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Mechanism Analysis of Effect of Oxygen on Molecular Weight of Hyaluronic Acid Produced by Streptococcus zooepidemicus

  • Duan, Xu-Jie (State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology) ;
  • Niu, Hong-Xing (State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology) ;
  • Tan, Wen-Song (State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology) ;
  • Zhang, Xu (State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology)
  • Received : 2008.01.28
  • Accepted : 2008.07.16
  • Published : 2009.03.31

Abstract

Dissolved oxygen (DO) has a significant effect on the molecular weight of hyaluronic acid (HA) during the fermentation of Streptococcus zooepidemicus. Therefore, to further investigate the effect of DO on the yield and molecular weight of HA, this study compared the metabolic flux distribution of S. zooepidemicus under aerobic conditions at various DO levels. The metabolic flux analysis demonstrated that the HA synthesis pathway, considered a dependent network, was little affected by the DO level. In contrast, the fluxes of lactate and acetate were greatly influenced, and more ATP was generated concomitant with acetate at a high DO level. Furthermore, the has gene expression and HA synthase activity were both repressed under anaerobic conditions, yet not obviously affected under aerobic conditions at various DO levels. Therefore, it was concluded that the HA molecular weight would seem to depend on the concomitant effect of the generation of ATP and reactive oxygen species. It is expected that this work will contribute to a better understanding of the effect of the DO level on the mechanism of the elongation of HA chains.

Keywords

References

  1. Armstrong, D. C. and M. R. Johns. 1997. Culture conditions affect the molecular weight properties of hyaluronic acid produced by Streptococcus zooepidemicus. Appl. Environ. Microbiol. 63:2759-2764
  2. Bai, D. M., X. M. Zhao, X. G. Li, and S. M. Xu. 2004. Strain improvement of Rhizopus oryzae for over-production $of_L$(+)-lactic acid and metabolic flux analysis of mutants. Biochem. Eng. J. 18: 41-48 https://doi.org/10.1016/S1369-703X(03)00126-8
  3. Bitter, T. and H. M. Muir. 1962. A modified uronic acid carbazole reaction. Anal. Biochem. 4: 330-333 https://doi.org/10.1016/0003-2697(62)90095-7
  4. Bunn, H. F. and R. O. Poyton. 1996. Oxygen sensing and molecular adaptation to hypoxia. Physiol. Rev. 76: 839-885 https://doi.org/10.1152/physrev.1996.76.3.839
  5. Crater, D. L. and I. van de Rijn. 1995. Hyaluronic acid synthesis operon (has) expression in group A Streptococci. J. Biol. Chem. 270: 18452-18458 https://doi.org/10.1074/jbc.270.31.18452
  6. Duan, X.-J., L. Yang, X. Zhang, and W.-S. Tan. 2008. Effect of oxygen and shear stress on molecular weight of hyaluronic acid produced by Streptococcus zooepidemicus. J. Microbiol. Biotechnol. 18: 718-724
  7. Fong Chong, B., L. M. Blank, R. McLaughlin, and L. K. Nielsen. 2005. Microbial hyaluronic acid production. Appl. Microbiol. Biotechnol. 66: 341-351 https://doi.org/10.1007/s00253-004-1774-4
  8. Fong Chong, B. and L. K. Nielsen. 2003. Aerobic cultivation of Streptococcus zooepidemicus and the role of NADH oxidase. Biochem. Eng. J. 16: 153-162 https://doi.org/10.1016/S1369-703X(03)00031-7
  9. Fong Chong, B. and L. K. Nielsen. 2003. Amplifying the cellular reduction potential of Streptococcus zooepidemicus. J. Biotechnol. 100: 33-41 https://doi.org/10.1016/S0168-1656(02)00239-0
  10. Gao, H. J., G. C. Du, and J. Chen. 2006. Analysis of metabolic fluxes for hyaluronic acid (HA) production by Streptococcus zooepidemicus. World J. Microbiol. Biotechnol. 22: 399-408 https://doi.org/10.1007/s11274-005-9047-7
  11. Hasegawa, S., M. Nagatsuru, M. Shibutani, S. Yamamoto, and S. Hasebe. 1999. Productivity of concentrated hyaluronic acid using a maxblend${\circledR}$ fermentor. J. Biosci. Bioeng. 88: 68-71 https://doi.org/10.1016/S1389-1723(99)80178-9
  12. Huang, W-C., S.-J. Chen, and T.-L. Chen. 2006. The role of dissolved oxygen and function of agitation in hyaluronic acid fermentation. Biochem. Eng. J. 32: 239-243 https://doi.org/10.1016/j.bej.2006.10.011
  13. Kang, S.-W., E. R. Cho, and B.-S. Kim. 2005. PLGA microspheres in hyaluronic acid gel as a potential bulking agent for urologic and dermatologic injection therapies. J. Microbiol. Biotechnol. 15: 510-518
  14. Kietzmann, T., J. Fandrey, and H. Acker. 2000. Oxygen radicals as messengers in oxygen-dependent gene expression. News Physiol. Sci. 15: 202-208
  15. Kim, J.-H., S.-J. Yoo, D.-K. Oh, Y.-G. Kweon, D.-W. Park, C.-H. Lee, and G.-H. Gil. 1996. Selection of a Streptococcus equimutant and optimization of culture conditions for the production of molecular weight hyaluronic acid. Enzyme Microb. Technol. 19: 440-445 https://doi.org/10.1016/S0141-0229(96)00019-1
  16. Kim, S.-J., S.-Y. Park, and C.-W. Kim. 2006. A novel approach to the production of hyaluronic by Streptococcus zooepidemicus. J. Microbiol. Biotechnol. 16: 1849-1855
  17. Kim, T. Y. and S. Y. Lee. 2006. Accurate metabolic flux analysis through data reconciliation of isotope balance-based data. J. Microbiol. Biotechnol. 16: 1139-1143
  18. Kogan, G., L. $\check{s}$olt$\acute{e}$s, R. Stern, and P. Gemeiner. 2007. Hyaluronic acid: A natural biopolymer with a broad range of biomedical and industrial applications. Biotechnol. Lett. 29: 17-25 https://doi.org/10.1007/s10529-006-9219-z
  19. Laurent, T. C., M. Ryan, and A. Pietruszkiewicz. 1960. Fraction of hyaluronic acid. The polydispersity of hyaluronic acid from the bovine vitreous body. Biochim. Biophys. Acta 42: 476-485 https://doi.org/10.1016/0006-3002(60)90826-X
  20. Liu, H. J., Q. Li, D. H. Liu, and J. J. Zhong. 2006. Impact of hyperosmotic condition on cell physiology and metabolic flux distribution of Candida krusei. Biochem. Eng. J. 28: 92-98 https://doi.org/10.1016/j.bej.2005.08.038
  21. Miller, G. L. 1959. Use of dinitrosalicylic reagent for determination of reducing sugars. Anal. Chem. 31: 426-428 https://doi.org/10.1021/ac60147a030
  22. Nordkvist, M., N. B. Siemsen Jensen, and J. Villadsen. 2003. Glucose metabolism in Lactococcus lactis MG1363 under different aeration conditions: Requirement of acetate to sustain growth under microaerobic conditions. Appl. Environ. Microbiol. 69: 3462-3468 https://doi.org/10.1128/AEM.69.6.3462-3468.2003
  23. Praest, B. M., H. Greiling, and R$\ddot{u}$diger. Kock. 1997. Effects of oxygenderived free radicals on the molecular weight and the polydispersity of hyaluronan solutions. Carbohydr. Res. 303: 153-157 https://doi.org/10.1016/S0008-6215(97)00162-6
  24. Presti, D. and J. E. Scott. 1994. Hyaluronan-mediated protective effect against cell damage caused by enzymatically produced hydroxyl (OH·) radicals is dependent on hyaluronan molecular mass. Cell Biochem. Funct. 12: 281-288 https://doi.org/10.1002/cbf.290120409
  25. Siemsen Jensen, N. B., C. R. Melchiorsen, K. V. Jokumsen, and J. Villadsen. 2001. Metabolic behavior of Lactococcus lactis MG1363 in microaerobic continuous cultivation at a low dilution rate. Appl. Environ. Microbiol. 67: 2677-2682 https://doi.org/10.1128/AEM.67.6.2677-2682.2001
  26. Stephanopoulos, G. and J. J. Vallino. 1991. Network rigidity and metabolic engineering in metabolite overproduction. Science 252: 1675-1681 https://doi.org/10.1126/science.1904627
  27. Tlapak-Simmons, V. L., B. A. Baggenstoss, K. Kumari, C. Heldermon, and P. H. Weigel. 1999. Kinetic characterization of the recombinant hyaluronan synthases from Streptococcus pyogenes and Streptococcus equisimilis. J. Biol. Chem. 274: 4246-4253 https://doi.org/10.1074/jbc.274.7.4246
  28. Widner, B., R$\acute{e}$gine Behr, S. Von Dollen, M. Tang, T. Heu, A. Sloma, et al. 2005. Hyaluronic acid production in Bacillus subtilis. Appl. Environ. Microbiol. 71: 3747-3752 https://doi.org/10.1128/AEM.71.7.3747-3752.2005
  29. Yu, H. and G. Stephanopoulos. 2008. Metabolic engineering of Escherichia coli for biosynthesis of hyaluronic acid. Metab. Eng. 10: 24-32 https://doi.org/10.1016/j.ymben.2007.09.001

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