Folia Parasitologica 54[4] 301-309 (2007) | DOI: 10.14411/fp.2007.039

Glycolytic and chitinolytic activities of Phlebotomus papatasi (Diptera: Psychodidae) from diverse ecological habitats

Raymond L. Jacobson, Liora Studentsky, Yosef Schlein
Department of Parasitology, The Hebrew University - Hadassah Medical School, P.O. Box 12272, Jerusalem, 91120, Israel

The sand fly Phlebotomus papatasi Scopoli, 1786, the vector of Leishmania major Yakimoff et Schokhor, 1914, is found in desert areas where sugars are scarce but also in habitats that abound in sugar sources. The sand flies require sugar meals from plant sources for their energy requirements and to hydrolyze these complex sugars, they need a repertoire of glycosidases. We presumed that there are differences in the levels of glycosidase activities in flies from such habitats and also assumed that they may be instrumental in modulating the flies' susceptibility to L. major infections. Phlebotomus papatasi originating from diverse ecological habitats ranging from an oasis to desert sites were colonized. They were analyzed for weight changes and glycosidase activities before and after feeding on 1M sucrose solution. Oasis flies were smaller than desert flies but took larger sugar meals. Homogenates of these flies hydrolyzed 16 synthetic and 2 natural glycoside substrates to varying degrees. The arid-region flies tended to produce more glycosidase activity than those originating in sugar-rich environments, especially sucrase, α- and β-glucosidase, α-fucosidase, α-mannosidase, and α- and β-N-acetylgalactosaminidase. However, chitinolytic enzyme activities and particularly the β-N-acetylhexosaminidase activity of oasis flies were higher than other flies tested. In comparing the desert flies, there were also significant differences in glycolytic enzyme activities between the spring-line (flowering season) of flies and the autumn-line (end of dry season) flies. A range of saccharide inhibitors was tested to demonstrate the specificity of the enzymes.

Keywords: Phlebotomus papatasi, glycosidases, chitinases, oasis, arid

Received: May 14, 2007; Accepted: July 13, 2007; Published: December 1, 2007  Show citation

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Jacobson, R.L., Studentsky, L., & Schlein, Y. (2007). Glycolytic and chitinolytic activities of Phlebotomus papatasi (Diptera: Psychodidae) from diverse ecological habitats. Folia Parasitologica54(4), 301-309. doi: 10.14411/fp.2007.039
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References

  1. ALEXANDER B., USMA M.C. 1994: Potential sources of sugar for the phlebotomine sandfly Lutzomyia youngi (Diptera: Psychodidae) in a Colombian coffee plantation. Ann. Trop. Med. Parasitol. 88: 543-549 Go to original source... Go to PubMed...
  2. APPLEBAUM S.W. 1985: Biochemistry of digestion. In: G.A. Kerkut and L.I. Gilbert (Eds.), Comprehensive Insect Physiology, Biochemistry and Pharmacology. Vol. 4. Pergamon Press, New York, pp. 279-311
  3. ASHFORD R.W. 1974: Sandflies (Diptera: Phlebotomidae) from Ethiopia: taxonomic and biological notes. J. Med. Entomol. 11: 605-616 Go to original source... Go to PubMed...
  4. ASHFORD R.W., BETTINI S. 1987: Ecology and epidemiology: Old World. In: W. Peters and R. Killick-Kendrick (Eds.), The Leishmaniasis in Biology and Medicine, Vol. 1. Academic Press, London, pp. 365-424
  5. BRADFORD M.M. 1976: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analyt. Biochem. 72: 248- 254 Go to original source... Go to PubMed...
  6. BYRNE D.N., HENDRIX D.L., WILLIAMS L.H. 2003: Presence of trehalulose and other oligosaccharides in hemipteran honeydew, particularly Aleyrodidae. Physiol. Entomol. 28: 144- 149 Go to original source...
  7. CAMERON M.M., PESSOA F.A., VASCONCELOS A.W., WARD R.D. 1995: Sugar meal sources for the phlebotomine sandfly Lutzomyia longipalpis in Ceara State, Brazil. Med. Vet. Entomol. 9: 263-272 Go to original source... Go to PubMed...
  8. CHARLAB R., VALENZUELA J.G., ROWTON E.D., RIBEIRO J.M.C. 1999: Toward an understanding of the biochemical and pharmacological complexity of the saliva of a hematophagous sand fly Lutzomyia longipalpis. Proc. Natl. Acad. Sci. U.S.A. 96: 15155-15160 Go to original source... Go to PubMed...
  9. DILLON R.J., EL KORDY E. 1997: Carbohydrate digestion in sandflies: alpha-glucosidase activity in the midgut of Phlebotomus langeroni. Comp. Biochem. Physiol. B - Biochem. Mol. Biol. 116: 35-40 Go to original source...
  10. DINESH D.S., DHIMAN R.C. 1991: Plant sources of fructose to sandflies, particularly Phlebotomus argentipes in nature. J. Commun. Dis. 23: 160-161 Go to PubMed...
  11. DO K-Y., DO S.I., CUMMINGS R.D. 1997: Differential expression of LacdiNAc sequences (GalNAcss1-4GlcNAc-R) in glycoproteins synthesized by Chinese hamster ovary and human 293 cells. Glycobiology 7: 183-194 Go to original source... Go to PubMed...
  12. EISIKOWITCH D., IVRI Y., DAFNI A. 1986: Reward partitioning in Capparis spp. along ecological gradient. Oecologia 71: 47- 50 Go to original source... Go to PubMed...
  13. FERREIRA C., TORRES B.B., TERRA W.R. 1998: Substrate specificities of midgut beta-glycosidases from insects of different orders. Comp. Biochem. Physiol. B - Biochem. Mol. Biol. 119: 219-225 Go to original source...
  14. GHASEMPOUR H.R., GAFF D.F., WILLIAMS R.P.W., GIANELLO R.D. 1998: Contents of sugars in leaves of drying desiccation tolerant flowering plants, particularly grasses. Plant Growth Regul. 24: 185-191 Go to original source...
  15. GONTIJO N.F., ALMEIDA-SILVA S., COSTA F.F., MARES-GUIA M.L., WILLIAMS P., MELO M.N. 1998: Lutzomyia longipalpis: pH in the gut, digestive glycosidases, and some speculations upon Leishmania development. Exp. Parasitol. 90: 212- 219 Go to original source... Go to PubMed...
  16. GONTIJO N.F., MELO M.N., RIANI E.B., ALMEIDA-SILVA S., MARES-GUIA M.L. 1996: Glycosidases in Leishmania and their importance for Leishmania in phlebotomine sandflies with special reference to purification and characterization of a sucrase. Exp. Parasitol. 83: 117-124 Go to original source... Go to PubMed...
  17. HAMILTON J.G.C., EL NAIEM D.A. 2000: Sugars in the gut of the sandfly Phlebotomus orientalis from Dinder National Park, Eastern Sudan. Med. Vet. Entomol. 14: 64-70 Go to original source... Go to PubMed...
  18. HARSHMAN L.G., HOFFMANN A.A., CLARK, A.G. 1999: Selection for starvation resistance in Drosophila melanogaster: physiological correlates, enzyme activities and multiple stress responses. J. Evol. Biol. 12: 370-379 Go to original source...
  19. HOPKINS W.G. 1995: Introduction to Plant Physiology. John Wiley and Sons, New York, 464 pp
  20. JACOBSON R.L., SCHLEIN Y. 1997: Cellulase activity of Leishmania major in the sandfly vector and in culture. J. Eukaryot. Microbiol. 44: 216-219 Go to original source... Go to PubMed...
  21. JACOBSON R.L., SCHLEIN Y. 2001: Phlebotomus papatasi and Leishmania major parasites express alpha-amylase and alphaglucosidase Acta Trop. 78: 41-49 Go to PubMed...
  22. JACOBSON R.L., SCHLEIN Y., EISENBERGER C.L. 2001: The biological function of sand fly and Leishmania glycosidases. Med. Microbiol. Immunol. 190: 51-55 Go to original source... Go to PubMed...
  23. KILLICK-KENDRICK R., KILLICK-KENDRICK M. 1987: Honeydew of aphids as a source of sugar for Phlebotomus ariasi. Med. Vet. Entomol. 1: 297-302 Go to original source... Go to PubMed...
  24. LEEE.A., WEISS S.L., LAMM., TORRES R., DIAMOND J.A. 1998: Method for assaying intestinal brush-border sucrase in an intact intestinal preparation. Proc. Natl. Acad. Sci. U.S.A. 95: 2111-2116 Go to original source... Go to PubMed...
  25. LEWIS D.J. 1982: A taxonomic review of the genus Phlebotomus (Diptera: Psychodidae). Bull. Brit. Mus. (Nat. Hist.), Entomol., 45: 121-209
  26. LUNN J.E., HATCH M.D. 1995: Primary partitioning and storage of photosynthate in sucrose and starch in leaves of C4 plants. Planta 197: 385-391 Go to original source...
  27. MACVICKER J.A.K., MOORE J.S., MOLYNEUX D.H., MAROLI M. 1990: Honeydew sugars in wild caught Italian phlebotomine sand flies (Diptera: Psychodidae) as detected by high performance liquid chromatography. Bull. Entomol. Res. 80: 339-344 Go to original source...
  28. MARTINEZ J.P., LUTTS S., SCHANCK A., BAJJI M., KINET J.M. 2004: Is osmotic adjustment required for water stress resistance in the Mediterranean shrub Atriplex halimus L? J. Plant Physiol. 161: 1041-1051 Go to original source... Go to PubMed...
  29. MARTINEZ DEL RIO C., BRUGGER K.E., RIOS J.L., VERGARA M.E., WITMER M. 1995: An experimental and comparative study of dietary modulation of intestinal enzymes in the European starling (Sturnus vulgaris). Physiol. Zool. 68: 490- 511 Go to original source...
  30. MOLYNEUX D.H., MOORE J., MAROLI M. 1991: Sugars in sand flies. Parassitologia 33: 431-436 Go to PubMed...
  31. MOORE J.S., KELLY T.B., KILLICK-KENDRICK M., WALLBANKS K.R., MOLYNEUX D.H., KILLICK-KENDRICK R. 1987: Honeydew sugars in wild caught Phlebotomus ariasi detected by high performance liquid chromatography (HPLC) and gas chromatography. Med. Vet. Entomol. 1: 427-434 Go to original source... Go to PubMed...
  32. MUeLLER G., SCHLEIN Y. 2004: Nectar and honeydew feeding of Phlebotomus papatasi in a focus of Leishmania major in Neot Hakikar oasis. J. Vector Ecol. 29: 154-158 Go to PubMed...
  33. PETANIDOU T. 2005: Sugars in Mediterranean floral nectars: An ecological and evolutionary approach. J. Chem. Ecol. 31: 1065-1088 Go to original source... Go to PubMed...
  34. PETTS S.L., TANG Y., WARD R.D. 1997: Nectar from a wax plant, Hoya sp., as a carbohydrate source for Lutzomyia longipalpis (Diptera: Psychodidae). Ann. Trop. Med. Parasitol. 91: 443- 446 Go to original source... Go to PubMed...
  35. RIBEIRO J.M.C., ROWTON E.D., CHARLAB R. 2000: Salivary amylase activity of the phlebotomine sand fly, Lutzomyia longipalpis. Insect Biochem. Mol. Biol. 30: 271-277 Go to original source... Go to PubMed...
  36. RAMALHO-ORTIGAO J.M., KAMHAWI S., JOSHI M.B., REYNOSO D., LAWYER P.G., DWYER D.M., SACKS D.L., VALENZUELA J.G. 2005: Characterization of a blood activated chitinolytic system in the midgut of the sand fly vectors Lutzomyia longipalpis and Phlebotomus papatasi. Insect Mol. Biol. 14: 703- 712 Go to original source... Go to PubMed...
  37. SAMIE M., WALLBANKS K.R., MOORE J.S., MOLYNEUX D.H. 1990: Glycosidase activity in the sandfly Phlebotomus papatasi. Comp. Biochem. Physiol. B - Biochem. Mol. Biol. 96: 577-579 Go to original source...
  38. SCHLEIN Y., JACOBSON R.L. 1994: Mortality of Leishmania major in Phlebotomus papatasi caused by plant-feeding of the sand flies. Am. J. Trop. Med. Hyg. 50: 20-27 Go to original source...
  39. SCHLEIN Y., JACOBSON R.L. 1999: Sugar meals and longevity of the sandfly Phlebotomus papatasi in an arid focus of Leishmania major in the Jordan Valley. Med. Vet. Entomol. 13: 65-71 Go to original source... Go to PubMed...
  40. SCHLEIN Y., JACOBSON R.L. 2000: Photosynthesis modulates the plant feeding of Phlebotomus papatasi (Diptera: Psychodidae). J. Med. Entomol. 37: 319-324 Go to original source... Go to PubMed...
  41. SCHLEIN Y., JACOBSON R.L. 2001: Parasitic infection - Hunger tolerance and Leishmania in sandflies. Nature 414: 168 Go to original source... Go to PubMed...
  42. SCHLEIN Y., JACOBSON R.L. 2002: Linkage between susceptibility of Phlebotomus papatasi to Leishmania major and hunger tolerance. Parasitology 125: 343-348 Go to original source... Go to PubMed...
  43. SCHLEIN Y., JACOBSON R.L., SHLOMAI J. 1991: Chitinase secreted by Leishmania functions in the sand fly vector. Proc. R. Soc. Lond., Ser. B - Biol. Sci., 245: 121-126 Go to original source... Go to PubMed...
  44. SCHLEIN Y., MUeLLER G. 1995: Assessment of plant tissue feeding by sand flies (Diptera: Psychodidae) and mosquitoes (Diptera: Culicidae). J. Med. Entomol. 32: 882-887 Go to original source... Go to PubMed...
  45. SCHLEIN Y., WARBURG A. 1986: Phytophagy and the feeding cycle of Phlebotomus papatasi (Diptera, Psychodidae) under experimental conditions. J. Med. Entomol. 23: 11-15 Go to original source... Go to PubMed...
  46. SCHLEIN Y., WARBURG A., SCHNUR L.F., GUNDERS A.E. 1982: Leishmaniasis in the Jordan Valley II. Sand-flies and transmission in the central endemic area. Trans. R. Soc. Trop. Med. Hyg. 76: 582-586 Go to original source... Go to PubMed...
  47. SCHNUR L.F., NASEREDDIN A., EISENBERGER C.L., JAFFE C.L., EL FARI M., AZMI K., ANDERS G., KILLICK-KENDRICK M., KILLICK-KENDRICK R., DEDET J.P., PRATLONG F., KANAAN M., GROSSMAN T., JACOBSON R.L., SCHONIAN G., WARBURG A. 2004: Multifarious characterization of Leishmania tropica from a Judean desert focus, exposing intraspecific diversity and incriminating Phlebotomus sergenti as its vector. Am. J. Trop. Med. Hyg. 70: 364-372 Go to original source... Go to PubMed...
  48. SCHOMBURG I., CHANG A., EBELING C., GREMSE M., HELDT C., HUHN G., SCHOMBURG D. 2004: BRENDA, the enzyme database: updates and major new developments. Nucleic Acids Res. 32: D431-433 Go to original source... Go to PubMed...
  49. TAYLOR K.A.C.C. 1995: A colorimetric fructose assay. Appl. Biochem. Biotechnol., Part A, Enzym. Eng. Biotechnol., 53: 215-227 Go to original source...
  50. WALLBANKS K.R., MOORE J.S., BENNET L.R., SOREN R., MOLYNEUX D.H., CARLIN J.M., PEREZ J.E. 1991: Aphid derived sugars in the sand fly Lutzomyia peruensis. Trop. Med. Parasitol. 42: 60-62 Go to PubMed...
  51. WASSERBERG G., YAROM I., WARBURG A. 2003: Seasonal abundance patterns of the sandfly Phlebotomus papatasi in climatically distinct foci of cutaneous leishmaniasis in Israeli deserts. Med. Vet. Entomol. 17: 452-456 Go to original source... Go to PubMed...
  52. ZAR J.H. 1999: Biostatistical Analysis. Fourth Edition. PrenticeHall, Englewood Cliffs, N.J., 663 pp