Applied Biochemistry and Biotechnology

, Volume 175, Issue 1, pp 573–588 | Cite as

Molecular and Biochemical Characterization of a Novel Multidomain Xylanase from Arthrobacter sp. GN16 Isolated from the Feces of Grus nigricollis

  • Junpei Zhou
  • Jidong Shen
  • Rui Zhang
  • Xianghua Tang
  • Junjun Li
  • Bo Xu
  • Junmei Ding
  • Yajie Gao
  • Dongyan Xu
  • Zunxi Huang
Article

Abstract

A novel glycosyl hydrolase family 10 (GH 10) xylanase (XynAGN16), consisting of five domains, was revealed from the genome sequence of Arthrobacter sp. GN16 isolated from the feces of Grus nigricollis. XynAGN16 and its truncated derivatives XynAGN16L (GH 10 domain at N-terminus) and XynAGN16Lpd (GH 10 domain at N-terminus and polysaccharide deacetylases domain) were expressed in Escherichia coli and characterized. Biochemical characterizations and hydrolysis products analyses of recombinant XynAGN16L and XynAGN16Lpd showed similar features, including showing catalytic activities at 0 °C, thermolabilities at temperatures of more than 50 °C, and similar substrate specificity. However, the polysaccharide deacetylases domain improved the affinity and catalytic efficiency towards xylans of the recombinant XynAGN16Lpd. The Km and kcat/Km values of recombinant XynAGN16L towards birchwood xylan were 2.6 mg/mL and 19.5 mL/mg/s, respectively, while the two values of recombinant XynAGN16Lpd were 1.2 mg/mL and 42.7 mL/mg/s, respectively. Towards beechwood xylan, the Km and kcat/Km values of recombinant XynAGN16L were 1.8 mg/mL and 27.1 mL/mg/s, respectively, while the two values of recombinant XynAGN16Lpd were 1.0 mg/mL and 35.3 mL/mg/s, respectively. Compared with three thermophilic endoxylanases, XynAGN16L has a surface loop from A57 to Y77 and a decreased number of salt bridges.

Keywords

Multidomain Xylanase Polysaccharide deacetylases Low-temperature-active Kinetic Grus nigricollis 

Supplementary material

12010_2014_1295_MOESM1_ESM.doc (30 kb)
ESM 1(DOC 30 kb)
12010_2014_1295_MOESM2_ESM.doc (514 kb)
ESM 2(DOC 514 kb)

References

  1. 1.
    Collins, T., Gerday, C., & Feller, G. (2005). FEMS Microbiology Reviews, 29, 3–23.CrossRefGoogle Scholar
  2. 2.
    Du, Y. L., Shi, P. J., Huang, H. Q., Zhang, X., Luo, H. Y., Wang, Y. R., & Yao, B. (2013). Bioresource Technology, 130, 161–167.CrossRefGoogle Scholar
  3. 3.
    Finn, R. D., Tate, J., Mistry, J., Coggill, P. C., Sammut, S. J., Hotz, H. R., Ceric, G., Forslund, K., Eddy, S. R., Sonnhammer, E. L. L., & Bateman, A. (2008). Nucleic Acids Research, 36, D281–D288.CrossRefGoogle Scholar
  4. 4.
    Blanco, A., Diaz, P., Zueco, J., Parascandola, P., & Pastor, F. I. J. (1999). Microbiology-UK, 145, 2163–2170.CrossRefGoogle Scholar
  5. 5.
    Zhou, J. P., Shi, P. J., Zhang, R., Huang, H. Q., Meng, K., Yang, P. L., & Yao, B. (2011). Journal of Industrial Microbiology & Biotechnology, 38, 523–530.CrossRefGoogle Scholar
  6. 6.
    Sakka, M., Higashi, Y., Kimura, T., Ratanakhanokchai, K., & Sakka, K. (2011). Applied and Environmental Microbiology, 77, 4260–4263.CrossRefGoogle Scholar
  7. 7.
    Kim, H., Jung, K. H., & Pack, M. Y. (2000). Applied Microbiology and Biotechnology, 54, 521–527.CrossRefGoogle Scholar
  8. 8.
    Ito, Y., Tomita, T., Roy, N., Nakano, A., Sugawara-Tomita, N., Watanabe, S., Okai, N., Abe, N., & Kamio, Y. (2003). Applied and Environmental Microbiology, 69, 6969–6978.CrossRefGoogle Scholar
  9. 9.
    Kim, D. Y., Han, M. K., Park, D. S., Lee, J. S., Oh, H. W., Shin, D. H., Jeong, T. S., Kim, S. U., Bae, K. S., Son, K. H., & Park, H. Y. (2009). Applied and Environmental Microbiology, 75, 7275–7279.CrossRefGoogle Scholar
  10. 10.
    Kong, D. J., Yang, X. J., Liu, Q., Zhong, X. Y., & Yang, J. X. (2011). Oryx, 45, 258–264.CrossRefGoogle Scholar
  11. 11.
    Brulc, J. M., Antonopoulos, D. A., Miller, M. E. B., Wilson, M. K., Yannarell, A. C., Dinsdale, E. A., Edwards, R. E., Frank, E. D., Emerson, J. B., Wacklin, P., Coutinho, P. M., Henrissat, B., Nelson, K. E., & White, B. A. (2009). Proceedings of the National Academy of Sciences of the United States of America, 106, 1948–1953.CrossRefGoogle Scholar
  12. 12.
    Kim, D. Y., Ham, S. J., Lee, H. J., Kim, Y. J., Shin, D. H., Rhee, Y. H., Son, K. H., & Park, H. Y. (2011). Enzyme and Microbial Technology, 48, 365–370.CrossRefGoogle Scholar
  13. 13.
    Ley, R. E., Hamady, M., Lozupone, C., Turnbaugh, P. J., Ramey, R. R., Bircher, J. S., Schlegel, M. L., Tucker, T. A., Schrenzel, M. D., Knight, R., & Gordon, J. I. (2008). Science, 320, 1647–1651.CrossRefGoogle Scholar
  14. 14.
    Wang, G., Luo, H., Wang, Y., Huang, H., Shi, P., Yang, P., Meng, K., Bai, Y., & Yao, B. (2011). Bioresource Technology, 102, 3330–3336.CrossRefGoogle Scholar
  15. 15.
    Warnecke, F., Luginbuhl, P., Ivanova, N., Ghassemian, M., Richardson, T. H., Stege, J. T., Cayouette, M., McHardy, A. C., Djordjevic, G., Aboushadi, N., Sorek, R., Tringe, S. G., Podar, M., Martin, H. G., Kunin, V., Dalevi, D., Madejska, J., Kirton, E., Platt, D., Szeto, E., Salamov, A., Barry, K., Mikhailova, N., Kyrpides, N. C., Matson, E. G., Ottesen, E. A., Zhang, X. N., Hernandez, M., Murillo, C., Acosta, L. G., Rigoutsos, I., Tamayo, G., Green, B. D., Chang, C., Rubin, E. M., Mathur, E. J., Robertson, D. E., Hugenholtz, P., & Leadbetter, J. R. (2007). Nature, 450, 560–565.CrossRefGoogle Scholar
  16. 16.
    Zhou, J. P., Gao, Y. J., Zhang, R., Mo, M. H., Tang, X. H., Li, J. J., Xu, B., Ding, J. M., & Huang, Z. X. (2014). Process Biochemistry. doi:10.1016/j.procbio.2014.06.013.Google Scholar
  17. 17.
    Zhou, J. P., Pan, L., Li, J. J., Tang, X. H., & Huang, Z. X. (2012). Wei Sheng Wu Xue Bao (Acta Microbiologica Sinica), 52, 611–619.Google Scholar
  18. 18.
    Chen, S., Kaufman, M. G., Miazgowicz, K. L., Bagdasarian, M., & Walker, E. D. (2013). Bioresource Technology, 128, 145–155.CrossRefGoogle Scholar
  19. 19.
    Song, H. Y., Lim, H. K., Kim, D. R., Lee, K. I., & Hwang, I. T. (2014). Enzyme and Microbial Technology, 54, 1–7.CrossRefGoogle Scholar
  20. 20.
    Sakka, M., Tachino, S., Katsuzaki, H., van Dyk, J. S., Pletschke, B. I., Kimura, T., & Sakka, K. (2012). Enzyme and Microbial Technology, 51, 193–199.CrossRefGoogle Scholar
  21. 21.
    Zerbino, D. R., & Birney, E. (2008). Genome Research, 18, 821–829.CrossRefGoogle Scholar
  22. 22.
    Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Journal of Molecular Biology, 215, 403–410.CrossRefGoogle Scholar
  23. 23.
    Jiang, Z. Q., Kobayashi, A., Ahsan, M. M., Lite, L., Kitaoka, M., & Hayashi, K. (2001). Journal of Bioscience and Bioengineering, 92, 423–428.CrossRefGoogle Scholar
  24. 24.
    Connerton, I., Cummings, N., Harris, G. W., Debeire, P., & Breton, C. (1999). Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, 1433, 110–121.CrossRefGoogle Scholar
  25. 25.
    Khasin, A., Alchanati, I., & Shoham, Y. (1993). Applied and Environmental Microbiology, 59, 1725–1730.Google Scholar
  26. 26.
    Humphrey, W., Dalke, A., & Schulten, K. (1996). Journal of Molecular Graphics, 14, 33–38.CrossRefGoogle Scholar
  27. 27.
    Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). Journal of Computational Chemistry, 25, 1605–1612.CrossRefGoogle Scholar
  28. 28.
    Willard, L., Ranjan, A., Zhang, H. Y., Monzavi, H., Boyko, R. F., Sykes, B. D., & Wishart, D. S. (2003). Nucleic Acids Research, 31, 3316–3319.CrossRefGoogle Scholar
  29. 29.
    Bradford, M. M. (1976). Analytical Biochemistry, 72, 248–254.CrossRefGoogle Scholar
  30. 30.
    Wang, G. Z., Meng, K., Luo, H. Y., Wang, Y. R., Huang, H. Q., Shi, P. J., Pan, X., Yang, P. L., & Yao, B. (2011). Applied Microbiology and Biotechnology, 91, 1561–1570.CrossRefGoogle Scholar
  31. 31.
    Lineweaver, H., & Burk, D. (1934). Journal of the American Chemical Society, 56, 658–666.CrossRefGoogle Scholar
  32. 32.
    Zhou, J. P., Wu, Q., Zhang, R., Mo, M. H., Tang, X. H., Li, J. J., Xu, B., Ding, J. M., Lu, Q., & Huang, Z. X. (2014). Folia Microbiologica, 59, 423–431.CrossRefGoogle Scholar
  33. 33.
    Vogel, C., Bashton, M., Kerrison, N. D., Chothia, C., & Teichmann, S. A. (2004). Current Opinion in Structural Biology, 14, 208–216.CrossRefGoogle Scholar
  34. 34.
    Duan, X. G., Chen, J., & Wu, J. (2013). Applied and Environmental Microbiology, 79, 4072–4077.CrossRefGoogle Scholar
  35. 35.
    Rodrigues, D. F., & Tiedje, J. M. (2008). Applied and Environmental Microbiology, 74, 1677–1686.CrossRefGoogle Scholar
  36. 36.
    Siddiqui, K. S., & Cavicchioli, R. (2006). Annual Review of Biochemistry, 75, 403–433.CrossRefGoogle Scholar
  37. 37.
    Zhou, J. P., Huang, H. Q., Meng, K., Shi, P. J., Wang, Y. R., Luo, H. Y., Yang, P. L., Bai, Y. G., Zhou, Z. G., & Yao, B. (2009). Applied Microbiology and Biotechnology, 85, 323–333.CrossRefGoogle Scholar
  38. 38.
    Stibor, M., Potocky, M., Pickova, A., Karasova, P., Russell, N. J., & Kralova, B. (2003). Enzyme and Microbial Technology, 32, 532–538.CrossRefGoogle Scholar
  39. 39.
    Lonhienne, T., Zoidakis, J., Vorgias, C. E., Feller, G., Gerday, C., & Bouriotis, V. (2001). Journal of Molecular Biology, 310, 291–297.CrossRefGoogle Scholar
  40. 40.
    Khandeparkar, R. D. S., & Bhosle, N. B. (2006). Enzyme and Microbial Technology, 39, 732–742.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Junpei Zhou
    • 1
    • 2
    • 3
    • 4
  • Jidong Shen
    • 2
  • Rui Zhang
    • 1
    • 2
    • 3
    • 4
  • Xianghua Tang
    • 1
    • 2
    • 3
    • 4
  • Junjun Li
    • 1
    • 2
    • 3
    • 4
  • Bo Xu
    • 1
    • 2
    • 3
    • 4
  • Junmei Ding
    • 1
    • 2
    • 3
    • 4
  • Yajie Gao
    • 2
  • Dongyan Xu
    • 2
  • Zunxi Huang
    • 1
    • 2
    • 3
    • 4
  1. 1.Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of EducationYunnan Normal UniversityKunmingPeople’s Republic of China
  2. 2.College of Life SciencesYunnan Normal UniversityKunmingPeople’s Republic of China
  3. 3.Key Laboratory of Yunnan for Biomass Energy and Biotechnology of Environment, YunnanKunmingPeople’s Republic of China
  4. 4.Key Laboratory of Enzyme EngineeringYunnan Normal UniversityKunmingPeople’s Republic of China

Personalised recommendations