Advertisement

Applied Biochemistry and Biotechnology

, Volume 171, Issue 4, pp 832–846 | Cite as

Dynamic Changes in Xylanases and β-1,4-Endoglucanases Secreted by Aspergillus niger An-76 in Response to Hydrolysates of Lignocellulose Polysaccharide

  • Sheng Xing
  • Guoli Li
  • Xulu Sun
  • Su Ma
  • Guanjun Chen
  • Lushan Wang
  • Peiji Gao
Article

Abstract

Aspergillus niger is an effective secretor of glycoside hydrolases that facilitate the saprophytic lifestyle of the fungus by degrading plant cell wall polysaccharides. In the present study, a series of dynamic zymography assays were applied to quantify the secreted glycoside hydrolases of A. niger cultured in media containing different carbon sources. Differences in the diversity and concentrations of polysaccharide hydrolysates dynamically regulated the secretion of glycoside hydrolases. The secretion of β-1,4-endoglucanase isozymes was observed to lag at least 24 h behind, rather than coincide with, the secretion of xylanase isozymes. Low concentrations of xylose could induce many endoxylanases (such as Xyn1/XynA, Xyn2, and Xyn3/XynB). High concentrations of xylose could sustain the induction of Xyn2 and Xyn3/XynB but repress Xyn1/XynA (GH10 endoxylanase), which has a broad substrate specificity, and also triggers the low-level secretion of Egl3/EglA, which also has a broad substrate specificity. Mixed polysaccharide hydrolysates sustained the induction of Egl1, whereas the other β-1,4-endoglucanases were sustainably induced by the specific polysaccharide hydrolysates released during the hydrolysis process (such as Egl2 and Egl4). These results indicate that the secretion of glycoside hydrolases may be specifically regulated by the production of polysaccharide hydrolysates released during the process of biomass degradation.

Keywords

Aspergillus niger Glycoside hydrolase Carbon source Dynamic zymography assay Hydrolysates of lignocellulose 

Notes

Acknowledgments

We thank Yinbo Qu, Bin Huang, Dandan Li, and Xiaomei Zhang for their critical reading of the manuscript. This work was supported by grants from the Major State Basic Research Development Research Program of China (grant no. 2011CB707401) and the National Natural Science Foundation of China (30970092, 31170071).

Supplementary material

12010_2013_402_MOESM1_ESM.doc (1.1 mb)
ESM 1 (DOC 1121 kb)

References

  1. 1.
    Dashtban, M., Schraft, H., & Qin, W. (2009). International Journal of Biological Sciences, 5, 578–595.CrossRefGoogle Scholar
  2. 2.
    de Vries, R. P., & Visser, J. (2001). Microbiology and Molecular Biology Reviews, 65, 497–522.CrossRefGoogle Scholar
  3. 3.
    Himmel, M. E., Ding, S. Y., Johnson, D. K., Adney, W. S., Nimlos, M. R., Brady, J. W., et al. (2007). Science, 315, 804–807.CrossRefGoogle Scholar
  4. 4.
    Lynd, L. R., Wyman, C. E., & Gerngross, T. U. (1999). Biotechnology Progress, 15, 777–793.CrossRefGoogle Scholar
  5. 5.
    Lynd, L. R., Laser, M. S., Bransby, D., Dale, B. E., Davison, B., Hamilton, R., et al. (2008). Nature Biotechnology, 26, 169–172.CrossRefGoogle Scholar
  6. 6.
    Ding, S. Y., & Himmel, M. E. (2006). Journal of Agricultural and Food Chemistry, 54, 597–606.CrossRefGoogle Scholar
  7. 7.
    Cosgrove, D. J. (2005). Nature Reviews. Molecular Cell Biology, 6, 850–861.CrossRefGoogle Scholar
  8. 8.
    Rubin, E. M. (2008). Nature, 454, 841–845.CrossRefGoogle Scholar
  9. 9.
    van den Brink, J., & de Vries, R. P. (2011). Applied Microbiology and Biotechnology, 91, 1477–1492.CrossRefGoogle Scholar
  10. 10.
    Pel, H. J., de Winde, J. H., Archer, D. B., Dyer, P. S., Hofmann, G., Schaap, P. J., et al. (2007). Nat. Biotechnol, 25, 221–231.CrossRefGoogle Scholar
  11. 11.
    Andersen, M. R., Nielsen, M. L., & Nielsen, J. (2008). Molecular Systems Biology, 4, 178.CrossRefGoogle Scholar
  12. 12.
    Baker, S. E. (2006). Medical Mycology, 44, 17–21.CrossRefGoogle Scholar
  13. 13.
    Andersen, M. R., Salazar, M. P., Schaap, P. J., van de Vondervoort, P. J. I., Culley, D., Thykaer, J., et al. (2011). Genome Research, 21, 885–897.CrossRefGoogle Scholar
  14. 14.
    Martinez, D., Berka, R. M., Henrissat, B., Saloheimo, M., Arvas, M., Baker, S. E., et al. (2008). Nature Biotechnology, 26, 553–560.CrossRefGoogle Scholar
  15. 15.
    Lu, X., Sun, J., Nimtz, M., Wissing, J., Zeng, A. P., & Rinas, U. (2010). Microbial Cell Factories, 9, 23.CrossRefGoogle Scholar
  16. 16.
    Adav, S. S., Chao, L. T. and Sze, S. K. (2012). Molecular & Cellular Proteomics, 11Google Scholar
  17. 17.
    Wilson, D. B. (2011). Current Opinion in Microbiology, 14, 259–263.CrossRefGoogle Scholar
  18. 18.
    Alon, U. (2007). An Introduction to Systems Biology: Design Principles of Biological Circuits. ed. CRC press.Google Scholar
  19. 19.
    Lynd, L. R., Weimer, P. J., van Zyl, W. H., & Pretorius, I. S. (2002). Microbiology and Molecular Biology Reviews, 66, 506–577.CrossRefGoogle Scholar
  20. 20.
    Dekel, E., & Alon, U. (2005). Nature, 436, 588–592.CrossRefGoogle Scholar
  21. 21.
    Zaslaver, A., Mayo, A. E., Rosenberg, R., Bashkin, P., Sberro, H., Tsalyuk, M., et al. (2004). Nature Genetics, 36, 486–491.CrossRefGoogle Scholar
  22. 22.
    Stricker, A. R., Mach, R. L., & de Graaff, L. H. (2008). Applied Microbiology and Biotechnology, 78, 211–220.CrossRefGoogle Scholar
  23. 23.
    Foreman, P. K., Brown, D., Dankmeyer, L., Dean, R., Diener, S., Dunn-Coleman, N. S., et al. (2003). The Journal of Biological Chemistry, 278, 31988–31997.CrossRefGoogle Scholar
  24. 24.
    Kostylev, M., & Wilson, D. (2012). Biofuels, 3, 61–70.CrossRefGoogle Scholar
  25. 25.
    Wang, L., Zhang, Y., Gao, P., Shi, D., Liu, H., & Gao, H. (2006). Biotechnology and Bioengineering, 93, 443–456.CrossRefGoogle Scholar
  26. 26.
    Ghose, T. K. (1987). Pure and Applied Chemistry, 59, 257–268.CrossRefGoogle Scholar
  27. 27.
    Dashtban, M., Buchkowski, R., & Qin, W. (2011). International Journal of Biochemistry and Molecular Biology, 2, 274–286.Google Scholar
  28. 28.
    Chen, H., Gao, P., & Wang, Z. (1990). Acta Microbiologica Sinica, 30, 351–357.Google Scholar
  29. 29.
    Jørgensen, T., Goosen, T., van den Hondel, C., Ram, A., & Iversen, J. (2009). BMC Genomics, 10, 44.CrossRefGoogle Scholar
  30. 30.
    Gao, P., Qu, Y., Zhao, X., Zhu, M., & Duan, Y. (1997). Enzyme and Microbial Technology, 20, 581–584.CrossRefGoogle Scholar
  31. 31.
    Margolles-clark, E., Ihnen, M., & Penttila, M. (1997). Journal of Biotechnology, 57, 167–179.CrossRefGoogle Scholar
  32. 32.
    Miller, G. L. (1959). Analytical Chemistry, 31, 426–428.CrossRefGoogle Scholar
  33. 33.
    Levasseur, A., Asther, M., & Record, E. (2005). Canadian Journal of Microbiology, 51, 177–183.CrossRefGoogle Scholar
  34. 34.
    Narasimha, G., Sridevi, A., Buddolla, V., Subhosh, C. M., & Rajasekhar, R. B. (2006). African Journal of Biotechnology, 5(5), 472–476.Google Scholar
  35. 35.
    Zhang, X., Liu, N., Yang, F., Li, J., Wang, L., Chen, G., et al. (2012). Electrophoresis, 33, 280–287.CrossRefGoogle Scholar
  36. 36.
    Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V., & Mann, M. (2006). Nature Protocols, 1, 2856–2860.CrossRefGoogle Scholar
  37. 37.
    Jackson, P. (1990). The Biochemical Journal, 270, 705–713.Google Scholar
  38. 38.
    Zhang, Y. H. P., & Lynd, L. R. (2003). Analytical Biochemistry, 322, 225–232.CrossRefGoogle Scholar
  39. 39.
    Viniegra-Gonzále, G., Favela-Torres, E., Aguilar, C. N., Rómero-Gomez, S. J., Díaz-Godínez, G., & Augur, C. (2003). Biochemical Engineering Journal, 13, 157–167.CrossRefGoogle Scholar
  40. 40.
    Beesley, T. E., Buglio, B. and Scott, R. P. W. (2001). Quantitative Chromatographic Analysis. ed. CRC.Google Scholar
  41. 41.
    Mach-Aigner, A. R., Omony, J., Jovanovic, B., van Boxtel, A. J. B., & de Graaff, L. H. (2012). Applied and Environmental Microbiology, 78, 3145–3155.CrossRefGoogle Scholar
  42. 42.
    Olivares-Hernández, R., Usaite, R., & Nielsen, J. (2010). Biotechnology and Bioengineering, 107, 865–875.CrossRefGoogle Scholar
  43. 43.
    Mach-Aigner, A. R., Pucher, M. E., & Mach, R. L. (2010). Applied and Environmental Microbiology, 76, 1770–1776.CrossRefGoogle Scholar
  44. 44.
    Zeilinger, S., Mach, R. L., Schindler, M., Herzog, P., & Kubicek, C. P. (1996). The Journal of Biological Chemistry, 271, 25624–25629.CrossRefGoogle Scholar
  45. 45.
    Dodd, D., & Cann, I. K. (2009). GCB Bioenergy, 1, 2–17.CrossRefGoogle Scholar
  46. 46.
    Khandeparker, R., & Numan, M. T. (2008). Journal of Industrial Microbiology and Biotechnology, 35, 635–644.CrossRefGoogle Scholar
  47. 47.
    Powlowski, J., Mahajan, S., Schapira, M., & Master, E. R. (2009). Carbohydrate Research, 344, 1175–1179.CrossRefGoogle Scholar
  48. 48.
    Aro, N., Pakula, T., & Penttilä, M. (2005). FEMS Microbiology Reviews, 29, 719–739.CrossRefGoogle Scholar
  49. 49.
    Galazka, J. M., Tian, C., Beeson, W. T., Martinez, B., Glass, N. L., & Cate, J. H. D. (2010). Science, 330, 84–86.CrossRefGoogle Scholar
  50. 50.
    Jojima, T., Omumasaba, C. A., Inui, M., & Yukawa, H. (2010). Applied Microbiology and Biotechnology, 85, 471–480.CrossRefGoogle Scholar
  51. 51.
    Burton, R. A., Gidley, M. J., & Fincher, G. B. (2010). Nature Chemical Biology, 6, 724–732.CrossRefGoogle Scholar
  52. 52.
    Coutinho, P. M., Andersen, M. R., Kolenova, K., VanKuyk, P. A., Benoit, I., Gruben, B. S., et al. (2009). Fungal Genetics and Biology, 46(Suppl 1), S161–S169.CrossRefGoogle Scholar
  53. 53.
    Znameroski, E. A., Coradetti, S. T., Roche, C. M., Tsai, J. C., Iavarone, A. T., Cate, J. H. D., et al. (2012). Proceedings of the National Academy of Sciences USA, 109, 6012–6017.CrossRefGoogle Scholar
  54. 54.
    Hori, C., Suzuki, H., Igarashi, K., & Samejima, M. (2012). Applied and Environmental Microbiology, 78, 3770–3773.CrossRefGoogle Scholar
  55. 55.
    Furukawa, T., Shida, Y., Kitagami, N., Mori, K., Kato, M., Kobayashi, T., et al. (2009). Fungal Genetics and Biology, 46, 564–574.CrossRefGoogle Scholar
  56. 56.
    Igarashi, K., Uchihashi, T., Koivula, A., Wada, M., Kimura, S., Okamoto, T., et al. (2011). Science, 333, 1279–1282.CrossRefGoogle Scholar
  57. 57.
    Raman, B., Pan, C., Hurst, G. B., Rodriguez, M., Jr., McKeown, C. K., Lankford, P. K., et al. (2009). PloS One, 4, e5271.CrossRefGoogle Scholar
  58. 58.
    Bahari, L., Gilad, Y., Borovok, I., Kahel-Raifer, H., Dassa, B., Nataf, Y., et al. (2011). Journal of Industrial Microbiology & Biotechnology, 38, 825–832.CrossRefGoogle Scholar
  59. 59.
    Schmoll, M., & Kubicek, C. P. (2003). Acta Microbiologica et Immunologica Hungarica, 50, 125–145.CrossRefGoogle Scholar
  60. 60.
    Himmel, M. E. (2008). Biomass Recalcitrance: Deconstructing the Plant Cell Wall for Bioenergy. ed. Blackwell Pub.Google Scholar
  61. 61.
    Wilson, D. B. (2012). Applied Microbiology and Biotechnology, 93, 497–502.CrossRefGoogle Scholar
  62. 62.
    Kurašin, M., & Väljamäe, P. (2011). The Journal of Biological Chemistry, 286, 169–177.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Sheng Xing
    • 1
  • Guoli Li
    • 1
  • Xulu Sun
    • 1
  • Su Ma
    • 2
  • Guanjun Chen
    • 1
  • Lushan Wang
    • 1
  • Peiji Gao
    • 1
  1. 1.State Key Laboratory of Microbial TechnologyShandong UniversityJinanPeople’s Republic of China
  2. 2.Department of Molecular Biology, School of Medicine and PharmacyOcean University of ChinaQingdaoPeople’s Republic of China

Personalised recommendations