Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Characterization of Cellobiohydrolase from a Newly Isolated Strain of Agaricus arvencis

  • Lee, Kyung-Min (Department of Chemical Engineering, Konkuk University) ;
  • Moon, Hee-Jung (Department of Chemical Engineering, Konkuk University) ;
  • Kalyani, Dayanand (Department of Chemical Engineering, Konkuk University) ;
  • Kim, Hoon (Department of Agricultural Chemistry, Sunchon National University) ;
  • Kim, In-Won (Department of Chemical Engineering, Konkuk University) ;
  • Jeya, Marimuthu (Department of Chemical Engineering, Konkuk University) ;
  • Lee, Jung-Kul (Department of Chemical Engineering, Konkuk University)
  • Received : 2011.02.07
  • Accepted : 2011.03.27
  • Published : 2011.07.28
Download PDF
⟨ Previous Next ⟩

Abstract

A highly efficient cellobiohydrolase (CBH)-secreting basidiomycetous fungus, Agaricus arvensis KMJ623, was isolated and identified based on its morphological features and sequence analysis of internal transcribed spacer rDNA. An extracellular CBH was purified to homogeneity from A. arvencis culture supernatant using sequential chromatography. The relative molecular mass of A. arvencis CBH was determined to be 65 kDa by SDSPAGE and 130 kDa by size-exclusion chromatography, indicating that the enzyme is a dimer. A. arvencis CBH showed a catalytic efficiency ($k_{cat}/K_m$) of 31.8 $mM^{-1}\;s^{-1}$ for p-nitrophenyl-${\beta}$-D-cellobioside, the highest level seen for CBH-producing microorganisms. Its internal amino acid sequences showed significant homology with CBHs from glycoside hydrolase family 7. Although CBHs have been purified and characterized from other sources, A. arvencis CBH is distinguished from other CBHs by its high catalytic efficiency.

Keywords

References

  1. Barros, L., P. Baptista, D. M. Correia, S. Casal, B. Oliveira, and I. C. F. R. Ferreira. 2007. Fatty acid and sugar compositions and nutritional value of five wild edible mushrooms. Food Chem. 105: 140-145. https://doi.org/10.1016/j.foodchem.2007.03.052
  2. Bayer, E. A., H. Chanzy, R. Lamed, and Y. Shoham. 1998. Cellulose, cellulases and cellulosomes. Curr. Opin. Struct. Biol. 8: 548-557. https://doi.org/10.1016/S0959-440X(98)80143-7
  3. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254. https://doi.org/10.1016/0003-2697(76)90527-3
  4. Bukhtojarov, F. E., B. B. Ustinov, T. N. Salanovich, A. I. Antonov, A. V. Gusakov, O. N. Okunev, and A. P. Sinitsyn. 2004. Cellulase complex of the fungus Chrysosporium lucknowense: Isolation and characterization of endoglucanases and cellobiohydrolases. Biochemistry 69: 542-551.
  5. Deshpande, M. V., K. E. Eriksson, and L. G. Pettersson. 1984. An assay for selective determination of exo-1,4-b-glucanases in a mixture of cellulolytic enzymes. Anal. Biochem. 138: 481-487. https://doi.org/10.1016/0003-2697(84)90843-1
  6. Doran-Peterson, J., A. Jangid, S. K. Brandon, E. DeCrescenzo- Henriksen, B. Dien, and L. O. Ingram. 2009. Simultaneous saccharification and fermentation and partial saccharification and co-fermentation of lignocellulosic biomass for ethanol production. Methods Mol. Biol. 581: 263-280.
  7. Edwards, I. P., R. A. Upchurch, and R. Z. Donald. 2008. A classification of glycosyl hydrolases based on amino acid sequence similarity. Appl. Environ. Microbiol. 74. 74: 3481- 3489.
  8. Gusakov, A. V., A. P. Sinitsyn, T. N. Salanovich, F. E. Bukhtojarov, A. V. Markov, B. B. Ustinov, C. Van Zeijl, P. Punt, and R. Burlingame. 2005. Purification, cloning and characterization of two forms of thermostable and highly active cellobiohydrolase I (Cel7A) produced by the industrial strain of Chrysosporium lucknowense. Enzyme Microb. Technol. 36: 57-69. https://doi.org/10.1016/j.enzmictec.2004.03.025
  9. Haakana, H., A. Miettinen-Oinonen, V. Joutsjoki, A. Mantyla, P. Suominen, and J. Vehmaanpera. 2004. Cloning of cellulose genes from Melanocarpus albomyces and their efficient expression in Trichoderma reesei. Enzyme Microb. Technol. 34: 159-167. https://doi.org/10.1016/j.enzmictec.2003.10.009
  10. Hamada, N., K. Ishikawa, N. Fuse, R. Kodaira, M. Shimosaka, Y. Amano, T. Kanda, and M. Okazaki. 1999. Purification characterization and gene analysis of exo-cellulase II (Ex-2) from the white rot basidiomycete Irpex lacteus. J. Biosci. Bioeng. 87: 442-451. https://doi.org/10.1016/S1389-1723(99)80092-9
  11. Henrissat, B. 1991. A classification of glycosyl hydrolases based on amino acid sequence similarity. Biochem. J. 280: 309- 316. https://doi.org/10.1042/bj2800309
  12. Hong, J., H. Tamaki, K. Yamamoto, and H. Kumagai. 2003. Cloning of a gene encoding thermostable cellobiohydrolase from Thermoascus aurantiacus and its expression in yeast. Appl. Microbiol. Biotechnol. 63: 42-50. https://doi.org/10.1007/s00253-003-1379-3
  13. Jia, J., P. S. Dyer, and J. F. Buswell. 1999. Cloning of the CBHI and CBHII genes involved in cellulose utilization by the straw mushroom Volvariella volvacea. Mol. Gen. Genet. 261: 985- 993. https://doi.org/10.1007/s004380051047
  14. Kajisa, T., K. Igarahi, and M. Samejima. 2009. The genes encoding glycoside hydrolase family 6 and 7 cellulases from the brown-rot fungus Coniphora puteana. J. Wood Sci. 55: 376- 380. https://doi.org/10.1007/s10086-009-1042-4
  15. Koch, A., C. T. Weigel, and G. Schulz. 1993. Cloning, sequencing, and heterologous expression of a cellulase-encoding cDNA (cbh1) from Penicillium janthinellum. Gene 124: 57-65. https://doi.org/10.1016/0378-1119(93)90761-Q
  16. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680- 685. https://doi.org/10.1038/227680a0
  17. Lahjouji, K., R. Storms, Z. Xiao, K. B. Joung, Y. Zheng, J. Powlowski, A. Tsang, and L. Varin. 2007. Biochemical and molecular characterization of a cellobiohydrolase from Trametes versicolor. Appl. Microbiol. Biotechnol. 75: 337-346. https://doi.org/10.1007/s00253-006-0824-5
  18. Lee, C. C., D. W. Wong, and G. H. Robertson. 2001. Cloning and characterization of two cellulase genes from Lentinula edodes. FEMS Microbiol. Lett. 205: 355-360. https://doi.org/10.1111/j.1574-6968.2001.tb10972.x
  19. Li, Y. L., D. C. Li, and F. C. Teng. 2006. Purification and characterization of a cellobiohydrolase from the thermophilic fungus Chaetomium thermophilus CT2. Wei Sheng Wu Xue Bao 46: 143-146.
  20. Liete, R. S. R., E. Gomes, and R. Da-Silva. 2007. Characterization of $\beta$-glucosidases from a mesophilic Aureobasidium pullulana and thermophilic Thermoascus aurantiacus. Process Biochem. 42: 1101-1106. https://doi.org/10.1016/j.procbio.2007.05.003
  21. Limam, F., S. E. Chaabouni, R. Ghrir, and N. Marzouki. 1995. Two cellobiohydrolases of Penicillium occitanis mutant Pol 6: Purification and properties. Enzyme Microb. Technol. 17: 340- 346. https://doi.org/10.1016/0141-0229(94)00033-6
  22. Lin, J., B. Pillay, and S. Singh. 1999. Purification and biochemical characterization of $\beta$-glucosidase from a thermophilic fungus, Thermomyces lanuginosus. Biotechnol. Appl. Biochem. 30: 81- 87.
  23. Miller, G. L. 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31: 426-428. https://doi.org/10.1021/ac60147a030
  24. Ohnishi, Y., M. Nagase, T. Ichiyanagi, Y. Kitamoto, and T. Aimi. 2007. Transcriptional regulation of two cellobiohydrolase encoding genes (cel1 and cel2) from the wood-degrading basidiomycete Polyporus arcularius. Appl. Microbiol. Biotechnol. 76: 1069-1078. https://doi.org/10.1007/s00253-007-1090-x
  25. Percival Zhang, Y. H., M. E. Himmel, and J. R. Mielenz. 2006. Outlook for cellulase improvement: Screening and selection strategies. Biotechnol. Adv. 24: 452-481. https://doi.org/10.1016/j.biotechadv.2006.03.003
  26. Wolfe, R. S., R. K. Thauer, and N. Pfennig. 1987. A capillary racetrack method for isolation of magnetotactic bacteria. FEMS Microbiol. Lett. 45: 31-35. https://doi.org/10.1111/j.1574-6968.1987.tb02335.x
  27. Rouau, X. and E. Odier. 1986. Purification and properties of 2 enzymes from Duchomitus squalens which exhibit both cellobiohydrolase and xylanase activity. Carbohydr. Res. 145: 279-292. https://doi.org/10.1016/S0008-6215(00)90435-X
  28. Schmidhalter, D. R. and G. Canevascini. 1993. Purification and characterization of two exo-cellobiohydrolases from the brownrot fungus Coniophora puteana (Schum ex Fr) Karst. Arch. Biochem. Biophys. 300: 551-558. https://doi.org/10.1006/abbi.1993.1076
  29. Teeri, T. T. 1997. Crystalline cellulose degradation: New insight into the function of cello-biohydrolases. Trends Biotechnol. 15: 160-167. https://doi.org/10.1016/S0167-7799(97)01032-9
  30. Teeri, T. T., P. Lehtovaara, S. Kauppinen, I. Salovuori, and J. Knowles. 1987. Homologous domains in Trichoderma reesei cellulolytic enzymes: Gene sequence and expression of cellobiohydrolase II. Gene 51: 43-52. https://doi.org/10.1016/0378-1119(87)90472-0
  31. Tuohy, M. G., D. J. Walsh, P. G. Murray, M. Claeyssens, M. M. Cuffe, A. V. Savage, and M. P. Coughlan. 2002. Kinetic parameters and mode of action of the cellobiohydrolases produced by Talaromyces emersonii. Biochim. Biophys. Acta 1596: 366-380. https://doi.org/10.1016/S0167-4838(01)00308-9
  32. White, T. J., T. Bruns, S. Lee, and J. Taylor. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, pp. 315-322. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White (eds.). PCR Protocols: A Guide to Methods and Applications Academic Press, Inc., New York, NY.

Cited by

  1. Cloning and Sequence Analysis of the Cellobiohydrolase I Genes from Some Basidiomycetes vol.40, pp.2, 2012, https://doi.org/10.5941/myco.2012.40.2.107
  2. Redefining XynA from Penicillium funiculosum IMI 378536 as a GH7 cellobiohydrolase vol.39, pp.11, 2012, https://doi.org/10.1007/s10295-012-1166-1
  3. Purification and Characterization of a Novel ${\beta}$-1,3/1,4-glucanase from Sistotrema brinkmannii HQ717718 vol.56, pp.3, 2011, https://doi.org/10.1007/s13765-013-3028-6
  4. Characterization of a novel xylanase from Armillaria gemina and its immobilization onto SiO2 nanoparticles vol.97, pp.3, 2013, https://doi.org/10.1007/s00253-012-4381-9
  5. Structural characterization of a unique marine animal family 7 cellobiohydrolase suggests a mechanism of cellulase salt tolerance vol.110, pp.25, 2011, https://doi.org/10.1073/pnas.1301502110
  6. Plant-Polysaccharide-Degrading Enzymes from Basidiomycetes vol.78, pp.4, 2014, https://doi.org/10.1128/mmbr.00035-14
  7. Characterization of Lignocellulolytic Enzymes from White-Rot Fungi vol.70, pp.4, 2015, https://doi.org/10.1007/s00284-014-0743-0
  8. Screening of new secretory cellulases from different supernatants of white rot fungi from Misiones, Argentina vol.8, pp.1, 2011, https://doi.org/10.1080/21501203.2016.1267047
  9. Optimization of cellobiohydrolase production and secretome analysis of Trametes villosa LBM 033 suitable for lignocellulosic bioconversion vol.26, pp.1, 2011, https://doi.org/10.1080/25765299.2019.1598107
  10. Characterization of two GH5 endoglucanases from termite microbiome using synthetic metagenomics vol.104, pp.19, 2011, https://doi.org/10.1007/s00253-020-10831-5