Abstract
In the past decade, a century of debate over whether termites produce their own cellulases has been resolved by the application of molecular genetic techniques. Cellulase genes were present in ancient bilaterian animals, and have been passed down to termites and many other invertebrate lineages over several hundred million years. Termites contain multiple endoglucanase gene copies, all of which come from glycosyl hydrolase family 9, but the roles of the different gene copies are not yet clear. Enzyme assays and RNAi experiments indicate that endogenous cellulases play a key role in termite metabolism. The overall contribution of these enzymes in members of the Termitidae (which lack cellulolytic flagellates) appears to be greater than in members of other families. A major shift in the site of expression of endoglucanases and β-glucosidases from the salivary glands to the midgut has occurred in some members of the speciose family Termitidae. Investigations into the roles of different members of the termite colony in digesting cellulose have begun, and have revealed major variations in the level of expression, including differences between different sized workers. In fungus-growers and soil-feeders, endogenous cellulases appear to be of relatively minor importance, but have nonetheless been retained in the genome.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Bayer EA, Chanzy H, Lamed R, Shoham Y (1998) Cellulose, cellulases and cellulosomes. Curr Opin Struct Biol 8:548–557
Béguin P, Aubert J (1994) The biological degradation of cellulose. FEMS Microbiol Rev 13:25–58
Biedermann W, Moritz P (1898) Beiträge zur vergeleichenden Physiologie der Verdauung. II. Uver ein celluloselödendes Enzyme im Leversecret der Schnecke (Helix pomatia). Pflüdg Arch Gem 73:219–287
Boyle PJ, Mitchell R (1978) Absence of microorganisms in crustacean digestive tracts. Science 200:1157–1159
Buscalioni L, Comes S (1910) La digestione delle membrane vegatali per opera dei conternuti nell ‘intestina dei termitidi e il problema, della simbiosi’. Atti Accad Gioenia Sci Nat Catania 3:1–16
Cleveland LR (1923) Symbiosis between termites and their intestinal protozoa. Proc Natl Acad Sci U S A 9:424–428
Cleveland LR, Hall SR, Saunders EP, Collier J (1934) The wood-feeding roach Cryptocercus, its protozoa, and the symbiosis between protozoa and roach. Mem Am Acad Sci 17:185–342
Davies G, Henrissat B (1995) Structures and mechanisms of glycosyl hydrolases. Structure 3:853–859
Davison A, Blaxter M (2005) Ancient origin of glycosyl hydrolase family 9 cellulase genes. Mol Biol Evol 22:1273–1284
Dehal P, Satou Y, Campbell RK et al (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167
Esenther GR, Kirk TK (1974) Catabolism of aspen sapwood in Reticulitermes flavipes. Ann Entomol Soc Am 67:989–991
Fujita A, Hojo M, Aoyagi T et al (2010) Details of the digestive system in the midgut of Coptotermes formosanus Shiraki. J Wood Sci 56:222–226
Fujita A, Miura T, Matsumoto T (2008) Differences in cellulose digestive systems among castes in two termite lineages. Physiol Entomol 33:73–82
Fujita A, Shimizu I, Abe T (2001) Distribution of lysozyme and protease, and amino acid concentration in the guts of a wood-feeding termite, Reticulitermes speratus (Kolbe): possible digestion of symbiont bacteria transferred by trophallaxis. Physiol Entomol 26:116–123
Grassi B, Sandias A (1893) The constitution and development of the society of termites: observations on their habits; with appendices on the parasitic protozoa of Termitidae, and on the Embiidae. Q J Microsc Sci 39:245–322
Hahn MW (2009) Distinguishing among evolutionary models for the maintenance of gene duplicates. J Hered 100:605–617
Henrissat B (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 280:309–316
Henrissat B, Davies G (1997) Structural and sequence-based classification of glycoside hydrolases. Curr Opin Struct Biol 7:637–644
Hungate RE (1947) Studies on cellulose fermentation: III. The culture and isolation for cellulose-decomposing bacteria from the rumen of cattle. J Bacteriol 53:631–645
Imms AD (1920) On the structure and biology of Archotermopsis, together with descriptions of new species of intestinal protozoa, and general observations on the Isoptera. Phil Trans R Soc Lond B 209:75–180
Lamberty M, Zachary D, Lanot R et al (2001) Insect immunity. Constitutive expression of a cysteine-rich antifungal and a linear antibacterial peptide in a termite insect. J Biol Chem 276:4085–4092
Lasker R, Giese AC (1956) Cellulose digestion in the silverfish Ctenolepisma lineata. J Exp Biol 33:542–553
Leidy J (1881) The parasites of the termites. J Acad Nat Sci Philadelphia III 8:425–447
Li L, Frohlich J, Pfeiffer P, Konig H (2003) Termite gut symbiotic archaezoa are becoming living metabolic fossils. Eukaryot Cell 2:1091–1098
Lo N, Tokuda G, Watanabe H et al (2000) Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr Biol 10:801–804
Lo N, Watanabe H, Sugimura M (2003) Evidence for the presence of a cellulase gene in the last common ancestor of bilaterian animals. Proc R Soc Lond B 270:S69–S72
Martin MM (1982) The role of ingested enzymes in the digestive processes of insects. In: Anderson JM, Rayner ADM, Walton DWH (eds) Invertebrate-microbial interactions. Cambridge University Press, Cambridge, pp 155–172
Martin MM (1991) The evolution of cellulose digestion in insects. Phil Trans R Soc Lond B 333:281–288
Martin MM, Martin JS (1978) Cellulose digestion in the midgut of the fungus-growing termite Macrotermes natalensis: the role of acquired digestive enzymes. Science 199:1453–1455
Matsuura K, Yashiro T, Shimizu K et al (2009) Cuckoo fungus mimics termite eggs by producing the cellulose-digesting enzyme β-glucosidase. Curr Biol 19:30–36
Nakashima K, Watanabe H, Saitoh H et al (2002) Dual cellulose-digesting system of the wood-feeding termite, Coptotermes formosanus Shiraki. Insect Biochem Mol Biol 32:777–784
Qiu-Ying H, Wei-Ping W, Rang-Yu M, Chao-Liang L (2008) Studies on feeding and trophallaxis in the subterranean termite Odontotermes formosanus using rubidium chloride. Entomol Exp Appl 129:210–215
Ray DL, Julian JR (1952) Occurrence of cellulase in Limnoria. Nature 169:32–33
Reinhard J, Kaib M (2001a) Food exploitation in termites: indication for a general feeding stimulating signal in labial gland secretion of Isoptera. J Chem Ecol 27:189–201
Reinhard J, Kaib M (2001b) Thin-layer chromatography assessing feeding stimulation by labial gland secretion compared to synthetic chemicals in the subterranean termite Reticulitermes santonensis. J Chem Ecol 27:175–187
Richmond PA (1991) Occurrence and functions of native cellulose. In: Haigler CH, Weimer PJ (eds) Biosynthesis and biodegradation of cellulose. Marcel Dekker Inc, New York, NY, pp 5–24
Sakon J, Irwin D, Wilson DB, Karplus PA (1997) Structure and mechanism of endo/exocellulase E4 from Thermomonospora fusca. Nat Struct Biol 4:810–818
Scharf ME, Wu-Scharf D, Zhou X et al (2005) Gene expression profiles among immature and adult reproductive castes of the termite Reticulitermes flavipes. Insect Mol Biol 14:31–44
Schulz MW, Slaytor M, Hogan ME, O’Brien RW (1986) Components of cellulase from the higher termite, Nasutitermes walkeri. Insect Biochem 16:929–932
Scrivener AM, Slaytor M (1994) Properties of the endogenous cellulase from Panesthia cribrata Saussure and purification of major endo-β-1,4-glucanase components. Insect Biochem Mol Biol 24:223–231
Scrivener AM, Slaytor M, Rose HA (1989) Symbiont-independent digestion of cellulose and starch in Panesthia cribrata Saussure, an Australian wood-eating cockroach. J Insect Physiol 35:935–941
Slaytor M (1992) Cellulose digestion in termites and cockroaches: what role do symbionts play? Comp Biochem Physiol 103B:775–784
Smant G, Stokkermans J, Yan YT et al (1998) Endogenous cellulases in animals: isolation of beta-1,4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc Natl Acad Sci U S A 95:4906–4911
Sugio K, Simojo K, Isozaki J et al (2006) Distribution of cellulase activities in the salivary glands and the guts of pseudoworkers and soldiers of the drywood-feeding termite Neotermes koshunensis (Shiraki) and the effect of defaunation. Jpn J Appl Entomol Zool 50:1–6
Suzuki K, Ojima T, Nishita K (2003) Purification and cDNA cloning of a cellulase from abalone Haliotis discus hannai. Eur J Biochem 270:771–778
Tamaru Y, Karita S, Ibrahim A et al (2000) A large gene cluster for the Clostridium cellulovorans cellulosome. J Bacteriol 182:5906–5910
Tokuda G, Lo N, Watanabe H et al (1999) Metazoan cellulase genes from termites: intron/exon structures and sites of expression. Biochim Biophys Acta 1447:146–159
Tokuda G, Lo N, Watanabe H et al (2004) Major alteration of the expression site of endogenous cellulases in members of an apical termite lineage. Mol Ecol 13:3219–3228
Tokuda G, Lo N, Watanabe H (2005) Marked variations in patterns of cellulase activity against crystalline- versus carboxymethyl-cellulose in the digestive systems of diverse, wood-feeding termites. Physiol Entomol 30:372–380
Tokuda G, Miyagi M, Makiya H et al (2009) Digestive β-glucosidases from the wood-feeding higher termite, Nasutitermes takasagoensis: intestinal distribution, molecular characterization, and alteration in sites of expression. Insect Biochem Mol Biol 39:931–937
Tokuda G, Saito H, Watanabe H (2002) A digestive beta-glucosidase from the salivary glands of the termite, Neotermes koshunensis (Shiraki): distribution, characterization and isolation of its precursor cDNA by 5′- and 3′-RACE amplifications with degenerate primers. Insect Biochem Mol Biol 32:1681–1689
Tokuda G, Watanabe H (2007) Hidden cellulases in termites: revision of an old hypothesis. Biol Lett 3:336–339
Tokuda G, Watanabe H, Matsumoto T, Noda H (1997) Cellulose digestion in the wood-eating higher termite, Nasutitermes takasagoensis (Shiraki): distribution of cellulases and properties of endo-β-1,4-glucanase. Zool Sci 14:83–93
Tomme P, Warren RA, Gilkes NR (1995) Cellulose hydrolysis by bacteria and fungi. Adv Micro Physiol 37:1–81
Watanabe H, Nakamura M, Tokuda G et al (1997) Site of secretion and properties of endogenous endo-beta-1,4-glucanase components from Reticulitermes speratus (Kolbe), a Japanese subterranean termite. Insect Biochem Mol Biol 27:305–313
Watanabe H, Noda H, Tokuda G, Lo N (1998) A cellulase gene of termite origin. Nature 394:330–331
Watanabe H, Takase A, Tokuda G et al (2006) Symbiotic ‘Archaezoa’ of the primitive termite Mastotermes darwiniensis still play a role in cellulase production. Eukaryot Cell 5:1571–1576
Watanabe H, Tokuda G (2010) Cellulolytic systems in insects. Annu Rev Entomol 55:609–632
Wood TG (1978) Feed and feeding habits of termites. In: Brian MV (ed) Production ecology of ants and termites. Cambridge University Press, New York, NY, pp 55–80
Yokoe Y (1964) Cellulose activity in the termite, Leucotermes speratus, with new evidence in support of a cellulase produced by the termite itself. Sci Pap Coll Gen Educ Univ Tokyo 14:115–120
Yokoe Y, Yasumasu I (1964) The distribution of cellulase in invertebrates. Comp Biochem Physiol 13:323–328
Yuki M, Moriya S, Inoue T, Kudo T (2008) Transcriptome analysis of the digestive organs of Hodotermopsis sjostedti, a lower termite that hosts mutualistic microorganisms in its hindgut. Zool Sci 25:401–406
Zachary A, Colwell RR (1979) Gut-associated microflora of Limnoria tripunctata in marine creosote-treated wood pilings. Nature 282:716–717
Zhou X, Wheeler MM, Oi FM, Scharf ME (2008) RNA interference in the termite Reticulitermes flavipes through ingestion of double-stranded RNA. Insect Biochem Mol Biol 38:805–815
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2010 Springer Netherlands
About this chapter
Cite this chapter
Lo, N., Tokuda, G., Watanabe, H. (2010). Evolution and Function of Endogenous Termite Cellulases. In: Bignell, D., Roisin, Y., Lo, N. (eds) Biology of Termites: a Modern Synthesis. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3977-4_3
Download citation
DOI: https://doi.org/10.1007/978-90-481-3977-4_3
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-90-481-3976-7
Online ISBN: 978-90-481-3977-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)