Abstract
Cellulases, as environmentally appropriate catalysts specifically acting on cellulosic substrates, are important for the industrial conversion of lignocellulose and modification of cellulose products. After decades of research, a fundamental understanding of cellulase-mediated hydrolysis of cellulose is that its ability to processively act as a key for the complete enzymatic hydrolysis of natural crystalline cellulose. Two types of processive cellulases are known: exoglucanases and processive endoglucanases. Exoglucanases are typical processive enzymes, and they have been studied in detail so that their modes of action and mechanisms are reasonably well characterized. Conversely, endoglucanases are less well characterized because of the non-universality and structural diversity. However, processive endoglucanases have certain characteristics that exoglucanases lack such as hydrolysis product diversity and independent hydrolyze natural crystalline cellulose. Therefore, besides the conversion of cellulose to monosaccharide, they might be useful for modification of fibrous substrates and preparation of cellulose oligosaccharides. Herein, we review in detail the sources, hydrolysis products, application, and possible hydrolysis mechanisms of processive endoglucanases.
Similar content being viewed by others
References
Kargarzadeh, H., Mariano, M., Gopakumar, D., Ishak, A., Thomas, S., Dufresne, A., Huang, J., & Lin, N. (2018). Advances in cellulose nanomaterial. Cellulose, 25(4), 2151–2189.
Charreau, H., Foresti, M. L., & Vazquez, A. (2013). Nanocellulose patents trends: a comprehensive review on patents on cellulose nanocrystals, microfibrillated and bacterial cellulose. Recent Patents on Nanotechnology, 7(1), 56–80.
Bhat, M. K. (2000). Cellulases and related enzymes in biotechnology. Biotechnology Advances, 18(5), 355–383.
Anoop, K. V., Suresh, C. K. R., Snishamol, C., & Nagendra, P. G. (2019). Role of cellulases in food, feed, and beverage industries. In Green bio-processes. energy, environment, and sustainability. Singapore: Springer.
Bauer, F., Coenen, L., Hansen, T., McCormick, K., & Palgan, Y. V. (2017). Technological innovation systems for biorefineries: a review of the literature. Biofuels, Bioproducts and Biorefining, 11(3), 534–548.
Menon, V., & Rao, M. (2012). Trends in bioconversion of lignocellulose: biofuels, platform chemicals and biorefnery concept. Progress in Energy and Combustion Science, 38(4), 522–550.
Obeng, E. M., Adam, S. N. N., Budiman, C., Ongkudon, C. M., Maas, R., & Joachim, J. (2017). Lignocellulases: a review of emerging and developing enzymes, systems, and practices, Bioresour. Bioprocess, 4, 16.
Hippel, V. P. H. (1994). Protein-DNA recognition: new perspectives and underlying themes. Science, 263(5148), 769–770.
Kipper, K., Väljamäe, P., & Johansson, G. (2005). Processive action of cellobiohydrolase Cel7A from Trichoderma reesei isrevealed as ‘burst’ kinetics on fluorescent polymeric model substrates. Biochem, 385(Pt2), 527–535.
Rouvinen, J., Bergfors, T., Teeri, T., Knowles, J. K., & Jones, T. A. (1990). Three dimensional structure of cellobiohydrolase II from Trichoderma reesei. Science, 249(4967), 380–386.
Karnaouri, A., Madhu, N. M., Dimarogona, M., Topakas, E., Rova, U., Sandgren, M., & Christakopoulos, P. (2017). Recombinant expression of thermostable processive MtEG5 endoglucanase and its synergism with MtLPMO from Myceliophthora thermophila during the hydrolysis of lignocellulosic substrates. Biotechnology for Biofuels, 10(1), 126–143.
Asha, P., Jose, D., & Singh, B. I. S. (2016). Purification and characterisation of processive-type endoglucanase and β-glucosidase from Aspergillus ochraceus MTCC 1810 through saccharification of delignified coir pith to glucose. Bioresource Technology, 213, 245–248.
Chiriac, A. I., Pastor, F. I. J., Popa, V. I., Aflori, M., & Ciolacu, D. (2014). Changes of supramolecular cellulose structure and accessibility induced by the processive endoglucanase Cel9B from Paenibacillus barcinonensis. Cellulose, 21(1), 203–219.
Zhang, C., Wang, Y., Li, Z., Zhou, X., Zhang, W., Zhao, Y., & Lu, X. (2014). Characterization of a multi-function processive endoglucanase CHU_2103 from Cytophaga hutchinsonii. Applied Microbiology and Biotechnology, 98(15), 6679–6687.
Zhang K, Li W, Wang Y, Zheng Y, Tan Fang, Ma Xiao-Qing, Yao Li-Shan, Bayer E A, Wang L and Li Fu, Processive degradation of crystalline cellulose by a multimodular endoglucanase via a wirewalking mode. Biomacromolecules 19(5):1686–1696(2018).
Taylor, L. E., Henrissat, B., Coutinho, P. M., Ekborg, N. A., Hutcheson, S. W., & Weiner, R. A. (2006). Complete cellulase system in the marine bacterium Saccharophagus degradans strain 2-40T. Journal of Bacteriology, 188(11), 3849–3861.
Wu, B., Zheng, S., Pedroso, M. M., Guddat, L. W., Chang, S., He, B., & Schenk, G. (2018). Processivity and enzymatic mechanism of a multifunctional family 5 endoglucanase from Bacillus subtilis BS-5 with potential applications in the saccharification of cellulosic substrates. Biotechnology for Biofuels, 11(1), 20–34.
Cohen, R., Suzuki, M. R., & Hammel, K. E. (2005). Processive endoglucanase active in crystalline cellulose hydrolysis by the brown rot basidiomycete Gloeophyllum trabeum. Applied and Environmental Microbiology, 71(5), 2412–2417.
Kim, H. M., Lee, Y. G., Patel, D. H., Lee, K. H., Lee, D. S., & Bae, H. J. (2012). Characteristics of bifunctional acidic endoglucanase (Cel5B) from Gloeophyllum trabeum. Journal of Industrial Microbiology & Biotechnology, 39(7), 1081–1089.
Zheng, F., & Ding, S. (2013). processivity and enzymatic mode of a glycoside hydrolase family 5 endoglucanase from Volvariella volvacea. Applied and Environmental Microbiology, 79(3), 989–996.
Reverbel-Leroy, C., Pages, S., Belaich, A., Belaich, J. P., & Tardif, C. (1997). The processive endocellulase CelF, a major component of the Clostridium cellulolyticum cellulosome: purification and characterization of the recombinant form. Journal of Bacteriology, 179(1), 46–52.
Bronnenmeier, K., & Staudenbauer, L. W. (1990). Cellulose hydrolysis by a highly thermostable endo-1, 4-β-glucanase (Avicelase I) from Clostridium stercorarium. Enzyme and Microbial Technology, 12(6), 431–436.
Irwin, D. C., Spezio, M., Walker, L. P., & Wilson, D. B. (1993). Activity studies of eight purified cellulases: Specificity, synergism, and binding domain effects. Biotechnology and Bioengineering, 42(8), 1002–1013.
Gal, L., Gaudin, C., Belaich, A., Pages, S., Tardif, C., & Belaich, J. P. (1997). CelG from Clostridium cellulolyticum: A multidomain endoglucanase acting Efficiently on crystalline cellulose. Journal of Bacteriology, 179(21), 6595–6601.
Jeon, S. D., Yu, K. O., Kim, S. W., & Han, S. O. (2012). The processive endoglucanase EngZ is active in crystalline cellulose degradation as a cellulosomal subunit of Clostridium cellulovorans. New Biotechnology, 29(3), 366–372.
Zverlov, V. V., Schantz, N., & Schwarz, W. H. (2005). A major new component in the cellulosome of Clostridium thermocellum is a processive endo-β −1,4-glucanase producing cellotetraose. FEMS Microbiology Letters, 249(2), 353–358.
Ko, K. C., Han, Y., Choi, J. H., Geun-Joong, K., Seung-Goo, L., & Song, J. J. (2011). A novel bifunctional endo-/exo-type cellulose from an anaerobic ruminal bacterium. Applied Microbiology and Biotechnology, 89(5), 1453–1462.
Eriksson, K. E. L., Blanchette, R. A., & Ander, P. (1990). Microbial and enzymatic degradation of wood and wood components. Berlin: Springer-Verlag.
Mejia-Castillo, T., Hidalgo-Lara, M. E., Brieba, L. G., & Ortega-Lopez, J. (2008). Purification, characterization and modular organization of a cellulose-binding protein, CBP105, a processive β-1,4-endoglucanase from Cellulomonas flavigena. Biotechnology Letters, 30(4), 681–687.
Irwin, D. C., Shin, D. H., Zhang, S., Barr, B. K., Sakon, J., Karplus, P. A., & Wilson, D. B. (1998). Roles of the catalytic domain and two cellulose binding domains of Thermomonospora fusca E4 in cellulose hydrolysis. Journal of Bacteriology, 180(7), 1709–1714.
Chiriac, A. I., Cadena, E. M., Vidal, T., Torres, A. L., Diaz, P., & Pastor, F. I. (2010). Engineering a family 9 processive endoglucanase from Paenibacillus barcinonensis displaying a novel architecture. Applied Microbiology and Biotechnology, 86(4), 1125–1134.
Weiner, R. M., Taylor, L. E., Henrissat, B., Hauser, L., Land, M., Coutinho, P. M., Rancurel, C., Saunders, E. H., Longmire, A. G., Zhang, H. T., Bayer, E. A., Gilbert, H. J., Larimer, F., Zhulin, I. B., Ekborg, N. A., Lamed, R., Richardson, P. M., Borovok, I., & Hutcheson, S. (2008). Complete genome sequence of the complex carbohydrate-degrading marine bacterium, Saccharophagus degradans strain 2–40(T). PLoS Genetics, 4(5), e100087.
Watson, B. J., Zhang, H., Longmire, A. G., Moon, Y. H., & Hutcheson, S. W. (2009). Processive endoglucanases mediate degradation of cellulose by Saccharophagus degradans. Journal of Bacteriology, 191(18), 5697–5705.
Ghatge, S. S., Telke, A. A., Kang, S. H., Arulalapperumal, V., Keun-Woo, L., Govindwar, S. P., Um, Y., Oh, D. B., Shin, H. D., & Kim, S. W. (2014). Characterization of modular bifunctional processive endoglucanase Cel5 from Hahella chejuensis KCTC 2396. Applied Microbiology and Biotechnology, 98(10), 4421–4435.
Wu, S., Ding, S., Zhou, R., & Li, Z. (2007). Comparative characterization of a recombinant Volvariella volvacea endoglucanase I (EG1) with its truncated catalytic core (EG1-CM), and their impact on the bio-treatment of cellulose-based fabrics. Journal of Biotechnology, 130(4), 364–369.
Rouvinen, J., Bergfors, T., Teeri, T., Knowles, J. K., & Jones, T. A. (1990). Three-dimensional structure of cellobiohydrolase II from Trichoderma reesei. Science, 249(4967), 380–386.
Divne, C., Stahlberg, J., Reinikainen, T., Ruohonen, L., Pettersson, G., Knowles, J. K. C., Teeri, T. T., & Jones, A. (1994). The three-dimensional structure of the catalytic core of cellobiohydrolase I from Trichoderma reesei. Science, 265(5171), 524–528.
Li, Y., Irwin, D. C., & Wilson, D. B. (2007). Processivity, substrate binding, and mechanism of cellulose hydrolysis by Thermobi fidafusca Cel9A. Applied and Environmental Microbiology, 73(10), 3165–3172.
Sánchez, M. M., Fritze, D., Blanco, A., Spröer, C., Tindall, B. J., Schumann, P., Kroppenstedt, R. M., Diaz, P., & Pastor, F. I. J. (2005). Paenibacillus barcinonensis sp. nov., a xylanase-producing bacterium isolated from a rice field in the Ebro River delta. International Journal of Systematic and Evolutionary Microbiology, 55(2), 935–939.
Gilad, R., Rabinovich, L., Yaron, S., Bayer, A. E., Lamed, R., Gilbert, J. H., & Shoham, Y. (2003). CelI, a Noncellulosomal Family 9 Enzyme from Clostridium thermocellum, is a processive endoglucanase that degrades crystalline cellulose. Journal of Bacteriology, 185(1), 391–398.
Burstein, T., Shulman, M., Jindou, S., Petkun, S., Frolow, F., & Shoham, Y. (2009). Physical association of the catalytic and helper modules of a family-9 glycoside hydrolase is essential for activity. FEBS Letters, 583(5), 879–884.
Sakon, J., Irwin, D., Wilson, B. D., & Karplus, P. A. (1997). Structure and mechanism of endo/exocellulase E4 from Thermomonospora fusca. Nature Structural Biology, 4(10), 810–818.
Tormo, J., Lamed, R., Chirino, A. J., Morag, E., Bayer, E. A., Shoham, Y., & Steitz, T. A. (1996). Crystal structure of a bacterial family-III cellulose-binding domain: a general mechanism for attachment to cellulose. The EMBO Journal, 15(21), 5739–5751.
Jindou, S., Xu, Q., Kenig, R., Shoham, Y., Bayer, E. A., & Lamed, R. (2006). Novel architectural theme of family-9 glycoside hydrolases identified in cellulosomal enzymes of Acetivibrio cellulolyticus and Clostridium thermocellum. FEMS Microbiology Letters, 254(2), 308–316.
Oliveira, O. V., Freitas, L. C., Straatsma, T. P., & Lins, R. D. (2009). Interaction between the CBM of Cel9A from Thermobifida fusca and cellulose fibers. Journal of Molecular Recognition, 22(1), 38–45.
Zhou W, Irwin CD, Escovar-Kousen Jose, Wilson B, David K, Studies of Thermobifida fusca Cel9A active site mutant enzymes. Biochemistry 43(30): 9655–9663(2004).
Kataeva, I. A., Shah, A., West, L. T., Li, X. L., & Ljungdahl, L. G. (2002). The fibronectin type 3-like repeat from the Clostridium thermocellum cellobiohydrolase CbhA promotes hydrolysis of cellulose by modifying its surface. Applied and Environmental Microbiology, 68(9), 4292–4300.
Tomme, P., Kwan, E., Gilkes, N. R., Kilburn, D. G., & Warren, R. A. J. (1996). Characterization of CenC, an enzyme from Cellulomonas fimi with both endo- and exoglucanase activities. Journal of Bacteriology, 178(14), 4216–4223.
Haq, I. U., Akram, F., Khan, M. A., Hussain, Z., Nawaz, A., Iqbal, K., & Shah, A. J. (2015). CenC, a multidomain thermostable GH9 processive endoglucanase from Clostridium thermocellum: Cloning, characterization and saccharification studies. World Journal of Microbiology and Biotechnology, 31(11), 1–12.
Cohen, R., Jensen, K. A., Houtman, C. J., & Hammel, K. E. (2002). Significant levels of extracellular reactive oxygen species produced by brown rot basidiomycetes on cellulose. FEBS Letters, 531(3), 483–488.
Rättö, M., Ritschkoff, A. C., & Viikari, L. (1997). The effect of oxidative pretreatment on cellulose degradation by Poria placenta and Trichoderma reesei cellulases. Applied Microbiology and Biotechnology, 48(1), 53–57.
Parsiegla, G., Juy, M., Reverbel-Leroy, C., Tardif, C., Belaïch, J. P., Driguez, H., & Haser, R. (1998). The crystal structure of the processive endocellulase CelF of Clostridium cellulolyticum in complex with a thiooligosaccharide inhibitor at 2.0 Å resolution. The EMBO Journal, 17(19), 5551–5562.
Horn, S. J., Sørlie, M., Vårum, K. M., Väljamäe, P., & Eijsink, V. G. (2012). Measuring processivity. Methods in Enzymology, 510, 69–95.
Zhang, X. Z., Sathitsuksanoh, N., & Zhang, Y. H. P. (2010). Glycoside hydrolase family 9 processive endoglucanase from Clostridium phytofermentans: heterologous expression, characterization, and synergy with family 48 cellobiohydrolase. Bioresource Technology, 101(14), 5534–5538.
Fagerstam, L. G., & Pettersson, L. G. (1980). The 1,4-β-glucan cellobiohydrolase of Trichoderma reesei QM9414. FEBS Letters, 119(1), 97–100.
Henrissat, B., Driguez, H., Viet, C., & Schulein, M. (1985). Synergism of cellulases from Trichoderma reesei in the degradation of cellulose. Bio/Techno, 3(8), 722–726.
Violot, S., Aghajari, N., Czjzek, M., Feller, G., Sonan, G. K., Gouet, P., Gerday, C., Haser, R., & Receveur-Brechot, V. (2005). Structure of a full length psychrophilic cellulase from Pseudoalteromonas haloplanktis revealed by x-ray diffraction and small angle x-ray scattering. Journal of Molecular Biology, 348(5), 1211–1224.
Wu, S. S., Zhang, Y. M., Xu, S., Wu S. F. (2019). Processive action of glycoside hydrolase family 5 endoglucanase from Volvariella volvacea and its application in the preparation of nanofibers. 257th ACS National Meeting & Exposition, Orlando, USA, March 31-April 4, 2019.
Funding
This project was financially supported by the National Natural Science Foundation of China (no. 31470593, no. 31730106) and the Priority Academic Program Development of Jiangsu Higher Education Institutions.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Wu, S., Wu, S. Processivity and the Mechanisms of Processive Endoglucanases. Appl Biochem Biotechnol 190, 448–463 (2020). https://doi.org/10.1007/s12010-019-03096-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12010-019-03096-w