Eur. J. Entomol. 106 (2): 185-191, 2009 | DOI: 10.14411/eje.2009.022

Purification and characterization of a novel thermoacidophilic and thermostable α-mannosidase from the digestive fluid of oil palm weevil Rhynchophorus palmarum (Coleoptera: Curculionidae) larvae

Micaël BÉDIKOU1, Pascal AHI2, Martial KONÉ3, Betty FAULET2, Jean GONNETY2, Patrice KOUAMÉ2, Sébastien NIAMKÉ*,1,2
1 Laboratoire de Biotechnologies, Filière Biochimie-Microbiologie de l'Unité de Formation et de Recherche en Biosciences de l'Université de Cocody-Abidjan, 22 BP 582 Abidjan 22, Côte d'Ivoire
2 Laboratoire de Biochimie et Technologie des Aliments de l'Unité de Formation et de Recherche en Sciences et Technologie des Aliments de l'Université d'Abobo-Adjamé, 02 BP 801 Abidjan 02, Côte d'Ivoire
3 Unité de Biotechnologie, Biocatalyse et Biorégulation, CNRS-UMR 6204, Laboratoire de Biochimie, Faculté des Sciences et Techniques, 2 Rue de la Houssinière, BP 92208, F-44322 Nantes Cedex 3, France

An extracellular α-mannosidase with unusual properties was purified from the digestive fluid of oil palm weevil (Rhynchophorus palmarum Linnaeus) larvae using ammonium sulphate saturation, size exclusion and anion-exchange chromatography. The enzyme named RpltM is thermoacidophilic, thermostable and behaves like lysosomal α-mannosidase (EC 3.2.1.24). The molecular weight, Km value, optimum reaction temperature and pH are 108-112 kDa, 0.36 mM, 65°C and 4.5, respectively. Zn2+ enhanced whereas Cu2+, Sodium dodecyl sulphate, swainsonine and 1,4-dideoxy-1,4-iminomannitol strongly inhibited its hydrolytic activity. The enzyme was stable for 25 min at 65°C and retained 70% of its initial activity after 60 min. At 70°C, around 60% of this activity was conserved after 25 min. RpltM retained more than 90% of its activity over a pH range of 4.2 to 5.0 and remained fully active in the presence of detergents such as nonidet P-40, triton X-100, polyoxyethylen-10-oleyl ether (up to 1%, w/v), dithiothreitol and β-mercaptoethanol. The stability under these conditions is also better than that reported for other insect α-mannosidases. Thus, RpltM could be used as an important bioindustrial tool for removing mannose residues from oligosaccharides.

Keywords: a-mannosidase, thermoacidophilic, thermostable, oil palm weevil, Rhynchophorus palmarum, Curculionidae

Received: October 17, 2008; Accepted: January 5, 2009; Revised: January 5, 2009; Published: May 20, 2009Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
BÉDIKOU, M., AHI, P., KONÉ, M., FAULET, B., GONNETY, J., KOUAMÉ, P., & NIAMKÉ, S. (2009). Purification and characterization of a novel thermoacidophilic and thermostable α-mannosidase from the digestive fluid of oil palm weevil Rhynchophorus palmarum (Coleoptera: Curculionidae) larvae. Eur. J. Entomol.106(2), 185-191. doi: 10.14411/eje.2009.022.
Download citation

References

  1. AHI A.P., GONNETY T.J., FAULET B.M., KOUAME L.P. & NIAMKE S.L. 2007: Biochemical characterization of two D-mannosidases from breadfruit (Artocarpus communis) seeds. Afr. J. Biochem. Res. 1: 106-116
  2. AKAMA T.O., NAKAGAWA H., WONG N.K., SUTTON-SMITH M., DELL A., NAKAYAMA J., NISHIMURA S., PAI A., MOREMEN K.W., MARTH J.D. & FUKUDA M.N. 2006: Essential and mutually compensatory roles of D-mannosidase II and D-mannosidase IIx in N-glycan processing in vivo in mice. Proc. Natl. Acad. Sci. USA 103: 8983-8988 Go to original source...
  3. ALTMANN F. & MARZ L. 1995: Processing of asparagines-linked oligosaccharides in insect cells: evidence for D-mannosidase II. Glycoconj. J. 12: 150-155 Go to original source...
  4. ANGELOV A., PUTYRSKI M. & LIEBL W. 2006: Molecular and biochemical characterization of D-glucosidase and D-mannosidase and their clustered genes from the thermoacidophilic archaeon, Picrophilus torridus. J. Bacteriol. 188: 7123-7131 Go to original source...
  5. ATHANASOPOULOS V.I., NIRANJAN K. & RASTALL R.A. 2004: Regioselective synthesis of mannobiose and mannotriose by reverse hydrolysis using a novel 1,6-D-mannosidase from Aspergillus phoenicis. J. Mol. Catal. B Enzym. 27: 215-219 Go to original source...
  6. BECKER B., RAMAKRISHNAN S., MENOVSKY A.A., NIEUWENHUYS G.J. & MYDOSH J.A. 1997: Unusual ordering behaviour single-crystal U2Rh3Si5. Phys. Rev. Lett. 78: 1347-1350 Go to original source...
  7. BLUM H., BEIER H. & GROSS B. 1987: Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8: 93-99 Go to original source...
  8. CENCI DI BELLO I., FLEET G., NAMGOONG S.K., TANDANO K.I. & WINCHESTER B. 1989: Stucture-activity relationship of swainsonine. Inhibition of human D-mannosidases by swainsonine analogs. Biochem. J. 159: 855-861 Go to original source...
  9. CHIPOULET J.M. & CHARARAS C. 1985: Survey and electrophoretical separation of the glycosidases of Rhagium inquisitor (Coleoptera: Cerambycidae) larvae. Comp. Biochem. Physiol. (B) 80: 241-246 Go to original source...
  10. DANIEL P.F., WINCHESTER B. & WARREN C.D. 1994: Mammalian alpha-mannosidases: multiple forms but a common purpose? Glycobiology 4: 551-566 Go to original source...
  11. FAULET M.B., NIAMKE S., GONNETY T.J. & KOUAME L.P. 2006: Purification and biochemical characteristics of a new strictly specific endoxylanase from termite Macrotermes subhyalinus workers (Macrotermitinae - Termitidae). Bull. Insectol. 59: 17-26
  12. FERREIRA C., RIBEIRO A.F., GARCIA E.S. & TERRA W.R. 1988: Digestive enzymes trapped between and associated with the double plasma membranes of Rhodnius prolixus posterior midgut cells. Insect Biochem. 18: 521-530 Go to original source...
  13. GIORDANI R., SEIPAIO M., MOULIN T.J. & REGLI P. 1991: Antifungal action of Carica papaya latex: isolation of fungal cell wall hydrolysing enzymes. Mycoses 34: 469-477 Go to original source...
  14. HEIKINHEIMO P., HELLAND R., LEIROS H.K., LEIROS I., KARLSEN S., EVJEN G., RAVELLI R., SCHOEHN G., RUIGROK R., TOLLERSRUD O.K., MCSWEENEY S. & HOUGH E. 2003: The structure of bovine lysosomal D-mannosidase suggests a novel mechanism for low-pH activation. J. Mol. Biol. 327: 631-644 Go to original source...
  15. HENRISSAT B. & BAIROCH A. 1993: New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 293: 781-788. Go to original source...
  16. HENRISSAT B. & BAIROCH A. 1996: Updating the sequence-based classification of glycosyl hydrolases. Biochem. J. 316: 695-696 Go to original source...
  17. HIRSCH C., BLOM D. & PLOEGH H.L. 2003: A role for N-glycanase in the cytosolic turnover of glycoproteins. EMBO J. 22: 1036-1046 Go to original source...
  18. HOWARD S., BRAUN C., MCCARTER J., MOREMEN K.W., LIAO Y.Y. & WITHERS S.G. 1997: Human lysosomal and Jack bean D-mannosidases are retaining glycosidases. Biochem. Biophys. Res. Commun. 238: 896-898 Go to original source...
  19. JARVIS D.L., BOHLMEYER D.A., LIAO Y.F., LOMAX K.K., MERKEL R.K., WEINKAUF C. & MOREMEN K.W. 1997: Isolation and characterization of a class II alpha-mannosidase cDNA from lepidopteran insect cells. Glycobiology 7: 113-127 Go to original source...
  20. KORNFELD R. & KORNFELD S. 1985: Assembly of asparaginelinked oligosaccharides. Annu. Rev. Biochem. 54: 631-664 Go to original source...
  21. LAEMMLI U.K. 1970: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 658-685 Go to original source...
  22. LIAO Y.F., LAL A. & MOREMEN K.W. 1996: Cloning, expression, purification and characterization of the human broad specificity lysosomal acid D-mannosidase. J. Biol. Chem. 271: 28348-28358 Go to original source...
  23. LOWRY O.H., ROSEBROUGH N.J., FARRA L. & RANDALL R.J. 1951: Protein measurement with Folin-phenol reagent. J. Biol. Chem. 193: 265-275
  24. MARUYAMA Y., NAKAJIMA T. & ICHISHIMA E. 1994: A 1,2-alphaD-mannosidase from a Bacillus sp.: purification, characterization and mode of action. Carbohydr. Res. 251: 89-98 Go to original source...
  25. MICHALSKI J.C., HAEUW J.F., WIERUSZESKI J.M., MONTREUIL J. & STRECKER G. 1990: In vitro hydrolysis of oligomannosyl oligosaccharides by the lysosomal alpha-D-mannosidases. Eur. J. Biochem. 189: 369-379 Go to original source...
  26. MISAKI R., FUJIYAMA K., YOKOYAMA H., IDO Y., MIYAUCHI K., YOSHIDA T. & SEKI T. 2003: Characterization of almond D-mannosidase and its application for structure analysis of sugar chain. J. Biosci. Bioeng. 96: 187-192 Go to original source...
  27. MOREMEN K.W. 2000: D-Mannosidases in asparagine-linked oligosaccharide processing and catabolism. In Ernst B., Hart G. & Sinay P. (eds): Oligosaccharides in Chemistry and Biology: A Comprehensive Handbook. Wiley & Sons, New York, pp. 81-117
  28. MOREMEN K.W., TRIMBLE R.B. & HERSCOVICS A. 1994: Glycosidases of the asparagine-linked oligosaccharide processing pathway. Glycobiology 4: 113-125 Go to original source...
  29. NANKAI H., HASHIMOTO W. & MURATA K. 2002: Molecular identification of family 38 D-mannosidase of Bacillus sp. strain GL1, responsible for complete depolymerisation of xanthan. Appl. Environ. Microb. 68: 2731-2736 Go to original source...
  30. NG T.K. & KENEALY W.R. 1986: Industrial application of thermostable enzymes. In Brock T.D. (ed.): Thermophiles General, Molecular and Applied Microbiology. John Wiley, New York, pp. 197-205
  31. NIEHAUS F., BERTOLDO C., KAHLER M. & ANTRANIKIAN G. 1999: Extremophiles as a source of novel enzymes for industrial application. Appl. Microbiol. Biotechnol. 51: 711-729 Go to original source...
  32. RABOUILLE G., KUNTZ D.A., LOCKYER A.E., WATSON R., SIGNORELLI T., ROSE D.R., VAN DER HEUVEL M. & ROBERTS D.B. 1999: The Drosophila GMII gene encodes a Golgi D-mannosidase II. J. Cell Sci. 112: 3319-3330
  33. SHAH N., KUNTZ D.A. & ROSE D.R. 2008: Golgi alphamannosidase II cleaves two sugars sequentially in the same catalytic site. Proc. Natl. Acad. Sci. USA 105: 9570-9575 Go to original source...
  34. SUN H., YANG H. & ASKINS M.E. 1999: Retrovirus vector mediated correction and cross correlation of lysosomal D-mannosidase deficiency in human and feline fibroblasts. Hum. Gen. Ther. 10: 1311-1319 Go to original source...
  35. TATARA Y., LEE B.R., YOSHIDA T., TAKAHASHI K. & ICHISHIMA E. 2003: Identification of catalytic residues of Ca2+ independent 1,2-D-D-mannosidase from Aspergillus saitoi by site-directed mutagenesis. J. Biol. Chem. 278: 25289-25294 Go to original source...
  36. TERRA W.R. & FERREIRA C. 1994: Insect digestive enzymes: properties, compartmentalization and function. Comp. Biochem. Physiol. (B) 109: 1-62 Go to original source...
  37. THOMAS B., BARBARA K., PETER J.M., OIVIND N., OLE K.T. & JOHN J.H. 2001: Purification and characterization of recombinant human lysosomal D-mannosidase. Mol. Genet. Metab. 73: 18-29 Go to original source...
  38. TREMBLAY L.O., KOVACS E.N., DANIELS E., WONG N.K., SUTTONSMITH M., MORRIS H.R., DELL A., MARCINKIEWICZ E., SEIDAH N.G., MCKERLIE C. & HERSCOVICS A. 2007: Respiratory distress and neonatal lethality in mice lacking Golgi D-1,2-mannosidase IB involved in N-glycan maturation. J. Biol. Chem. 282: 2558-2566 Go to original source...
  39. VAN DEN ELSEN J.M., KUNTZ D.A. & ROSE D.R. 2001: Structure of Golgi alpha-mannosidase II: a target for inhibition of growth and metastasis of cancer cells. EMBO J. 20: 3008-3017 Go to original source...
  40. VARKI A. 1993: Biological roles of oligosaccharides: all the theories are correct. Glycobiology 3: 97-130 Go to original source...
  41. ZAMOST L.B., NIELSEN K.H. & STARNES L.R. 1991: Thermostable enzymes for industrial applications. J. Ind. Microbiol. 8: 71-82 Go to original source...

This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.