Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2017, Article ID 5373262, 13 pages
https://doi.org/10.1155/2017/5373262
Research Article

Significance of Heavy-Ion Beam Irradiation-Induced Avermectin B1a Production by Engineered Streptomyces avermitilis

1Institute of Modern Physics, Chinese Academy of Sciences, 509 Nanchang Rd., Lanzhou, Gansu 730000, China
2Lanzhou University, 222 South Tianshui Road, Lanzhou, Gansu 730000, China
3Institute of Veterinary Drug Quality Inspection of Shandong Province, Jinan 250022, China

Correspondence should be addressed to Shu-Yang Wang; nc.ca.sacpmi@ysgnaw

Received 30 June 2016; Revised 9 October 2016; Accepted 23 October 2016; Published 24 January 2017

Academic Editor: Somboon Tanasupawat

Copyright © 2017 Shu-Yang Wang 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. W. Burg, B. M. Miller, E. E. Baker et al., “Avermectins, new family of potent anthelmintic agents: producing organism and fermentation,” Antimicrobial Agents and Chemotherapy, vol. 15, no. 3, pp. 361–367, 1979. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Bum Kim and M. Goodfellow, “Streptomyces avermitilis sp. nov., nom. rev., a taxonomic home for the avermectin-producing streptomycetes,” International Journal of Systematic and Evolutionary Microbiology, vol. 52, no. 6, pp. 2011–2014, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. S. Y. Lee, D. Y. Lee, and T. Y. Kim, “Systems biotechnology for strain improvement,” Trends in Biotechnology, vol. 23, no. 7, pp. 349–358, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. A. B. A. Boxall, L. A. Fogg, P. Kay, P. A. Blackwell, E. J. Pemberton, and A. Croxford, “Prioritisation of veterinary medicines in the UK environment,” Toxicology Letters, vol. 142, no. 3, pp. 207–218, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. A. B. A. Boxall, D. W. Kolpin, B. Halling-Sørensen, and J. Tolls, “Are veterinary medicines causing environmental risks?” Environmental Science and Technology, vol. 37, no. 15, pp. 286A–294A, 2003. View at Google Scholar · View at Scopus
  6. K. D. Floate, K. G. Wardhaugh, A. B. A. Boxall, and T. N. Sherratt, “Fecal residues of veterinary parasiticides: nontarget effects in the pasture environment,” Annual Review of Entomology, vol. 50, pp. 153–179, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. D. Witt and E. Stackebrandt, “Unification of the genera Streptoverticillium and Streptomyces, and amendation of Streptomyces Waksman and Henrici 1943, 339(AL),” Systematic and Applied Microbiology, vol. 13, no. 4, pp. 361–371, 1990. View at Publisher · View at Google Scholar · View at Scopus
  8. Y. Lin, H. M. Kieser, D. A. Hopwood, and C. W. Chen, “The chromosomal DNA of Streptomyces lividans 66 is linear,” Molecular Microbiology, vol. 10, no. 5, pp. 923–933, 1993. View at Publisher · View at Google Scholar · View at Scopus
  9. 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
  10. W. Wang, X. Li, Y. Li, S. Li, K. Fan, and K. Yang, “A genetic biosensor for identification of transcriptional repressors of target promoters,” Scientific Reports, vol. 5, Article ID 15887, 2015. View at Publisher · View at Google Scholar · View at Scopus
  11. H.-W. Yen and H.-P. Hsiao, “Effects of dissolved oxygen level on rapamycin production by pellet-form of Streptomyces hygroscopicus,” Journal of Bioscience and Bioengineering, vol. 116, no. 3, pp. 366–370, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. N. Mehmood, E. Olmos, J.-L. Goergen et al., “Decoupling of oxygen transfer and power dissipation for the study of the production of pristinamycins by Streptomyces pristinaespiralis in shaking flasks,” Biochemical Engineering Journal, vol. 68, pp. 25–33, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. R. A. Gamboa-Suasnavart, N. A. Valdez-Cruz, L. E. Cordova-Dávalos et al., “The O-mannosylation and production of recombinant APA (45/47 KDa) protein from Mycobacterium tuberculosis in Streptomyces lividans is affected by culture conditions in shake flasks,” Microbial Cell Factories, vol. 10, article 110, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. X. Xia, S. Lin, X.-X. Xia, F.-S. Cong, and J.-J. Zhong, “Significance of agitation-induced shear stress on mycelium morphology and lavendamycin production by engineered Streptomyces flocculus,” Applied Microbiology and Biotechnology, vol. 98, no. 10, pp. 4399–4407, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. C. Bandaiphet and P. Prasertsan, “Effect of aeration and agitation rates and scale-up on oxygen transfer coefficient, kLa in exopolysaccharide production from Enterobacter cloacae WD7,” Carbohydrate Polymers, vol. 66, no. 2, pp. 216–228, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. L. C. Fritz, C. C. Wang, and A. Gorio, “Avermectin B1a irreversibly blocks postsynaptic potentials at the lobster neuromuscular junction by reducing muscle membrane resistance,” Proceedings of the National Academy of Sciences of the United States of America, vol. 76, no. 4, pp. 2062–2066, 1979. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Zhang, C. Albermann, X. Fu, and J. S. Thorson, “The in vitro characterization of the iterative avermectin glycosyltransferase AveBI reveals reaction reversibility and sugar nucleotide flexibility,” Journal of the American Chemical Society, vol. 128, no. 51, pp. 16420–16421, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. Z. Xu and P. Cen, “Stimulation of avermectin B1a biosynthesis in Streptomyces avermilitis by feeding glucose and propionate,” Biotechnology Letters, vol. 21, no. 1, pp. 91–95, 1999. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Kitani, K. T. Miyamoto, S. Takamatsu et al., “Avenolide, a Streptomyces hormone controlling antibiotic production in Streptomyces avermitilis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 39, pp. 16410–16415, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Awasthi, M. Razzak, R. Al-Kassas, J. Harvey, and S. Garg, “An overview on chemical derivatization and stability aspects of selected avermectin derivatives,” Chemical and Pharmaceutical Bulletin, vol. 60, no. 8, pp. 931–944, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. C. Pfefferle, U. Theobald, H. Gürtler, and H.-P. Fiedler, “Improved secondary metabolite production in the genus Streptosporangium by optimization of the fermentation conditions,” Journal of Biotechnology, vol. 80, no. 2, pp. 135–142, 2000. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Inoue, Y. Yoshimi, T. Hino, and H. Oka, “Simultaneous determination of avermectins in bovine tissues by LC-MS/MS,” Journal of Separation Science, vol. 32, no. 21, pp. 3596–3602, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Ishida, R. Haga, N. Nishimura, H. Matuzaki, and R. Nakano, “High cell density suspension culture of mammalian anchorage independent cells: oxygen transfer by gas sparging and defoaming with a hydrophobic net,” Cytotechnology, vol. 4, no. 3, pp. 215–225, 1990. View at Publisher · View at Google Scholar · View at Scopus
  24. M. S. Felipe, “Transcriptional profiles of the human pathogenic fungus Paracoccidioides brasiliensis in mycelium and yeast cells,” Journal of Biological Chemistry, vol. 280, no. 26, pp. 24706–24714, 2005. View at Publisher · View at Google Scholar
  25. F. B. Abeles, P. W. Morgan, and M. E. Saltveit Jr., Ethylene in Plant Biology, Academic Press, 2012.
  26. P. Gervais and P. Molin, “The role of water in solid-state fermentation,” Biochemical Engineering Journal, vol. 13, no. 2-3, pp. 85–101, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. F. Garcia-Ochoa and E. Gomez, “Bioreactor scale-up and oxygen transfer rate in microbial processes: an overview,” Biotechnology Advances, vol. 27, no. 2, pp. 153–176, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Hortsch, A. Stratmann, and D. Weuster-Botz, “New milliliter-scale stirred tank bioreactors for the cultivation of mycelium forming microorganisms,” Biotechnology and Bioengineering, vol. 106, no. 3, pp. 443–451, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Lei, Y. Zhao, R. Cheng et al., “Fluorescence emission from CsI(Tl) crystal induced by high-energy carbon ions,” Optical Materials, vol. 35, no. 6, pp. 1179–1183, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. X. Zhou, J.-R. Xie, L. Tao et al., “The effect of microdosimetric 12C6+ heavy ion irradiation and Mg2+ on canthaxanthin production in a novel strain of Dietzia natronolimnaea,” BMC Microbiology, vol. 13, no. 1, article no. 213, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. S.-Y. Wang, B.-L. Jiang, X. Zhou et al., “Study of a high-yield cellulase system created by heavy-ion irradiation-induced mutagenesis of Aspergillus Niger and mixed fermentation with Trichoderma reesei,” PLoS ONE, vol. 10, no. 12, Article ID e0144233, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Jun, T. Kieselbach, and L. J. Jönsson, “Comparative proteome analysis of Saccharomyces cerevisiae: a global overview of in vivo targets of the yeast activator protein 1,” BMC Genomics, vol. 13, no. 1, article 230, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. V. Neuhoff, N. Arold, D. Taube, and W. Ehrhardt, “Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250,” Electrophoresis, vol. 9, no. 6, pp. 255–262, 1988. View at Publisher · View at Google Scholar · View at Scopus
  34. S.-J. Wang and J.-J. Zhong, “A novel centrifugal impeller bioreactor. II. Oxygen transfer and power consumption,” Biotechnology and Bioengineering, vol. 51, no. 5, pp. 520–527, 1996. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Kato, S. Kawzao, and Y. Soh, “Viscosity of the broth of tobacco cells in suspension culture: biomass production of tobacco cells (Part IV),” Journal of Fermentation Technology, vol. 56, no. 3, pp. 224–228, 1978. View at Google Scholar
  36. X. Zhang, Z. Chen, M. Li, Y. Wen, Y. Song, and J. Li, “Construction of ivermectin producer by domain swaps of avermectin polyketide synthase in Streptomyces avermitilis,” Applied Microbiology and Biotechnology, vol. 72, no. 5, pp. 986–994, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. L.-Y. Wang, Z.-L. Huang, G. Li et al., “Novel mutation breeding method for Streptomyces avermitilis using an atmospheric pressure glow discharge plasma,” Journal of Applied Microbiology, vol. 108, no. 3, pp. 851–858, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Omura, H. Ikeda, J. Ishikawa et al., “Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 21, pp. 12215–12220, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Jenke-Kodama, T. Börner, and E. Dittmann, “Natural biocombinatorics in the polyketide synthase genes of the actinobacterium Streptomyces avermitilis,” PLoS Computational Biology, vol. 2, no. 10, article e132, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. X. Zhou, X.-H. Lu, X.-H. Li et al., “Radiation induces acid tolerance of Clostridium tyrobutyricum and enhances bioproduction of butyric acid through a metabolic switch,” Biotechnology for Biofuels, vol. 7, no. 1, article 22, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. C.-X. Di, L. Han, H. Zhang et al., “Diallyl disulfide attenuated carbon ion irradiation-induced apoptosis in mouse testis through changing the ratio of Tap73/Np73 via mitochondrial pathway,” Scientific Reports, vol. 5, Article ID 16020, 2015. View at Publisher · View at Google Scholar · View at Scopus
  42. X. Jin, F. Li, X. Zheng et al., “Carbon ions induce autophagy effectively through stimulating the unfolded protein response and subsequent inhibiting Akt phosphorylation in tumor cells,” Scientific Reports, vol. 5, Article ID 13815, 2015. View at Publisher · View at Google Scholar · View at Scopus
  43. T. Kanai, M. Endo, S. Minohara et al., “Biophysical characteristics of HIMAC clinical irradiation system for heavy-ion radiation therapy,” International Journal of Radiation Oncology Biology Physics, vol. 44, no. 1, pp. 201–210, 1999. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Kramer and M. Scholz, “Treatment planning for heavy-ion radiotherapy: calculation and optimization of biologically effective dose,” Physics in Medicine and Biology, vol. 45, no. 11, pp. 3319–3330, 2000. View at Publisher · View at Google Scholar · View at Scopus
  45. C. A. Tobias, E. A. Blakely, E. L. Alpen et al., “Molecular and cellular radiobiology of heavy ions,” International Journal of Radiation Oncology, Biology, Physics, vol. 8, no. 12, pp. 2109–2120, 1982. View at Publisher · View at Google Scholar · View at Scopus
  46. D. T. Goodhead, R. J. Munson, J. Thacker, and R. Cox, “Mutation and inactivation of cultured mammalian cells exposed to beams of accelerated heavy ions IV. Biophysical interpretation,” International Journal of Radiation Biology, vol. 37, no. 2, pp. 135–167, 1980. View at Publisher · View at Google Scholar · View at Scopus
  47. J.-P. Pouget and S. J. Mather, “General aspects of the cellular response to low- and high-LET radiation,” European Journal of Nuclear Medicine, vol. 28, no. 4, pp. 541–561, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. K. Stutzman-Engwall, S. Conlon, R. Fedechko et al., “Semi-synthetic DNA shuffling of aveC leads to improved industrial scale production of doramectin by Streptomyces avermitilis,” Metabolic Engineering, vol. 7, no. 1, pp. 27–37, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Gaisser, L. Kellenberger, A. L. Kaja et al., “Direct production of ivermectin-like drugs after domain exchange in the avermectin polyketide synthase of Streptomyces avermitilis ATCC31272,” Organic and Biomolecular Chemistry, vol. 1, no. 16, pp. 2840–2847, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. T. Hui and Z. Li Ping, “Site-directed mutagenesis of Streptomyces avermitilis aveD gene,” Agricultural Science & Technology—Hunan, vol. 12, no. 10, pp. 1424–1426, 2011. View at Google Scholar
  51. M. Papagianni, “Fungal morphology and metabolite production in submerged mycelial processes,” Biotechnology Advances, vol. 22, no. 3, pp. 189–259, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. F. J. Brockman, T. L. Kieft, J. K. Fredrickson et al., “Microbiology of vadose zone paleosols in south-central Washington State,” Microbial Ecology, vol. 23, no. 3, pp. 279–301, 1992. View at Publisher · View at Google Scholar · View at Scopus
  53. J. I. Prosser and A. J. Tough, “Growth mechanisms and growth kinetics of filamentous microorganisms,” Critical Reviews in Biotechnology, vol. 10, no. 4, pp. 253–274, 1991. View at Publisher · View at Google Scholar · View at Scopus
  54. R. Krull, T. Wucherpfennig, M. E. Esfandabadi et al., “Characterization and control of fungal morphology for improved production performance in biotechnology,” Journal of Biotechnology, vol. 163, no. 2, pp. 112–123, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. C. Bendig and D. Weuster-Botz, “Reaction engineering analysis of cellulase production with Trichoderma reesei RUT-C30 with intermittent substrate supply,” Bioprocess and Biosystems Engineering, vol. 36, no. 7, pp. 893–900, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. E. Olmos, N. Mehmood, L. H. Husein, J.-L. Goergen, M. Fick, and S. Delaunay, “Effects of bioreactor hydrodynamics on the physiology of Streptomyces,” Bioprocess and Biosystems Engineering, vol. 36, no. 3, pp. 259–272, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. E. Galindo, C. P. Larralde-Corona, T. Brito et al., “Development of advanced image analysis techniques for the in situ characterization of multiphase dispersions occurring in bioreactors,” Journal of Biotechnology, vol. 116, no. 3, pp. 261–270, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. E. Jonsbu, M. McIntyre, and J. Nielsen, “The influence of carbon sources and morphology on nystatin production by Streptomyces noursei,” Journal of Biotechnology, vol. 95, no. 2, pp. 133–144, 2002. View at Publisher · View at Google Scholar · View at Scopus