Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-22T20:08:13.909Z Has data issue: false hasContentIssue false

Biochemical and catalytic properties of two β-glycosidases purified from workers of the termite Macrotermes subhyalinus (Isoptera: Termitidae)

Published online by Cambridge University Press:  28 February 2007

Lucien Patrice Kouame*
Affiliation:
Laboratoire de Biochimie et Technologie des Aliments de l'Université d'Abobo-Adjamé, 22 BP 1297, Abidjan, 22, Côte d'Ivoire
Françoise Akissi Kouame
Affiliation:
Laboratoire de Biochimie et Technologie des Aliments de l'Université d'Abobo-Adjamé, 22 BP 1297, Abidjan, 22, Côte d'Ivoire
Sebastien Lamine Niamke
Affiliation:
Laboratoire de Biotechnologie de l'Université de Cocody, 22 BP 582, Abidjan, 22, Côte d'Ivoire
Betty Meuwia Faulet
Affiliation:
Laboratoire de Biochimie et Technologie des Aliments de l'Université d'Abobo-Adjamé, 22 BP 1297, Abidjan, 22, Côte d'Ivoire
Alphonse Kamenan
Affiliation:
Laboratoire de Biochimie et Technologie des Aliments de l'Université d'Abobo-Adjamé, 22 BP 1297, Abidjan, 22, Côte d'Ivoire
Get access

Abstract

Two β-glycosidases were purified from the termite Macrotermes subhyalinus (Rambur) workers by chromatography on gel filtration, ion exchange and hydrophobic interaction columns. The preparations were shown to be homogeneous on polyacrylamide gel. Both enzymes have a similar molecular mass (68 KDa) and optimum pH (5.4) but differ in optimal temperature and thermal stability. The β-glycosidases preferred β-fucosides to β-glucosides, β-galactosides and β-xylosides, and hydrolysed glucose-glucose-β-(1–4) linkages better than β-(1–3), β-(1–2) and β-(1–6) linkages. They did not hydrolyse saccharides such as melibiose, sucrose, lactose, xylobiose, melizitose, stachyose, lactose, raffinose, laminarin, arabinogalactan, carboxymethylcellulose, inulin, lichenan and starch. β-Glycosidase A and β-glycosidase B of M. subhyalinus workers are capable of catalysing transglucosylation reactions. The yields of glucosylation of hydroxyamino acid derivatives and phenylethanol, catalysed by the two enzymes in the presence of cellobiose as glucosyl donor, were lower than those reported previously with conventional sources of β-glycosidases. In addition, the optimum pH is different for the hydrolysis and transglucosylation reactions. On the basis of this work, it is proposed that the physiological role of β-glycosidase A and β-glycosidase B of M. subhyalinus workers is the digestion of di- and oligosaccharides derived from hemicelluloses and celluloses.

Type
Research Article
Copyright
Copyright © ICIPE 2005

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Azevedo, T. R., Terra, W. R., Ferreira, C. (2003) Purification and characterization of three beta-glycosidases from midgut of the sugar cane borer, Diatraea saccharalis. Insect Biochemistry and Molecular Biology 33, 8192.CrossRefGoogle ScholarPubMed
Breznak, J. A., Brune, A. (1994) Role of microorganisms in the digestion of lignocellulose by termites. Annual Review of Entomology 39, 453487.CrossRefGoogle Scholar
Brimer, L., Nout, M. J., Tuncel, G. (1998) Beta-glycosidase (amygdalase and linamarase) from Endomyces fibuliger (LU677): Formation and crude enzyme properties. Applied Microbiology and Biotechnology 49, 182188.CrossRefGoogle ScholarPubMed
Butler, J. H. A., Buckerfield, J. C. (1973) Digestion of lignin by termites. Soil Biology and Biochemistry 11, 507513.CrossRefGoogle Scholar
Cabezas, J. A., Reglero, A., Calvo, P. (1983) Glycosidases (fucosidases, galactosidases, glucosidases, hexosaminidases and glucuronidases) from some molluscs and vertebrates and neuraminidases from virus. International Journal of Biochemistry 15, 243259.CrossRefGoogle ScholarPubMed
Calvo, P., Santamaria, M. G., Melgar, M. J., Cabezas, J. A. (1983) Kinetic evidence for two active sites in β- d -fucosidase of Helicella ericetorum. International Journal of Biochemistry 15, 685693.CrossRefGoogle ScholarPubMed
Colas, B. (1980) Kinetic studies on β-fucosidases of Achatina balteata. Biochimica et Biophysica Acta 613, 448458.CrossRefGoogle ScholarPubMed
Colas, B., Attias, J. (1977) Purification of two β- d -glucosidases from the digestive juice of Achatina balteata. Biochimie 59, 577585.CrossRefGoogle Scholar
Cookson, L. J. (1992) Studies of lignin degradation in mound material of the termite Nasutitermes exitiosus. Australian Journal of Soil Research 30, 189193.CrossRefGoogle Scholar
D'Auria, S., Morana, A., Febbraio, F., Vaccaro, C. De, Rosa, M., Nucci, R. (1996) Functional and structural properties of the homogeneous beta-glycosidase from the extreme thermoacidophilic archaeon Sulfolobus solfataricus expressed in Saccharomyces cerevisiae. Protein Expression and Purification 7, 299308.CrossRefGoogle ScholarPubMed
D'Auria, S., Nucci, R., Rossi, M., Gryczynski, I., Gryczynski, Z., Lakowicz, J. R. (1999a) The beta-glycosidase from the hyperthermophilic archaeon Sulfolobus solfataricus: Enzyme activity and conformational dynamics at temperatures above 100 degrees C. Biophysical Chemistry 81, 2331.CrossRefGoogle ScholarPubMed
D'Auria, S., Nucci, R., Rossi, M., Bertoli, E., Tanfani, F., Gryczynski, I., Malak, H., Lakowicz, J. R. (1999) Beta-glycosidase from the hyperthermophilic archaeon Sulfolobus solfataricus: Structure and activity in the presence of alcohols. Journal of Biochemistry 126, 545552. (Tokyo)CrossRefGoogle ScholarPubMed
Dion, M., Fourage, L., Hallet, J. N., Colas, B. (1999) Cloning and expression of a beta-glycosidase gene from Thermus thermophilus. Sequence and biochemical characterization of the encoded enzyme. Glycoconjugate Journal 16, 2737.CrossRefGoogle ScholarPubMed
Ferreira, A. H., Marana, S. R., Terra, W. R., Ferreira, C. (2001) Purification, molecular cloning, and properties of a beta-glycosidase isolated from midgut lumen of Tenebrio molitor (Coleoptera) larvae. Insect Biochemistry and Molecular Biology 31, 10651076.CrossRefGoogle ScholarPubMed
Ferreira, A. H., Ribeiro, A. F., Terra, W. R., Ferreira, C. (2002) Secretion of beta-glycosidase by middle midgut cells and its recycling in the midgut of Tenebrio molitor larvae. Journal of Insect Physiology 48, 113118.CrossRefGoogle ScholarPubMed
Ferreira, A. H., Terra, W. R., Ferreira, C. (2003) Characterization of a beta-glycosidase highly active on disaccharides and of a beta-galactosidase from Tenebrio molitor midgut lumen. Insect Biochemistry and Molecular Biology 33, 253265.CrossRefGoogle ScholarPubMed
Fourage, L., Dion, M., Colas, B. (2000) Kinetic study of a thermostable β-glycosidase of Thermus thermophilus. Effects of temperature and glucose on hydrolysis and transglycosylation reactions. Glycoconjugate Journal 17, 377383.CrossRefGoogle ScholarPubMed
Gijsen, H. J. M., Quio, L., Fitz, W., Wong, C. H. (1996) Recent advances in the chemoenzymatic synthesis of carbohydrates and carbohydrate mimetics. Chemical Reviews 96, 443473.CrossRefGoogle ScholarPubMed
Grasse, P. P. (1982) Termitologia tome I: Anatomie, Physiologie, Reproduction des Termites. Masson, Paris. 676 pp.Google Scholar
Got, R., Marnay, A. (1968) Isolation, purification and some physicochemical characteristics of 2 β-hexosidases of the digestive juice of Helix pomatia. European Journal of Biochemistry 4, 240246.CrossRefGoogle ScholarPubMed
Heim, R. (1977) Termites et champignons. Boubée, Paris. 207 pp.Google Scholar
Henrissat, B. (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochemical Journal 280, 309316.CrossRefGoogle ScholarPubMed
Hosel, W. (1976) Purification and properties of two beta-glycosidases from Cicer arietinum L. with preferential specificity for biochanin A 7-beta-apiosylglucoside. Hoppe-Seyler's Zeitschrift für Physiologische Chemie 357, 16731681.Google ScholarPubMed
Hosel, W., Tober, I., Eklund, S. H., Conn, E. E. (1987) Characterization of beta-glucosidases with high specificity for the cyanogenic glucoside dhurrin in Sorghum bicolor (L.) Moench seedlings. Archives of Biochemistry and Biophysics 252, 152162.CrossRefGoogle ScholarPubMed
Huber, R. E., Gaunt, M. T., Sept, R. L., Babiak, M. J. (1983) Differences in the effects of pH on the hydrolytic and transgalactosylic reactions of β-galactosidases ( Escherichia coli ). Canadian Journal of Biochemistry and Cell Biology 61, 198206.CrossRefGoogle ScholarPubMed
Kouame, L. P., Niamkey, S., Diopoh, J., Colas, B. (2001) Transglycosylation reactions by exoglycosidases from the termite Macrotermes subhyalinus. Biotechnology Letters 23, 15751581.CrossRefGoogle Scholar
Kunst, A., Draeger, B., Ziegenhorn, J. (1984) Colorimetric methods with glucose oxidase and peroxidase, pp. 178185. In Methods of Enzymatic Analysis (Edited by Bergmeyer, H. U.). vol.6. Verlag Chemie, Weinheim.Google Scholar
Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T 4. Nature 227, 680685.CrossRefGoogle Scholar
Leparoux, S., Padrines, M., Placier, G., Colas, B. (1997) Characterization of a strictly specific acid β-galactosidase from Achatina achatina. Biochimica et Biophysica Acta 1336, 522532.CrossRefGoogle ScholarPubMed
Marana, S. R., Terra, W. R., Ferreira, C. (2000) Purification and properties of a beta-glycosidase purified from midgut cells of Spodoptera frugiperda (Lepidoptera) larvae. Insect Biochemistry and Molecular Biology 30, 11391146.CrossRefGoogle ScholarPubMed
Martin, M. M. (1991) The evolution of cellulose digestion in insects. Philosophical Transactions of the Royal Society of London 333, 281288.Google Scholar
Moracci, M., Nucci, R., Febbraio, F., Vaccaro, C., Vespa, N. La, Cara, F., Rossi, M. (1995) Expression and extensive characterization of a beta-glycosidase from the extreme thermoacidophilic archaeon Sulfolobus solfataricus in Escherichia coli: Authenticity of the recombinant enzyme. Enzyme and Microbial Technology 17, 992997.CrossRefGoogle ScholarPubMed
Mora, P., Rouland, C. (1994) Comparison of hydrolytic enzymes produced during growth on carbohydrate substrates by Termitomyces associates of Pseudacanthotermes spiniger and Microtermes subhyalinus (Isoptera: Termitidae). Sociobiology 26, 258262.Google Scholar
Morana, A., Moracci, M., Ottombrino, A., Ciaramella, M., Rossi, M. De, Rosa, M. (1995) Industrial-scale production and rapid purification of an archaeal beta-glycosidase expressed in Saccharomyces cerevisiae. Biotechnology and Applied Biochemistry 22, 261268.CrossRefGoogle ScholarPubMed
Nilsson, K. G. I. (1988) Enzymatic synthesis of oligosaccharides. Trends in Biotechnology 6, 256546.CrossRefGoogle Scholar
Nucci, R., Moracci, M., Vaccaro, C., Vespa, N., Rossi, M. (1993) Exo-glucosidase activity and substrate specificity of the beta-glycosidase isolated from the extreme thermophile Sulfolobus solfataricus. Biotechnology and Applied Biochemistry 17, 239250.CrossRefGoogle ScholarPubMed
Petrova, S. D., Bakalova, N. G., Bankova, E. D., Andonova, S. B., Kolev, D. N. (2003) Separation of enzymes from polyenzyme mixture used in medicine and pharmacy. II. Purification and characterization of extracellular beta-glycosidases with high transglycosylation activities from Aspergillus oryzae. Die Pharmazie 58, 6367.Google Scholar
Rouland, C. (1986) Contribution à l' étude des osidases digestives de plusieurs termites africains. These de Doctorat es sciences, Université Paris Val de Marne 210 pp.Google Scholar
Rouland, C., Brauman, A., Keleke, S., Labat, M., Mora, P., Renoux, J. (1990) Endosymbiosis and exosymbiosis in the fungus-growing termites: Microbiology of poecilotherms (Edited by Lesel, R.). Elsevier Science Publishers, 79 pp.Google Scholar
Rouland, C., Civas, A., Renoux, J., Petex, F. (1988) Purification and properties of cellulases from termite Macrotermes mulleri (Termitidae, Macrotermitinae) and its symbiotic fungus Termitomyces sp. Comparative Biochemistry and Physiology 91, 449458.Google Scholar
Rouland, C., Matoub, M., Mora, P., Petek, F. (1992) Properties of two β-glucosidases purified from the termite Macrotermes muelleri and from its symbiotic fungus Termitomyces sp. Carbohydrate Research 233, 273278.CrossRefGoogle Scholar
Sands, W. A. (1962) The evaluation of insecticides as soil and mound poisons against termites in agriculture and forestry in West Africa. Bulletin of Entomological Research 53, 179192.CrossRefGoogle Scholar
Sands, W. A. (1973) Termites as pests of tropical food crops. Paris 19, 167177.Google Scholar
Sands, W. A. (1977) The role of termites in tropical agriculture. Outlook on Agriculture 9, 136143.CrossRefGoogle Scholar
Slaytor, M. (1992) Cellulose digestion in termite and cockroaches: What role do symbionts play?. Comparative Biochemistry and Physiology 103, 775784.Google Scholar
Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gatner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J., Klenk, D. C. (1985) Measurements of protein using bicinchoninic acid. Analytical Biochemistry 150, 7685.CrossRefGoogle ScholarPubMed
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 Biochemistry and Molecular Biology 32, 16811689.CrossRefGoogle ScholarPubMed
Wong, C. H., Halcomb, R. L., Ichikawa, Y., Kajimoto, T. (1995) Enzymes in organic synthesis: Application to the problems of carbohydrate recognition (part 2). Angewandte Chemie (International Edition in English) 34, 521546.CrossRefGoogle Scholar
Wood, T. M., MacCrae, S. I. (1979) Synergism between enzymes involved in the solubilization of native cellulose, pp. 181209. In Hydrolysis of Cellulose: Mechanisms of Enzymatic and Acid Catalysis (Edited by Brown, R. D., Jurasek, L.). Ame. Soc. Washington.CrossRefGoogle Scholar
Xiangyuan, H., Shuzheng, Z., Shoujun, Y. (2001) Cloning and expression of thermostable beta-glycosidase gene from Thermus nonproteolyticus HG102 and characterization of recombinant enzyme. Applied Biochemistry and Biotechnology 94, 243255.CrossRefGoogle ScholarPubMed