Insect cellulolytic enzymes: Novel sources for degradation of lignocellulosic biomass
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Abstract
Alternative and renewable fuels derived from lignocellulosic biomass offer the potential to reduce our dependence on fossil fuels and mitigate global climate change. Cellulose is one of the major structural components in all lignocellulosic wastes and enzymatic depolymerization of cellulose by cellulases is an essential step in bio-ethanol production. Wood-degrading insects are potential source of biochemical catalysts for converting wood lignocellulose into biofuels. Cellulose digestion has been demonstrated in more than 20 insect families representing ten distinct insect orders. Termite guts been have considered as the “world’s smallest bioreactors” since they digest a significant proportion of cellulose (74-99%) and hemicellulose (65-87%) components of lignocelluloses they ingest. The lower termites harbor protistan symbionts in hindgut whereas higher termites lack these in the hind gut. Studies on cellulose digestion in termites and other insects with reference to ligno-cellulose degrading enzymes have been well focused in this review. The studies on insect cellulolytic systems can lead to the discovery of a variety of novel biocatalysts and genes that encode them, as well as associated unique mechanisms for efficient biomass conversion into biofuels.
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Keywords
Bioethanol, Insect cellulases, Lignocellulosic biomass, Sustainable energy, Termites
References
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Brown, R.M. Jr. and Saxena, I.M. (2000). Cellulose biosynthesis: a model for understanding the assembly of biopolymers. Plant Physiol Biochem 38: 57-67.
Brune, A. (1998). Termite guts: the world’s smallest bioreactors. Trends Biotechnol 16: 16?21.
Coughlan, M.P. and Ljungdahl, L.G. (1988). Comparative biochemistry of fungal and bacterial cellulolytic enzyme system. pp. 11–30. In: J.P. Aubert, P. Beguin and J. Millet (eds.) FEMS Symposium No. 43, Biochemistry and Genetics of Cellulose Degradation. Academic Press, London.
Delalibera, I. Jr., Handelsman, J. and Raffa, K.F. (2005). Contrasts in cellulolytic activities of gut microorganisms between the wood borer, Saperda vestita (Coleoptera: Cerambycidae), and the bark beetles, Ips pini and Dendroctonus frontalis (Coleoptera: Curculionidae). Physiol Ecol 34: 541-47.
Douglas, A.E. (2009). The microbial dimension in insect nutritional ecology. Funct Ecol 23: 38-47.
Duff, S.J.B. and Murray, W.D. (1996). Bioconversion of forest products industry waste cellulosics to fuel ethanol: a review. Biores Technol 55: 1-33.
Fischer, R., Ostafe, R. and Twyman, R.M. (2013). Cellulases from insects. Adv Biochem Eng Biotechnol 136: 51-64.
Franco Cairo, J.P.L., Leonardo, F.C., Alvarez, T.M., Ribeiro, D.A., Büchli, F., Costa-Leonardo, A.M., Carazzolle, M.F., Costa, F.F., Paes L., Adriana F., Pereira, G.A.G. and Squina, F.M. (2011). Functional characterization and target discovery of glycoside hydrolases from the digestome of the lower termite Coptotermes gestroi. Biotechnol Biofuels 4: 50.
Fry, S.C. (1995). Polysaccharide-modifying enzymes in the plant cell wall. Ann Rev Pl Physiol Pl Mol Biol 46: 497-520.
Geib, S.M., Tien, M. and Hoover, K. (2010). Identification of proteins involved in lignocellulose degradation using in gel zymogram analysis combined with mass spectros-copy-based peptide analysis of gut proteins from larval Asian longhorned beetles, Anoplophora glabripennis. Insect Sci 17: 253-64.
Gokcol, C., Dursun, B., Alboyaci, B. and Sunan, E. (2009). Importance of biomass energy as alternative to other sources in Turkey. Energy Policy 37: 424-31.
Huang, S.W., Zhang, H.Y., Marshall, S. and Jackson, T.A. (2010). The scarab gut: Apotential bioreactor for bio-fuel production. Insect Sci 17: 175-83.
Kim, N., Choo, Y.M., Lee, K.S., Hong, S.J., Seol, K.Y., Je, Y.H., Sohn, H.D. and Jin, B.R. (2008). Molecular cloning and characterization of a glycosyl hydrolase family 9 cellulase distributed throughout the digestive tract of the cricket Teleogryllus emma. Comp Biochem Physiol 150: 368-76.
Kukor, J.J. and Martin, M.M. (1986). Cellulose digestion in Monochamus marmorator by (Coleoptera: Cerambycidae): role of acquired fungal enzymes. J Chem Ecol 12: 1057-70.
Lee, S., Kim, S.R., Yoon, H.J., Kim, I., Lee, K.S., Je, Y.H., Lee, S.M., Seo, S.J., Sohn, H.D. and Jin, B.R. (2004). cDNA cloning, expression, and enzymatic activity of a cellulase from the mulberry longicorn beetle, Apriona germari. Comp Biochem Physiol 139: 107-16.
Lee, S.J., Lee, K.S., Kim, S.R., Gui, Z.Z., Kim, Y.S., Yoon, H.J., Kim, I., Kang, P.D., Sohn, H.D. and Jin, B.R. (2005). A novel cellulase gene from the mulberry longicorn beetle, Apriona germari: gene structure, expression, and enzymatic activity. Comp Biochem Physiol 140: 551-60.
Li, Xing-hua, Yang, Hua-jun, Roy, B., Wang, D., Yue, Wan-fu., Jiang, Li-jun., Park, E.Y. and Miao, Yun-gen. (2009). The most stirring technology in future: Cellulase enzyme and biomass utilization. Afr J Biotechnol 8: 2418-22.
Lynd, L.R., Cushman, J.H., Nichols, R.J. and Wyman, C.E. (1991). Fuel ethanol from cellulosic biomass. Science 251: 1318.
Lynd, L.R., Laser, M.S., Bransby, D., Dale, B.E., Davison, B., Hamilton, R., Himmel, M., Keller, M., McMillan, J.D., Sheehan, J. and Wyman, C.E. (2008). How biotech can transform biofuels. Nature Biotechnol 26: 169-172.
Lynd, L.R., Weimer, P.J., van Zyl, W.H. and Pretorius, I.S. (2002). Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66(3): 506-77.
Moran, N.A. (2006). Symbiosis. Curr Biol 16: 866-71.
Naik, S.N., Goud, V.V., Rout, P.K. and Dalai, A.K. (2010). Production of first and second generation biofuels: a comprehensive review. Renew Sust Energ Rev 14: 578-97.
Nakashima, K., Watanabe, H., Saitoh, H., Tokuda, G. and Azuma, J.I. (2002). Dual cellulose-digesting system of the wood-feeding termite, Coptotermes formosanus Shiraki. Insect Biochem Mol Biol 32: 777-84.
Ohkuma, M. (2003). Termite symbiotic systems: efficient biorecycling of lignocelluloses. Appl Microbiol Biotechnol 61: 1-9.
Oppert, C., Klingeman, W.E., Willis, J.D., Oppert, B. and Jurat-Fuentes, J.L. (2010). Prospecting for cellulolytic activity in insect digestive fluids. Comp Biochem Physiol - Part B 155: 145-54.
Rogers, T.E. and Doran-Peterson, J. (2010). Analysis of cellulolytic and hemicellulolytic enzyme activity within the Tipula abdominalis (Diptera: Tipulidae) larval gut and characterization of Crocebacterium ilecola gen. nov. sp. nov., isolated from the Tipula abdominalis larval hindgut. Insect Sci 17: 291-302.
Saha, B.C. (2003). Hemicellulose bioconversion. J Ind Microbiol Biotechnol 30(5): 279-91.
Scharf, M.E. and Tartar, A. (2008). Termite digestomes as sources for novel lignocellulases. Biofuels Bioprod Bioref 2: 540-52.
Schmer, M.R., Vogel, K.P., Mitchell, R.B. and Perrin, R.K. (2008). Net energy of cellulosic ethanol from switchgrass. Proc Nat Acad Sci USA 105: 464-69.
Scrivener, A.M., Slaytor, M. and Rose, H.A. (1989). Symbiont-independent digestion of cellulose and starch in Panesthia cribrata Saussure, an Australian wood-eating cockroach. J. Insect Physiol 35(12): 935-41.
Su, L.J., Zhang, H.F., Yin, X.M., Chen, M., Wang, F.Q., Xie, H., Zhang, G.Z. and Song, A.D. (2013). Evaluation of cellulolytic activity in insect digestive fluids. Genet Mol Res 12(3): 2432-41.
Sun, J.Z. and Scharf, M.E. (2010). Exploring and integrating cellulolytic systems of insects to advance biofuel technology. Insect Sci 17: 163-65.
Sun, Y. and Cheng, J. (2002). Hydrolysis of lignocellulosic materials for ethanol production: a review. Biores Technol 83: 1-11.
Tokuda, G. and Watanabe, H. (2007). Hidden cellulases in termites: revision of an old hypothesis. Biol Lett 3: 336-39.
Tartar, A., Wheeler, M.M., Zhou, X., Coy, M.R., Boucias, D.G. and Scharf, M.E. (2009). Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite Reticulitermes flavipes. Biotech Biofuels 2: 25
Tokuda, G., Lo, N. and Watanabe, H. (2005). Marked variations in patterns of cellulase activity against crystalline- vs carboxymethyl-cellulose in the digestive systems of diverse, wood-feeding termites. Physiol. Entomol 30: 372–80.
Treves, D.S. and Martin, M.M. (1994). Cellulose digestion in primitive hexapods: Effect of ingested antibiotics on gut microbial populations and gut cellulase levels in the firebrat, Thermobia domestica (Zygentoma, Lepismatidae). J Chem Ecol 20(8): 2003-20.
Warnecke, F., Luginbühl, 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., Hernández, 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. and Leadbetter, J.R. (2007). Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450 (7169): 560-65.
Watanabe, H. and Tokuda, G. (2010). Cellulolytic systems in insects. A cellulase gene of termite origin. Ann Rev Entomol 55: 609-32.
Watanabe, H., Noda, H., Nakamura, M., Tokuda, G. and Lo, N. (1998). A cellulase gene of termite origin. Nature 394: 330-31.
Wei, Y.D., Lee, K.S., Gui, Z.Z., Yoon, H.J., Kim, I., Zhang, G.Z., Guo, X., Sohn, H.D. and Jin, B.R. (2006). Molecular cloning, expression, and enzymatic activity of a novel endogenous cellulose from the mulberry longicorn beetle, Apriona germari. Comp Biochem Physiol 145: 220-29.
Wenzel, M., Schonig, I., Berchtold, M., Kampfer, P. and Konig, H. (2002). Aerobic and facultatively anaerobic cellulolytic bacteria from the gut of the termite Zootermopsis angusticollis. J Appl Microbiol 92: 32-40.
Willis, J.D., Oppert, C. and Jurat-Fuentes, J.L. (2010). Methods for discovery and characterization of cellulolytic enzymes from insects. Insect Sci 17: 184-98.
Zhou, X., Smith, J.A., Oi, F.M., Koehler, P.G., Bennett, G.W. and Scharf, M.E. (2007). Correlation of cellulase gene expression and cellulolytic activity throughout the gut of the termite Reticulitermes flavipes. Gene 395: 29-39.
Brown, R.M. Jr. and Saxena, I.M. (2000). Cellulose biosynthesis: a model for understanding the assembly of biopolymers. Plant Physiol Biochem 38: 57-67.
Brune, A. (1998). Termite guts: the world’s smallest bioreactors. Trends Biotechnol 16: 16?21.
Coughlan, M.P. and Ljungdahl, L.G. (1988). Comparative biochemistry of fungal and bacterial cellulolytic enzyme system. pp. 11–30. In: J.P. Aubert, P. Beguin and J. Millet (eds.) FEMS Symposium No. 43, Biochemistry and Genetics of Cellulose Degradation. Academic Press, London.
Delalibera, I. Jr., Handelsman, J. and Raffa, K.F. (2005). Contrasts in cellulolytic activities of gut microorganisms between the wood borer, Saperda vestita (Coleoptera: Cerambycidae), and the bark beetles, Ips pini and Dendroctonus frontalis (Coleoptera: Curculionidae). Physiol Ecol 34: 541-47.
Douglas, A.E. (2009). The microbial dimension in insect nutritional ecology. Funct Ecol 23: 38-47.
Duff, S.J.B. and Murray, W.D. (1996). Bioconversion of forest products industry waste cellulosics to fuel ethanol: a review. Biores Technol 55: 1-33.
Fischer, R., Ostafe, R. and Twyman, R.M. (2013). Cellulases from insects. Adv Biochem Eng Biotechnol 136: 51-64.
Franco Cairo, J.P.L., Leonardo, F.C., Alvarez, T.M., Ribeiro, D.A., Büchli, F., Costa-Leonardo, A.M., Carazzolle, M.F., Costa, F.F., Paes L., Adriana F., Pereira, G.A.G. and Squina, F.M. (2011). Functional characterization and target discovery of glycoside hydrolases from the digestome of the lower termite Coptotermes gestroi. Biotechnol Biofuels 4: 50.
Fry, S.C. (1995). Polysaccharide-modifying enzymes in the plant cell wall. Ann Rev Pl Physiol Pl Mol Biol 46: 497-520.
Geib, S.M., Tien, M. and Hoover, K. (2010). Identification of proteins involved in lignocellulose degradation using in gel zymogram analysis combined with mass spectros-copy-based peptide analysis of gut proteins from larval Asian longhorned beetles, Anoplophora glabripennis. Insect Sci 17: 253-64.
Gokcol, C., Dursun, B., Alboyaci, B. and Sunan, E. (2009). Importance of biomass energy as alternative to other sources in Turkey. Energy Policy 37: 424-31.
Huang, S.W., Zhang, H.Y., Marshall, S. and Jackson, T.A. (2010). The scarab gut: Apotential bioreactor for bio-fuel production. Insect Sci 17: 175-83.
Kim, N., Choo, Y.M., Lee, K.S., Hong, S.J., Seol, K.Y., Je, Y.H., Sohn, H.D. and Jin, B.R. (2008). Molecular cloning and characterization of a glycosyl hydrolase family 9 cellulase distributed throughout the digestive tract of the cricket Teleogryllus emma. Comp Biochem Physiol 150: 368-76.
Kukor, J.J. and Martin, M.M. (1986). Cellulose digestion in Monochamus marmorator by (Coleoptera: Cerambycidae): role of acquired fungal enzymes. J Chem Ecol 12: 1057-70.
Lee, S., Kim, S.R., Yoon, H.J., Kim, I., Lee, K.S., Je, Y.H., Lee, S.M., Seo, S.J., Sohn, H.D. and Jin, B.R. (2004). cDNA cloning, expression, and enzymatic activity of a cellulase from the mulberry longicorn beetle, Apriona germari. Comp Biochem Physiol 139: 107-16.
Lee, S.J., Lee, K.S., Kim, S.R., Gui, Z.Z., Kim, Y.S., Yoon, H.J., Kim, I., Kang, P.D., Sohn, H.D. and Jin, B.R. (2005). A novel cellulase gene from the mulberry longicorn beetle, Apriona germari: gene structure, expression, and enzymatic activity. Comp Biochem Physiol 140: 551-60.
Li, Xing-hua, Yang, Hua-jun, Roy, B., Wang, D., Yue, Wan-fu., Jiang, Li-jun., Park, E.Y. and Miao, Yun-gen. (2009). The most stirring technology in future: Cellulase enzyme and biomass utilization. Afr J Biotechnol 8: 2418-22.
Lynd, L.R., Cushman, J.H., Nichols, R.J. and Wyman, C.E. (1991). Fuel ethanol from cellulosic biomass. Science 251: 1318.
Lynd, L.R., Laser, M.S., Bransby, D., Dale, B.E., Davison, B., Hamilton, R., Himmel, M., Keller, M., McMillan, J.D., Sheehan, J. and Wyman, C.E. (2008). How biotech can transform biofuels. Nature Biotechnol 26: 169-172.
Lynd, L.R., Weimer, P.J., van Zyl, W.H. and Pretorius, I.S. (2002). Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66(3): 506-77.
Moran, N.A. (2006). Symbiosis. Curr Biol 16: 866-71.
Naik, S.N., Goud, V.V., Rout, P.K. and Dalai, A.K. (2010). Production of first and second generation biofuels: a comprehensive review. Renew Sust Energ Rev 14: 578-97.
Nakashima, K., Watanabe, H., Saitoh, H., Tokuda, G. and Azuma, J.I. (2002). Dual cellulose-digesting system of the wood-feeding termite, Coptotermes formosanus Shiraki. Insect Biochem Mol Biol 32: 777-84.
Ohkuma, M. (2003). Termite symbiotic systems: efficient biorecycling of lignocelluloses. Appl Microbiol Biotechnol 61: 1-9.
Oppert, C., Klingeman, W.E., Willis, J.D., Oppert, B. and Jurat-Fuentes, J.L. (2010). Prospecting for cellulolytic activity in insect digestive fluids. Comp Biochem Physiol - Part B 155: 145-54.
Rogers, T.E. and Doran-Peterson, J. (2010). Analysis of cellulolytic and hemicellulolytic enzyme activity within the Tipula abdominalis (Diptera: Tipulidae) larval gut and characterization of Crocebacterium ilecola gen. nov. sp. nov., isolated from the Tipula abdominalis larval hindgut. Insect Sci 17: 291-302.
Saha, B.C. (2003). Hemicellulose bioconversion. J Ind Microbiol Biotechnol 30(5): 279-91.
Scharf, M.E. and Tartar, A. (2008). Termite digestomes as sources for novel lignocellulases. Biofuels Bioprod Bioref 2: 540-52.
Schmer, M.R., Vogel, K.P., Mitchell, R.B. and Perrin, R.K. (2008). Net energy of cellulosic ethanol from switchgrass. Proc Nat Acad Sci USA 105: 464-69.
Scrivener, A.M., Slaytor, M. and Rose, H.A. (1989). Symbiont-independent digestion of cellulose and starch in Panesthia cribrata Saussure, an Australian wood-eating cockroach. J. Insect Physiol 35(12): 935-41.
Su, L.J., Zhang, H.F., Yin, X.M., Chen, M., Wang, F.Q., Xie, H., Zhang, G.Z. and Song, A.D. (2013). Evaluation of cellulolytic activity in insect digestive fluids. Genet Mol Res 12(3): 2432-41.
Sun, J.Z. and Scharf, M.E. (2010). Exploring and integrating cellulolytic systems of insects to advance biofuel technology. Insect Sci 17: 163-65.
Sun, Y. and Cheng, J. (2002). Hydrolysis of lignocellulosic materials for ethanol production: a review. Biores Technol 83: 1-11.
Tokuda, G. and Watanabe, H. (2007). Hidden cellulases in termites: revision of an old hypothesis. Biol Lett 3: 336-39.
Tartar, A., Wheeler, M.M., Zhou, X., Coy, M.R., Boucias, D.G. and Scharf, M.E. (2009). Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite Reticulitermes flavipes. Biotech Biofuels 2: 25
Tokuda, G., Lo, N. and Watanabe, H. (2005). Marked variations in patterns of cellulase activity against crystalline- vs carboxymethyl-cellulose in the digestive systems of diverse, wood-feeding termites. Physiol. Entomol 30: 372–80.
Treves, D.S. and Martin, M.M. (1994). Cellulose digestion in primitive hexapods: Effect of ingested antibiotics on gut microbial populations and gut cellulase levels in the firebrat, Thermobia domestica (Zygentoma, Lepismatidae). J Chem Ecol 20(8): 2003-20.
Warnecke, F., Luginbühl, 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., Hernández, 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. and Leadbetter, J.R. (2007). Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450 (7169): 560-65.
Watanabe, H. and Tokuda, G. (2010). Cellulolytic systems in insects. A cellulase gene of termite origin. Ann Rev Entomol 55: 609-32.
Watanabe, H., Noda, H., Nakamura, M., Tokuda, G. and Lo, N. (1998). A cellulase gene of termite origin. Nature 394: 330-31.
Wei, Y.D., Lee, K.S., Gui, Z.Z., Yoon, H.J., Kim, I., Zhang, G.Z., Guo, X., Sohn, H.D. and Jin, B.R. (2006). Molecular cloning, expression, and enzymatic activity of a novel endogenous cellulose from the mulberry longicorn beetle, Apriona germari. Comp Biochem Physiol 145: 220-29.
Wenzel, M., Schonig, I., Berchtold, M., Kampfer, P. and Konig, H. (2002). Aerobic and facultatively anaerobic cellulolytic bacteria from the gut of the termite Zootermopsis angusticollis. J Appl Microbiol 92: 32-40.
Willis, J.D., Oppert, C. and Jurat-Fuentes, J.L. (2010). Methods for discovery and characterization of cellulolytic enzymes from insects. Insect Sci 17: 184-98.
Zhou, X., Smith, J.A., Oi, F.M., Koehler, P.G., Bennett, G.W. and Scharf, M.E. (2007). Correlation of cellulase gene expression and cellulolytic activity throughout the gut of the termite Reticulitermes flavipes. Gene 395: 29-39.
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Insect cellulolytic enzymes: Novel sources for degradation of lignocellulosic biomass. (2015). Journal of Applied and Natural Science, 7(2), 625-630. https://doi.org/10.31018/jans.v7i2.656
