production of antibacterial violet pigment by psychrotropic bacterium RT102 strain. Biotechnol. Bioprocess Eng. 8: 37–40.CrossRefGoogle Scholar
  3. 3.
    Laatsch, H. and R. H. Thomson (1984) Spectroscopic properties of violacein and related compound: crystal structure of tetramethylviolacein. J. Chem. Soc. Perkin. Trans. II 8: 1331–1339.CrossRefGoogle Scholar
  4. 4.
    Tan, T. L., F. P. Montforts, and D. Meyer (2002) Microbiological method for the biosynthesis of natural blue-violet colorants violacein and desoxyviolacein. PCT Int. Appl. WO 2002050299 A2Google Scholar
  5. 5.
    Choi, S. Y., S. Kim, S. Lyuck, S. B. Kim, and R. J. Mitchell (2015) High-level production of violacein by the newly isolated Duganella violaceinigra str. NI28 and its impact on Staphylococcus aureus. Sci. Rep. 5: 15598.CrossRefGoogle Scholar
  6. 6.
    Shirata, A., T. Tsukamoto, H. Yasui, T. Hata, S. Hayasaka, A. Kojima, and H. Kato (2000) Isolation of bacteria producing bluish-purple pigment and use for dyeing. Japan Agric. Res. Quart. 34: 131–140.Google Scholar
  7. 7.
    Durán, M., A. N. Ponezi, A. Faljoni-Alario, M. F. S. Teixeira, G Z. Justo, and N. Durán (2012) Potential applications of violacein: a microbial pigment. Med. Chem. Res. 21: 1524–1532.CrossRefGoogle Scholar
  8. 8.
    Ahmetagic, A. and J. M. Pemberton (2010) Stable high level expression of the violacein indolocarbazole anti-tumour gene cluster and the Streptomyces lividans amyA gene in E. coli K12. Plasmid 63: 79–85.CrossRefGoogle Scholar
  9. 9.
    Fang, M. Y., C. Zhang, S. Yang, J. Y. Cui, P. X. Jiang, K. Lou, M. Wachi, and X. H. Xing (2015) High crude violacein production from glucose by Escherichia coli engineered with interactive control of tryptophan pathway and violacein biosynthetic pathway. Microb. Cell Fact. 14: 8.CrossRefGoogle Scholar
  10. 10.
    Jones, J. A., V. R. Vernacchio, D. M. Lachance, M. Lebovich, L. Fu, A. N. Shirke, V. L. Schultz, B. Cress, R. J. Linhardt, and M. A. Koffas (2015) ePathOptimize: A combinatorial approach for transcriptional balancing of metabolic pathways. Sci. Rep. 5: 11301.CrossRefGoogle Scholar
  11. 11.
    Takii, T., S. Hamasaki, K. Hirano, C. Abe, and K. Onozaki (2005) Simple fibroblast-based assay to test the pyrazinamide susceptibility of Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 49: 804–807.CrossRefGoogle Scholar
  12. 12.
    Shirata, A., T. Tsukamoto, H. Yasui, H. Kato, S. Hayasaka, and A. Kojima (1997) Production of bluish-purple pigments by Janthinobacterium lividum isolated from the raw silk and dyeing with them. Nippon Sanshigaku Zasshi 66: 377–385.Google Scholar
  13. 13.
    Melo, P. S., S. S. Maria, B. C. Vidal, M. Haun, and N. Durán (2000) Violacein cytotoxicity and induction of apoptosis in V79 cells. In Vitro Cell Dev. Biol. Anim. 36: 539–543.CrossRefGoogle Scholar
  14. 14.
    Bromberg, N., J. L. Dreyfuss, C. V. Regatieri, M. V. Palladino, N. Durán, H. B. Nader, M. Haun, and G. Z. Justo (2010) Growth inhibition and proapoptotic activity of violacein in Ehrlich ascites tumor. Chem. Biol. Interact. 186: 43–52.CrossRefGoogle Scholar
  15. 15.
    Durán, N. and C. F. M. Menck (2001) Chromobacterium violaceum: A review of pharmacological and industrial perspectives. Crit. Rev. Microbiol. 27: 201–222.CrossRefGoogle Scholar
  16. 16.
    Costa, F. T. M., G. Z. Justo, N. Durán, P. A. Nogueira, and S. C. P. Lopes (2005) The use of violacein in its free and encapsulated form in polymeric systems against malaria. Brazilian Patent PIBr 056399-0.Google Scholar
  17. 17.
    Lopes, S. C. P., Y. C. Blanco, G. Z. Justo, P. A. Nogueira, F. L. S. Rodrigues, U. Goelnitz, G. Wunderlich, G. Facchini, M. Brocchi, N. Durán, and F. T. M. Costa (2009) Violacein extracted from Chromobacterium violaceum inhibits Plasmodium growth in vitro and in vivo. Antimocrob. Agents Chemother. 53: 2149–2152.CrossRefGoogle Scholar
  18. 18.
    Matz, C., P. Deines, J. Boenigk, H. Arndt, L. Eberl, S. Kjellberg, and K. Jurgens (2004) Impact of violacein-producing bacteria on survival and feeding of bacterivorous nanoflagellates. Appl. Environ. Microbiol. 70: 1593–1599.CrossRefGoogle Scholar
  19. 19.
    Andrighetti-Frohner, C. R., R. V. Antonio, T. B. Creczynski-Pasa, C. R. M. Barandi, and C. M. O. Simóes (2003) Cytotoxicity and potential antiviral evaluation of violacein produced by Chromobacterium violaceum. Mem. Inst. Oswaldo Cruz. 98: 834–848.CrossRefGoogle Scholar
  20. 20.
    Duran, N., G. Z. Justo, P. S. Melo, D. Jr. Martins, and L. Cordi (2007) Violacein: properties and biological activities. Biotechnol. Appl. Biochem. 48: 127–133.CrossRefGoogle Scholar
  21. 21.
    Antonisamy, P., P. Kannan, and S. Ignacimuthu (2009) Anti-diarrhoeal and ulcer-protective effects of violacein isolated from Chromobacterium violaceum in Wistar rats. Fundam. Clin. Pharmacol. 23: 483–490.CrossRefGoogle Scholar
  22. 22.
    Antonisamy, P. and S. Ignacimuthu (2010) Immunomodulatory, analgesic and antipyretic effects of violacein isolated from Chromobacterium violaceum. Phytomedicine 17: 300–304.CrossRefGoogle Scholar
  23. 23.
    Baek, S. H., H. S. Kang, I. H. Jang, J. S. Lee, S. Y. Kim, J. H. Baek, J. G. Kang, and J. M. Ahn (2007) Insecticide and fungicide containing violacein, and their preparation method. Repub. Korean Kongkae Taeho Kongbo KR 2007088150 AGoogle Scholar
  24. 24.
    Melo, P. S., G. Z. Justo, M. B. de Azevedo, N. Durán, and M. Haun (2003) Violacein and its beta-cyclodextrin complexes induce apoptosis and differentiation in HL60 cells. Toxicology 186: 217–225.CrossRefGoogle Scholar
  25. 25.
    Pandey, R.P., S. Malla, D. Simkhada, B. G. Kim, and J. K. Sohng (2013) Production of 3-O-xylosyl quercetin in Escherichia coli. Appl. Microbiol. Biotechnol. 97: 1889–1901.CrossRefGoogle Scholar
  26. 26.
    Parajuli, P., R. P. Pandey, N. T. Trang, A. K. Chaudhary, and J. K. Sohng (2015) Synthetic sugar cassettes for the efficient production of flavonol glycosides in Escherichia coli. Microb. Cell Fact. 14: 76.CrossRefGoogle Scholar
  27. 27.
    Balibar, C. J. and C. T. Walsh (2006) In vitro biosynthesis of violacein from L-tryptophan by the enzymes VioA-E from Chromobacterium violaceum. Biochemistry 45: 15444–15457.CrossRefGoogle Scholar
  28. 28.
    Hoshino, T. and N. Ogasawara (1990) Biosynthesis of violacein: evidence for the intermediacy of 5-hydroxy-l-tryptophan and the structure of a new pigment, oxyviolacein, produced by the metabolism of 5-hydroxytryptophan. Agric. Bioi. Chern. 54: 2339–2346.Google Scholar
  29. 29.
    Choi, H. Y., N. Van Minh, J. M. Choi, J. Y. Hwangm, S. T. Seo, S. K. Lee, and W. G. Kim (2018) Enzymatic synthesis of avermectin B1a glycosides for the effective prevention of the pine wood nematode Bursaphelenchus xylophilus. Appl. Microbiol. Biotechnol. 102: 2155–2165.CrossRefGoogle Scholar
  30. 30.
    Toth, A. (2011) Bursaphelenchus xylophilus, the pinewood nematode: its significance and a historical review. Acta Biol. Szeged. 55: 213–217.Google Scholar
  31. 31.
    Futai, K. (2013) Pine wood nematode, Bursaphelenchus xylophilus. Annu. Rev. Phytopathol. 51: 61–83.CrossRefGoogle Scholar
  32. 32.
    Mota, M. M. and P. R. Vieira (2008) Pine Wilt Disease: A Worldwide Threat to Forest Ecosystems Springer Verlag GmbH, Heidelberg, Germany.CrossRefGoogle Scholar
  33. 33.
    Huang, G., M. Lv, J. Hu, K. Huang, and H. Xu (2016) Glycosylation and activities of natural products. Mini Rev. Med. Chem. 16: 1013–1016.CrossRefGoogle Scholar
  34. 34.
    Weymouth-Wilson, A. C. (1997) The role of carbohydrates in biologically active natural products. Nat. Prod. Rep. 14: 99–110.CrossRefGoogle Scholar
  35. 35.
    Elshahawi, S. I., K. A. Shaaban, M. K. Kharel, and J. S. Thorson (2015) A comprehensive review of glycosylated bacterial natural products. Chem. Soc. Rev. 44: 7591–7697.CrossRefGoogle Scholar

Copyright information

© The Korean Society for Biotechnology and Bioengineering and Springer 2019

Authors and Affiliations

  1. 1.Department of Life Science and Biochemical EngineeringSun Moon UniversityAsanKorea
  2. 2.Department of Pharmaceutical Engineering and BiotechnologySun Moon UniversityAsanKorea

Personalised recommendations