Skip to main content
Log in

Gene Encoding Inulinase Isolated from Penicillium citrinum ESS and Its Molecular Phylogeny

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

Abstract

Inulinase is an enzyme produced by plants and several microorganisms, including fungi, to hydrolyze the β-2,1 glycosidic linkages present in some oligosaccharides to produce fructose and glucose. This enzyme, in conjunction with invertases, levanases, and two types of 1-fructosyl transferases have been described as members of the glycosyl hydrolases (family 32), the most diverse group of enzymes used by microbes for biomass degradation. As being part of the same clan, they have common evolutionary origin sharing the most important functional characteristics. Recently, a xerophylic fungi strain isolated from Mexican semi-desert, Penicillium citrinum ESS has been reported as inulinase producer, which could have greater stability than other enzymes due to a metabolic machinery adapted to typical temperature changes in this region. To continue the understanding of action mechanisms of these enzymes and to establish evolutionary relationships within this family, in the present study, phylogenetic analyses were used to analyze amino acid sequences coding fungal and yeast glycoside hydrolases of family 32, including the new sequenced inulinase of P. citrinum ESS. It was possible to elucidate the action mechanism of fungal glycoside hydrolases in present study and to classify inulinase from P. citrinum ESS as an exo-inulinase on the basis of their amino acid sequence phylogenetic affinities.

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

Similar content being viewed by others

References

  1. Vandamme, E. J., & Derycke, D. G. (1983). Advances in Applied Microbiology, 29, 139–176.

    Article  CAS  Google Scholar 

  2. Pandey, A., Soccol, C. R., Selvakumar, P., Soccol, V. T., Krieger, N., & Fontana, J. D. (1999). Applied Biochemistry and Biotechnology, 81, 35–52.

    Article  CAS  Google Scholar 

  3. Roberfroid, M. (1993). Critical Reviews in Food Science and Nutrition, 33, 103–148.

    Article  CAS  Google Scholar 

  4. Murphy, C., Powlowski, J., Wu, M., Butler, G., & Tsang, A. (2011). Database. doi:10.1093/database/bar020.

    Google Scholar 

  5. Onodera, S., & Shiomi, N. (1992). Bioscience, Biotechnology, and Biochemistry, 56, 1443–1447.

    Article  CAS  Google Scholar 

  6. Ettalibi, M., & Baratti, J. C. (1987). Applied Microbiology and Biotechnology, 26, 13–20.

    Article  CAS  Google Scholar 

  7. Nakamura, T., Shitara, A., Matsuda, S., Matsuo, T., Suiko, M., & Ohta, K. (1997). Journal of Fermentation and Bioengineering, 84, 313–318.

    Article  CAS  Google Scholar 

  8. Chi, Z., Zhang, T., Liu, G., & Yue, L. (2009). Applied Microbiology and Biotechnology, 82, 211–220.

    Article  CAS  Google Scholar 

  9. Nakamura, T., Kurokawa, T., Nakatsu, S., & Ueda, S. (1978). Nippon Nogeikagaku Kaishi, 52, 159–166.

    Article  CAS  Google Scholar 

  10. Onodera, S., Murakami, T., Ito, H., Mori, H., Matsui, H., Honma, M., Chiba, S., & Shiomi, N. (1996). Bioscience Biotechnology and Biochemistry, 60, 1780–1785.

    Article  CAS  Google Scholar 

  11. Ohta, K., Suetsugu, N., & Nakamura, T. (2002). Journal of Bioscience and Bioengineering, 94, 78–80.

    Article  CAS  Google Scholar 

  12. Uhm, T. B., Chae, K. S., Lee, D. W., Kim, H. S., Cassart, J. P., & Vandenhaute, J. (1998). Biotechnological Letters, 20, 809–812.

    Article  CAS  Google Scholar 

  13. Burne, R. A., & Penders, J. E. (1992). Infection and Immunity, 60, 4621–4632.

    CAS  Google Scholar 

  14. Arand, M., Golubev, A. M., Neto, J. R., Polikarpov, I., Wattiez, R., Korneeva, O. S., Eneyskaya, E. V., Kulminskaya, A. A., Shabalin, K. A., Shishliannikov, S. M., Chepurnaya, O. V., & Neustroev, K. N. (2002). Biochemical Journal, 362, 131–135.

    Article  CAS  Google Scholar 

  15. Tsujimoto, Y., Watanabe, A., Nakano, K., Watanabe, K., Matsui, H., Tsuji, K., Tsukihara, T., & Suzuki, Y. (2003). Applied Microbiology and Biotechnology, 62, 180–185.

    Article  CAS  Google Scholar 

  16. Flores-Gallegos, A. C., Morlett-Chávez, J., Aguilar, C. N., & Rodríguez-Herrera, R. (2012). Advance Journal of Food Science and Technology, 4(1), 46–50.

    CAS  Google Scholar 

  17. Borrego-Terrazas, J. A., Lara-Victoriano, F., Flores-Gallegos, A. C., Veana, F., Aguilar, C. N., & Rodríguez-Herrera, R. (2014). Canadian Journal of Microbiology, 60, 509–516.

    Article  CAS  Google Scholar 

  18. Varfolomeev, S. D., Uporov, I. V., & Federov, E. V. (2002). Biochemistry (Moscow), 67(10), 1099–1108.

    Article  CAS  Google Scholar 

  19. Henrissat, B., & Davies, G. (1997). Current Opinion in Structural Biology, 7, 637–644.

    Article  CAS  Google Scholar 

  20. Coutinho, P. M., & Henrissat, B. (1999). Carbohydrate active enzymes: an integrated database approach. In H. J. Gilbert, G. Davies, H. Henrissat, & B. Svensson (Eds.), Recent Advances in Carbohydrate Bioengineering (pp. 3–12). Cambridge: The Royal Society of Chemistry.

    Google Scholar 

  21. Naumoff, D. G. (2011). Biochemistry, 76, 622–635.

    CAS  Google Scholar 

  22. Henrissat, B. (1998). Biochemical Society Transactions, 26, 153–156.

    CAS  Google Scholar 

  23. Stoesser, G., Baker, W., van den Broek, A., Camon, E., Garcia-Pastor, M., Kanz, C., Kulikova, T., Lombard, V., Lopez, R., Parkinson, H., Redaschi, N., Sterk, P., Stoehr, P., & Tuli, M. A. (2001). Nucleic Acids Research, 29, 17–21.

    Article  CAS  Google Scholar 

  24. Bateman, A., Birney, E., Durbin, R., Eddy, S. R., Howe, K. L., & Sonnhammer, E. L. (2000). Nucleic Acids Research, 28, 263–266.

    Article  CAS  Google Scholar 

  25. Pellegrini, M. (2001). Current Opinion in Chemical Biology, 5, 46–50.

    Article  CAS  Google Scholar 

  26. Cruz-Hernandez, M. A., Contreras-Esquivel, J. C., Lara, F., Rodríguez-Herrera, R., & Aguilar, C. N. (2005). Naturforschung, 60, 844–848.

    CAS  Google Scholar 

  27. Barth, G., & Gallardin, G. (1993). In K. Wolf (Ed.), Non-conventional yeasts in biotechnology (pp. 313–388). Berlin: Springer.

    Google Scholar 

  28. Sambrook, J., & Russel, D. W. (2001). Molecular cloning, vol. 1 (3rd ed., pp. 32–34). New York: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  29. Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J., Kapp, B. A., & Wheeler, D. L. (2000). Nucleic Acids Research, 28, 15–18.

    Article  CAS  Google Scholar 

  30. Lammens, W., Le Roy, K., Schroeven, L., Van Laere, A., Rabijns, A., & Van den Ende, W. (2009). Journal of Experimental Botany, 60, 727–740.

    Article  CAS  Google Scholar 

  31. Finn, R. D., Tate, J., Mistry, J., Coggill, P. C., Sammut, S. J., Hotz, H.-R., Ceric, G., Forslund, K. M., Eddy, S. R., Sonhammer, E. L. L., & Batemanm, A. (2010). Nucleic Acids Research, 36, 281–288.

    Article  Google Scholar 

  32. Hall, T. A. (1999). Nucleic Acids Symposium Series, 41, 95–98.

    CAS  Google Scholar 

  33. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darlin, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., & Huelsenbeck, J. P. (2012). Systematic Biology, 61(3), 539–542.

    Article  Google Scholar 

  34. Guindon, S., & Gascuel, O. (2003). Systematic Biology, 52, 696–704.

    Article  Google Scholar 

  35. van den Berg, M. A., Albang, R., Albermann, K., Badger, J. H., Daran, J. M., Driessen, A. J., Garcia-Estrada, C., Fedorova, N. D., Harris, D. M., Heijne, W. H., Joardar, V., Kiel, J. A., Kovalchuk, A., Martin, J. F., Nierman, W. C., Nijland, J. G., Pronk, J. T., Roubos, J. A., van der Klei, I. J., van Peij, N. N., Veenhuis, M., von Dohren, H., Wagner, C., Wortman, J., & Bovenberg, R. A. (2008). Nature Biotechnology, 26(10), 1161–1168.

    Article  CAS  Google Scholar 

  36. Yuan, X. L., Goosen, C., Kools, H., van der Maarel, M. J., van den Hondel, C. A., Dijkhuizen, L., & Ram, A. F. (2006). Microbiology, 152(10), 3061–3073.

    Article  CAS  Google Scholar 

  37. Wang, L., Huang, Y., Long, X., Meng, X., & Liu, Z. (2011). Journal of Applied Microbiology, 111(6), 1371–1380.

    Article  CAS  Google Scholar 

  38. Akimoto, H., Kiyota, N., Kushima, T., Nakamura, T., & Ohta, K. (2000). Bioscience Biotechnology and Biochemistry, 64(11), 2328–2335.

    Article  CAS  Google Scholar 

  39. Henrissat, B. (1991). Biochemical Journal, 280, 309–316.

    CAS  Google Scholar 

  40. Altenbach, D., Nüesch, E., Ritsema, T., Boller, T., & Wiemken, A. (2004). FEBS Letters, 567, 214–218.

    Article  CAS  Google Scholar 

  41. Park, S., Han, Y., Kim, H., Song, S., Uhm, T. B., & Chae, K. S. (2003). Biochemistry (Moscow), 68, 658–661.

    Article  CAS  Google Scholar 

  42. Nagem, R. A., Rojas, A. L., Golubev, A. M., Korneeva, O. S., Eneyskaya, E. V., Kulminskaya, A. A., Neustroev, K. N., & Polikarpov, I. (2004). Journal of Molecular Biology, 344, 471–480.

    Article  CAS  Google Scholar 

  43. Singh, P., & Gill, P. K. (2006). Food Technology and Biotechnology, 44, 151–162.

    CAS  Google Scholar 

  44. Ohta, K., Akimoto, H., Matsuda, S., Toshimitsu, D., & Nakamura, T. (1998). Bioscience, Biotechnology, and Biochemistry, 62, 1731–1738.

    Article  CAS  Google Scholar 

  45. Laloux, O., Cassart, J. P., Delcour, J., Beeumen, J. V., & Vandenhaute, J. (1991). FEBS Letters, 289, 64–68.

    Article  CAS  Google Scholar 

  46. Zahn, L. M., King, H. Z., Leebens-Mack, J. H., Kim, S., Soltis, P. S., Landherr, L. L., Soltis, D. E., de Pamphilis, C. W., & Ma, H. (2005). Genetics, 169, 2209–2223.

    Article  CAS  Google Scholar 

  47. Litt, A., & Irish, V. F. (2003). Genetics, 165, 821–833.

    CAS  Google Scholar 

Download references

Acknowledgments

We would like to acknowledge Iñaki Ruiz-Trillo, who supported the present work in the search and analysis of protein domains. This project was financially supported by the Universidad Autónoma de Coahuila. A.C.F.G. wants to thank to the Mexican National Council of Science and Technology (CONACYT) for the financial support during her postgraduate studies.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Raúl Rodríguez-Herrera.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Flores-Gallegos, A.C., Morlett-Chávez, J.A., Aguilar, C.N. et al. Gene Encoding Inulinase Isolated from Penicillium citrinum ESS and Its Molecular Phylogeny. Appl Biochem Biotechnol 175, 1358–1370 (2015). https://doi.org/10.1007/s12010-014-1280-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-014-1280-9

Keywords

Navigation