Skip to main content

Advertisement

Log in

Enhancement of Stress Tolerance in the Polyhydroxyalkanoate Producers without Mobilization of the Accumulated Granules

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Poly(3-hydroxybutyrate) [P(3HB)], a polymer belonging to the polyhydroxyalkanoate (PHA) family, is accumulated by numerous bacteria as carbon and energy storage material. The mobilization of accumulated P(3HB) is associated with increased stress and starvation tolerance. However, the potential function of accumulated copolymer such as poly(3-hydroxybutyrate-co-3-hydroxyvalerate) [P(3HB-co-3HV)] remained unknown. In this study, Delftia acidovorans DS 17 was used to evaluate the contributions of P(3HB) and P(3HB-co-3HV) granules during simulated exogenous carbon deprivation on cell survival by transferring cells with PHAs to carbon-free mineral salt medium supplemented with 1 % (w/v) nitrogen source. By mobilizing the intracellular P(3HB) and P(3HB-co-3HV) at 11 and 40 mol% 3HV compositions, the cells survived starvation. Surprisingly, D. acidovorans containing P(3HB-co-94 mol% 3HV) also survived although the mobilization was not as effective. Similarly, recombinant Escherichia coli pGEM-T::phbCAB Cn (harboring the PHA biosynthesis genes of Cupriavidus necator) containing P(3HB) granules had a higher viable cell counts compared to those without P(3HB) granules but without any P(3HB) mobilization when exposed to oxidative stress by photoactivated titanium dioxide. This study provided strong evidence that enhancement of stress tolerance in PHA producers can be achieved without mobilization of the previously accumulated granules. Instead, PHA biosynthesis may improve bacterial survival via multiple mechanisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Sudesh, K., Abe, H., & Doi, Y. (2000). Progress in Polymer Science, 25(10), 1503–1555.

    Article  CAS  Google Scholar 

  2. Kadouri, D., Jurkevitch, E., Okon, Y., & Castro-Sowinski, S. (2005). Critical Reviews in Microbiology, 31(2), 55–67.

    Article  CAS  Google Scholar 

  3. Yu, J. (2006). Microbial production of bioplastics from renewable resources. In S. T. Yang (Ed.), Bioprocessing of value added products from renewable resources (pp. 585–610). Amsterdam: Elsevier.

    Google Scholar 

  4. Sudesh, K., & Iwata, T. (2008). CLEAN, 36(5–6), 433–442.

    CAS  Google Scholar 

  5. Keshavarz, T., & Roy, I. (2010). Current Opinion in Microbiology, 13(3), 321–326.

    Article  CAS  Google Scholar 

  6. Castro-Sowinski, S., Burdman, S., Matan, O., & Okon, Y. (2010). Natural functions of bacterial polyhydroxyalkanoates. In G.-Q. Chen (Ed.), Plastics from bacteria: natural functions and applications (Microbiology monographs, Vol. 14, pp. 39–61). Heidelberg: Springer.

    Chapter  Google Scholar 

  7. Tribelli, P. M., & Lopez, N. I. (2011). Extremophiles, 15, 541–547.

    Article  CAS  Google Scholar 

  8. Wang, Q., Yu, H., Xia, Y., Kang, Z., & Qi, Q. (2009). Microbial Cell Factories, 8(47), 47–55.

    Article  Google Scholar 

  9. Handrick, R., Reinhardt, S., & Jendrossek, D. (2000). Journal of Bacteriology, 182(20), 5916–5918.

    Article  CAS  Google Scholar 

  10. Ratcliff, W. C., Kadam, S. V., & Denison, R. F. (2008). FEMS Microbiology Ecology, 65, 391–399.

    Article  CAS  Google Scholar 

  11. James, B. W., Mauchline, W. S., Dennis, P. J., Keevil, C. W., & Wait, R. (1999). Applied and Environmental Microbiology, 65(2), 822–827.

    CAS  Google Scholar 

  12. Ruiz, J. A., López, N. I., Fernandez, R. O., & Mendez, B. S. (2001). Applied and Environmental Microbiology, 67(1), 225–230.

    Article  CAS  Google Scholar 

  13. Ayub, N. D., Pettinari, M. J., Ruiz, J. A., & López, N. I. (2004). Current Opinion in Microbiology, 49(3), 170–174.

    CAS  Google Scholar 

  14. Ayub, N., Tribelli, P., & López, N. (2009). Extremophiles, 13(1), 59–66.

    Article  CAS  Google Scholar 

  15. Zhao, Y. H., Li, H. M., Qin, L. F., Wang, H. H., & Chen, G.-Q. (2007). FEMS Microbiology Letters, 276(1), 34–41.

    Article  CAS  Google Scholar 

  16. Raiger-Iustman, L. J., & Ruiz, J. A. (2008). FEMS Microbiology Letters, 284(2), 218–224.

    Article  CAS  Google Scholar 

  17. Jendrossek, D. (2009). Journal of Bacteriology, 191(10), 3195–3202.

    Article  CAS  Google Scholar 

  18. Tessmer, N., Konig, S., Malkus, U., Reichelt, R., Potter, M., & Steinbuchel, A. (2007). Microbiology, 153(2), 366–374.

    Article  CAS  Google Scholar 

  19. Jiyeun, K. K., Yeo, J. W., Naruo, N., Hiroshi, N., Sang, H. H., Yoshitomo, K., et al. (2013). Proceedings of the National Academy of Sciences of the United States of America, 110(26), E2381–E2389. doi:10.1073/pnas.1303228110.

    Article  Google Scholar 

  20. Uchino, K., Saito, T., Gebauer, B., & Jendrossek, D. (2007). Journal of Bacteriology, 189(22), 8250–8256.

    Article  CAS  Google Scholar 

  21. Braunegg, G., Sonnleitner, B., & Lafferty, R. M. (1978). European Journal of Applied Microbiology and Biotechnology, 6, 29–37.

    Article  CAS  Google Scholar 

  22. Bradford, M. M. (1976). Analytical Biochemistry, 72(1–2), 248–254.

    Article  CAS  Google Scholar 

  23. Jendrossek, D., & Handrick, R. (2002). Annual Review of Microbiology, 56, 403–432.

    Article  CAS  Google Scholar 

  24. Huang, Z., Maness, P.-C., Blake, D. M., Wolfrum, E. J., Smolinski, S. L., & Jacoby, W. A. (2000). Journal of Photochemistry and Photobiology A: Chemistry, 130(2–3), 163–170.

    Article  CAS  Google Scholar 

  25. Maness, P.-C., Smolinski, S., Blake, D. M., Huang, Z., Wolfrum, E. J., & Jacoby, W. A. (1999). Applied and Environmental Microbiology, 65(9), 4094–4098.

    CAS  Google Scholar 

  26. Yan, Y.-B., Wu, Q., & Zhang, R.-Q. (2000). FEMS Microbiology Letters, 193(2), 269–273.

    Article  CAS  Google Scholar 

  27. Handrick, R., Reinhardt, S., Kimmig, P., & Jendrossek, D. (2004). Journal of Bacteriology, 186(21), 7243–7253.

    Article  CAS  Google Scholar 

  28. Potter, M., Muller, H., Reinecke, F., Wieczorek, R., Fricke, F., Bowien, B., et al. (2004). Microbiology, 150(7), 2301–2311.

    Article  Google Scholar 

  29. Rehm, B. H. A. (2010). Nature Reviews. Microbiology, 8, 578–592.

    Article  CAS  Google Scholar 

  30. Yamada, M., Wakuda, A., & Taguchi, S. (2007). Bioscience, Biotechnology, and Biochemistry, 71(6), 1572–1576.

    Article  CAS  Google Scholar 

  31. Ruiz, J. A., López, N. I., & Mendez, B. S. (2004). Current Microbiology, 48(6), 396–400.

    Article  CAS  Google Scholar 

  32. Eisenstark, A., Calcutt, M. J., Becker-Hapak, M., & Ivanova, A. (1996). Free Radical Biology and Medicine, 21(7), 975–993.

    Article  CAS  Google Scholar 

  33. Moreau, P. L. (2004). Journal of Bacteriology, 186(21), 7364–7368.

    Article  CAS  Google Scholar 

  34. Nyström, T. (2003). Cellular and Molecular Life Sciences, 60(7), 1333–1341.

    Article  Google Scholar 

  35. Nyström, T. (2004). Annual Review of Microbiology, 58(1), 161–181.

    Article  Google Scholar 

  36. Ireland, J. C., Klostermann, P., Rice, E. W., & Clark, R. M. (1993). Applied and Environmental Microbiology, 59(5), 1668–1670.

    CAS  Google Scholar 

  37. Pavasupree, S., Suzuki, Y., Pivsa-Art, S., & Yoshikawa, S. (2005). Journal of Solid State Chemistry, 178(1), 128–134.

    Article  CAS  Google Scholar 

  38. Jacoby, W. A., Maness, P. C., Wolfrum, E. J., Blake, D. M., & Fennell, J. A. (1998). Environmental Science and Technology, 32(17), 2650–2653.

    Article  CAS  Google Scholar 

  39. Grage, K., Jahns, A. C., Parlane, N., Palanisamy, R., Rasiah, I. A., Atwood, J. A., et al. (2009). Biomacromolecules, 10(4), 660–669.

    Article  CAS  Google Scholar 

  40. Sudesh, K., Maehara, A., Gan, Z., Iwata, T., & Doi, Y. (2004). Polymer Degradation and Stability, 83(2), 281–287.

    Article  CAS  Google Scholar 

  41. Franke, R., & Franke, C. (1999). Chemosphere, 39(15), 2651–2659.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work forms part of a study funded by the Long Term Research Grant Scheme (LRGS) project supported by the Ministry of Higher Education (MOHE), Malaysia. The authors thank Prof. Yoshiharu Doi for the D. acidovorans and recombinant E. coli strain. Prof. John Leslie’s help in editing the manuscript is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kumar Sudesh.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Goh, LK., Purama, R.K. & Sudesh, K. Enhancement of Stress Tolerance in the Polyhydroxyalkanoate Producers without Mobilization of the Accumulated Granules. Appl Biochem Biotechnol 172, 1585–1598 (2014). https://doi.org/10.1007/s12010-013-0634-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-013-0634-z

Keywords

Navigation