DIGESTIVE SYSTEM OF WORKER TERMITE Coptotermes curvignathus HOLMGREN AND ITS CHEMICAL AND CELLULOLYTIC MICROBIAL PROPERTIES
Abstract
Termites are able to feed and digest wood efficiently through orchestration of host and microbial enzymes. This study was carried out to characterize the anatomy of the Coptotermes curvignathus digestive system as well as its chemistry and cellulolytic microbial properties. Coptotermes curvignathus has three main regions in their digestive system namely the foregut, midgut and hindgut. The length of foregut was the shortest and the hindgut was the longest compartment. There were seven Malpighian tubules attached at the junction between the midgut and the anterior hindgut. Based on gut metabolites analysis, uric acid was found to be the most concentrated compound in all gut compartments. Some cellulolytic microbes isolated from the C. curvignathus digestive system displayed ability to produce uric acid. The second most abundant compound was propionic acid. Other organic acids, antibiotic and antioxidant compounds such as salicylic acid, butyric acid, vancomycin hydrochloride, pyrocatechol, and quercetin were also found in the fluid of C. curvignathus. From antioxidant tests, hindgut fluid of C. curvignathus exhibited the highest antioxidant activities, followed by midgut and the foregut fluids had the lowest antioxidant activity. The result agrees with the metabolites analysis, where ascorbic acid was found mainly in hindgut. The isolation of uric acid producing microbes from the gut of C. curvignathus is quite encouraging for further cultivation-based investigations, which are important to improve our understanding of the functional interactions of the symbiotic microbes involved in the digestion of wood matter in termites.
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Ames, B.N., Cathcart, R., Schwiers, E. & Hochstein, P. 1981. Uric acid provides an antioxidant defense in humans against oxidant- and radical-caused aging and cancer: A hypothesis. Proceedings of the National Academy of Sciences of the United States of America 78(11): 6858–6862.
Berdy, J. 2005. Bioactive microbial metabolites. The Journal of Antibiotics 58(1): 1–26.
Breznak, J.A. & Brune, A. 1994. Role of microorganisms in the digestion of lignocelluloses by termites. Annual Reviews of Entomology 39: 453–487.
Brand-Williams, W., Cuvelier, M.E. &Berset, C. 1995. Use of a free radical method to evaluate antioxidant activity. LWT Food Science Technology 28:25–30.
Brune, A. 2013. Symbiotic associations between termites and prokaryotes. In Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E. & Thompson, F. (eds.). The Prokaryotes – Prokaryotic Biology and Symbiotic Associations, pp. 545–577. Heidelberg, Berlin: Springer.
Brune, A. & Friedrich, M. 2000. Microecology of the termite gut: structure and function on a microscale. Current Opinion in Microbiology 3: 263–269.
Brune, A., Miambi, E. & Breznak, J.A. 1995. Roles of oxygen and the intestinal microflora in the metabolism of lignin-derived phenylpropanoids and other monoaromatic compounds by termites. Applied and Environmental Microbiology 61(7): 2688–2695.
Chaudhary, H.S., Soni, B., Shrivastava, A.R. & Shrivastava, S. 2013. Diversity and versatility of actinomycetes and its role in antibiotic production. Journal of Applied Pharmaceutical Science 3(8 Supplement 1): S83–S94.
Coasta-Leonardo, A.M., Laranjo, L.T., Janei, V. & Haifig, I. 2013. The fat body of termites: Functions and stored materials. Journal of Insect Physiology 59: 577–587.
Dorman, H.J., Bachmayer, O., Kosar, M. & Hiltunen, R. 2004. Antioxidant properties of aqueous extracts from selected lamiaceae species grown in Turkey. Journal of Agricultural and Food Chemistry 52(4): 762–770.
Engel, P. & Moran, N.A. 2013. The gut miocrobiota of insects – diversity in structure and function. Federation of European Microbiological Societies Mircorbiology Reviews 37: 699–735.
Fujita, A., Hojo, M., Aoyagi, T., Hayashi, Y., Arakawa, G., Tokuda, G. & Watanabe, H. 2010. Details of the digestive system in the midgut of Coptotermes formosanus Shiraki. The Japan Wood Research Society 56: 222–226.
Geib, S.M., Filley, T.R., Hatcher, P.G., Hoover, K., Carlson, J.E., Jimenez-Gasco, M.D., Nakagawa-Izumi, A., Sleighter, R.L. & Tien, M. 2008. Lignin degradation in wood-feeding insects. PNAS 105(35): 12932–12937.
Geng, A., Cheng, Y., Wang, Y., Zhu, D., Le, Y., Wu, J, Xie, R, Yuan, J.S. & Sun, J. 2018. Transcriptome analysis of the digestive system of a wood-feeding termite (Coptotermes formosanus) revealed a unique mechanism for effective biomass degradation. Biotechnology for Biofuels 11: 24.
Godoy, M.C. 2004. Gut structure of two species of the neotropical genus Tauritermes Krishna (Isoptera: Kalotermitidae). Neotropical Entomoglogy 33(2): 163–167.
Hariprabowo, L.E., Raffiudin, R. & Prawasti, T.S. 2006. Alimentary canal anatomy and histology of the worker termite Neotermes bosei. Biotropia 13(2): 99–110.
Hoe, P.K., King, P.J. H, Ong K.H., Bong, C.F. & Mahadi, N.M. 2019. Laccases repertoire of a subterranean termite Coptotermes curvignthus Holmgren (Blattodea: Rhinotermitidae). Serangga 24 (2): 169-197.
Karl, Z.J. & Scharf, M.E. 2015. Effects of five diverse lignocellulosic diets on digestive enzymes biochemistry in the termite Reticulitermes flavipes. Archives of Insect Biochemistry and Physiology 90 (2): 89-103.
Katsumata, K.S., Jin, Z., Hori, K. & Iiyama, K. 2007. Structural changes in lignin of tropical woods during digestion by termite, Cryptotermes brevis. Journal of Wood Science 53: 419–426.
Ke, J., Laskar, D., Gao, D. & Chen, S. 2012. Advanced bio refinery in lower termite-effect of combined pretreatment during the chewing process. Biotechnology for Biofuels 5(1): 11.
Ke, J., Singh, D. & Chen, S. 2011. Aromatic compound degradation by the wood- feeding termite Coptotermes formosanus (Shiraki). International Biodeterioration & Biodegradation 65: 744–756.
Ke, J., Sun, J.Z., Nguyen, H.D., Singh, D., Lee, K.C., Beyenal, H. & Chen, S.L. 2010. In-situ oxygen profiling and lignin modification in guts of wood-feeding termites. Insect Science 17: 277–290.
Khucharoenphaisan, K., Sripairoj, H. & Sinma, K. 2012. Isolation and identification of actinomycetes from termite’s gut against human pathogen. Asian Journal of Animal and Veterinary Advances 7(1): 68–73.
King, P.J.H., Nor, M.M., Bong, J.C.F., Ong, K.H. & Osman, H. 2014. Bacterial microbiome of Coptotermes curvignathus Holmgren (Isoptera: Rhinotermitidae) reflects the co-evolution of species and dietary pattern. Insect Science 21: 584–596.
Kramer, K.J. & Seib, P.A. 1982. Ascorbic acid and the growth and development of insects. In Seib, P.A. & Tolbert, B.M. (eds.). Ascorbic Acid: Chemistry, Metabolism, and Uses. Advances in Chemistry Series No. 200, pp. 275–291. Washington D.C.: American Chemical Society.
Kudo, T. 2009. Termite-microbe symbiotic system and its efficient degradation of lignocelluloses. Bioscience, Biotechnology, and Biochemistry 73: 2561–2567.
Kwong, W.K., Mancenido, A.L. & Moran, N.A. 2017. Immune system stimulation by the native gut microbiota of honey bees. Royal Society Open Science 4: 170003.
Levine, D.P. 2006. Vancomycin: A history. Clinical Infectious Dieseases 42 (Supplement 1): S5–12.
Li, H., Lu, J. & Mo, J. 2012. Physiochemical lignocelluloses modification by the Formosan Subterranean termite Coptotermes Formosanus Shiraki (Isoptera: Rhinotermitidae) and its potential uses in the production of biofuels. BioResources 7(1): 675–685.
Mathews, M.C., Summers, C.B. & Felton, G.W. 1997. Ascorbate peroxidase: A novel antioxidant enzyme in insects. Archieves of Insect Biochemistry and Physiology 34: 57–68.
Matsuo, T. & Ishikawa, Y. 1999. Protective role of uric acid against photooxidative stress in the silkworm, Bombyx mori (Lepidoptera: Bombycidae). Japanese Society of Applied Entomology and Zoology 34(4): 481–484.
Moellering, R.C.Jr. 2006. Vancomycin: A 50-year reassessment. Clinical Infectious Diseases 42 (Supplement 1): S3–4.
Nakashima, K., Watanabe, H., Saitoh, H., Tokuda, G. & Azuma, J.I. 2002. Dual cellulose-digesting system of the wood-feeding termite, Coptotermes formosanus Shiraki. Insect Biochemistry and Molecular Biology 32: 777–784.
Nocelli, R., Cintra-Socolowski, P., Roat, T., Silva-Zacarin, E. & Malaspina, O. 2016. Comparative physiology of Malpighian tubules: form and function. Open Access Insect Physiology 6:13-23.
Potrikus, C.J. & Breznak, J.A. 1980a. Anaerobic degradation of uric acid by gut bacteria of termites. Applied and Environmental Microbiology 40: 125–132.
Potrikus, C.J. & Breznak, J.A. 1980b. Uric acid in wood-eating termites. Insect Biochemistry 10: 19–27.
Potrikus, C.J. & Breznak, J.A. 1980c. Uric acid-degrading bacteria in guts of termites [Recticulitermes flavipes (Kollar)]. Applied and Environmental Microbiology 40(1): 117–124.
Potrikus, C.J. & Breznak, J.A. 1981. Gut bacteria recycle uric-acid nitrogen in termites – a strategy for nutrient conservation. Proceedings of the National Academy of Sciences of the United States of America 78: 4601–4605.
Ranković, B.R., Kosanić, M.M. & Stanojković, T.P. 2011. Antioxidant, antimicrobial and anticancer activity of the lichens Cladonia furcate, Lecanora atra and Lecanora muralis. BMC Complementary and Alternative Medicine 11: 97.
Rieu-Lesme, F., Dauga, C., Morvan, B., Bouvet, O.M.M., Grimont, P.A.D. & Dore, J. 1996. Acetogenic coccoid spore-forming bacteria isolated from the rumen. Research in Microbiology 147: 753–764.
Scharf, M.E. & Tartar, A. 2008. Termite digestomes as sources for novel lignocellulases. Biofuels, Bioproducts, and Biorefining 2: 540–552.
Schauer, C., Thompson, C.L. & Brune, A. 2012. The bacterial community in the gut of the cockroach Shelfordella lateralis reflects the close evolutionary relatedness of cockroaches and termites. Applied and Environmental Microbiology 78(8): 2758.
Schultz, J.E. & Breznak, J.A. 1978. Heterotrophic bacteria present in hindguts of wood-eating termites [Recticulitermes flavipes (Kollar)]. Applied and Environmental Microbiology 35(5): 930–936.
Schultz, J.E. & Breznak, J.A. 1979. Cross-feeding of lactate between Streptococcus lactis and Bacteroides sp. isolated from termite hindguts. Applied and Environmental Microbiology 37(6): 1206–1210.
Tartar, A., Wheeler, M.M., Zhou, X., Coy, M.R., Boucias, D.G. & Scharf, M.E. 2009. Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite Reticulitermes flavipes. Biotechnology for Biofuel 2: 25.
Tasaki, E., Sakurai, H., Nitao, M., Matsuura, K. & Iuchi, Y. 2017. Uric acid, an important antioxidant contributing to survival in termites. PLoS ONE12 (6): e0179426.
Teather, R.M., & Wood, P.J. 1982. Use of Congo red-polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rumen. Applied and environmental microbiology 43(4): 777–780.
Terra, W.R. & Ferreira, C. 1994. Insect digestive enzymes: properties, compartmentalization and function. Comparative Biochemistry and Physiology 109B: 1–62.
Terra, W.R. & Ferreira, C. 2012. Biochemistry and molecular biology of digestion. In Gilbert, L.I., Iatrou, K. & Gill, S.S. (eds.). Comprehensive Molecular Insect Science. Vol. 4, pp. 171–224. Elsevier: Oxford, UK.
Thapa, R.S. 1982. Termites of Sabah (East Malaysia). Sabah Forest Record 12: 1–374.
Tho, Y.P. 1992. Termites of Peninsular Malaysia. Malayan Forest Records No. 36. Kuala Lumpur: Forest Research Institute of Malaysia.
Tian, J.H., Pourcher, A.M. & Bouchez, T. 2014. Occurrence of lignin degradation genotypes and phenotypes among prokaryotes. Applied Microbiology and Biotechnology 98: 9527–9544.
Tokuda, G., Nakamura, T., Murakami, R. & Yamaoka, I. 2001. Morphology of the digestive system in the wood-feeding termite Nasutitermes takasagoensis(Shiraki) [Isoptera: Termitidae]. Zoological Science 18: 869–877.
Tokuda, G., Yamaoka, I. & Noda, H. 2000. Localization of symbiotic Clostridia in the mixed segment of the termite Nasutitermes takasagoensis (Shiraki). Applied and Enviromental Microbiology 66(5): 2199–2207.
Upadhyay, R.K. 2011. Symbiotic and non-symbiotic micro flora of termite gut: A unique nonhuman agricultural system that can recycle photo-synthetically fixed carbon and nutrients. Journal of Pharmacy Research 4(4): 1161–1166.
Veliká, B. & Kron, I. 2013. Antioxidant properties of phenols against superoxide radicals. Chemical Monthly 144: 1287–1290.
Watanabe, H. & Tokuda, G. 2010. Cellulolytic systems in insects. Annual Review of Entomology 55: 609–632.
Wu, Y.R. & He, J. 2013. Characterization of anaerobic consortia coupled lignin depolymerization with biomethane generation. Bioresource Technology 139: 5–12.
Zhang, D., Lax, A.R., Bland, J.M. & Allen, A.B. 2011. Characterization of a new endogenous endo--1,4-glucanase of Formosan subterranean termite (Coptotermes formosanus). Insect Biochemistry and Molecular Biology 41:211–218.
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