Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-24T06:48:16.982Z Has data issue: false hasContentIssue false

The antifungal activity of the cuticular and internal fatty acid methyl esters and alcohols in Calliphora vomitoria

Published online by Cambridge University Press:  08 April 2013

MAREK GOŁĘBIOWSKI*
Affiliation:
Faculty of Chemistry, Institute for Environmental and Human Health Protection, University of Gdańsk, ul. Sobieskiego 18/19, 80-952 Gdańsk, Poland
MAGDALENA CERKOWNIAK
Affiliation:
Faculty of Chemistry, Institute for Environmental and Human Health Protection, University of Gdańsk, ul. Sobieskiego 18/19, 80-952 Gdańsk, Poland
MAŁGORZATA DAWGUL
Affiliation:
Faculty of Pharmacy, Medical University of Gdańsk, Al. Gen. Hallera 107, 80-416 Gdańsk, Poland
WOJCIECH KAMYSZ
Affiliation:
Faculty of Pharmacy, Medical University of Gdańsk, Al. Gen. Hallera 107, 80-416 Gdańsk, Poland
MIECZYSŁAWA I. BOGUŚ
Affiliation:
Institute of Parasitology, Polish Academy of Sciences, Twarda 51/55, 00-818 Warszawa, Poland
PIOTR STEPNOWSKI
Affiliation:
Faculty of Chemistry, Institute for Environmental and Human Health Protection, University of Gdańsk, ul. Sobieskiego 18/19, 80-952 Gdańsk, Poland
*
*Corresponding author: Faculty of Chemistry, Institute for Environmental and Human Health Protection, University of Gdańsk, ul. Sobieskiego 18/19, 80-952 Gdańsk, Poland. Tel: +48 58 5235 398. Fax: +48 58 5235 472. E-mail: [email protected]

Summary

The composition of the fatty acid methyl ester (FAME) and alcohol fractions of the cuticular and internal lipids of Calliphora vomitoria larvae, pupae and male/female adults was obtained by separating these two fractions by HPLC–LLSD and analysing them quantitatively using GC–MS. Analysis of the cuticular lipids of the worldwide, medically important ectoparasite C. vomitoria revealed 6 FAMEs with odd-numbered carbon chains from C15:0 to C19:0 in the larvae, while internal lipids contained 9 FAMEs ranging from C15:1 to C19:0. Seven FAMEs from C15:0 to C19:0 were identified in the cuticular lipids of the pupae, whereas the internal lipids of the pupae contained 10 FAMEs from C13:0 to C19:0. The cuticular lipids of males and females and also the internal lipids of males contained 5, 7 and 6 FAMEs from C15:0 to C19:0 respectively. Seven FAMEs from C13:0 to C19:0 were identified in the internal lipids of females, and 7, 6, 5 and 3 alcohols were found in the cuticular lipids of larvae, pupae, males and females respectively. Only saturated alcohols with even-numbered carbon chains were present in these lipids. Only 1 alcohol (C22:0) was detected in the internal lipids of C. vomitoria larvae, while just 4 alcohols from – C18:0 to C24:0 – were identified in the internal lipids of pupae, and males and females. We also identified glycerol and cholesterol in the larvae, pupae, males and females of C. vomitoria. The individual alcohols and FAMEs, as well as their mixtures isolated from the cuticular and internal lipids of larvae, pupae, males and females of C. vomitoria, demonstrated antimicrobial activity against entomopathogenic fungi.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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

REFERENCES

Bałazy, S. (2004). Significance of protected areas for the preservation of entomopathogenic fungi. Kosmos 53, 516.Google Scholar
Benoit, J. B. and Denlinger, D. L. (2007). Suppression of water loss during adult diapause in the northern house mosquito, Culex pipiens. Journal of Experimental Biology 210, 217226.CrossRefGoogle ScholarPubMed
Boguś, M. I. and Scheller, K. (2002). Extraction of an insecticidal protein fraction from the pathogenic fungus Conidiobolus coronatus. Acta Parasitologica 47, 6672.Google Scholar
Boguś, M. I., Kędra, E., Bania, J., Szczepanik, M., Czygier, M., Jabłoński, P., Pasztaleniec, A., Samborski, J., Mazgajska, J. and Polanowski, A. (2007). Different defense strategies of Dendrolimus pini, Galleria mellonella, and Calliphora vicina against fungal infection. Journal of Insect Physiology 53, 909922.CrossRefGoogle ScholarPubMed
Boguś, M. I., Czygier, M., Gołębiowski, M., Kędra, E., Kucińska, J., Mazgajska, J., Samborski, J., Wieloch, W. and Włóka, E. (2010). Effects of insect cuticular fatty acids on in vitro growth and pathogenicity of the entomopathogenic fungus Conidiobolus coronatus. Experimental Parasitology 125, 400408.CrossRefGoogle ScholarPubMed
Böröczky, K., Park, K. C., Minard, R., Jones, T. H., Baker, T. C. and Tumlinson, J. H. (2008). Differences in cuticular lipid composition of the antennae of Helicoverpa zea, Heliothis virescens, and Manduca sexta. Journal of Insect Physiology 54, 13851391.CrossRefGoogle ScholarPubMed
Bourel, B., Fleurisse, L., Hedouin, V., Cailliez, J. C., Creusy, C., Gosset, D. and Goff, M. L. (2001). Immunohistochemical contribution to the study of morphine metabolism in Calliphoridae larvae and implications in forensic entomotoxicology. Journal of Forensic Sciences 46, 596599.CrossRefGoogle Scholar
Brey, P. T., Ohayon Lesourd, M., Castex, H., Roucache, J. and Latge, J. P. (1985). Ultrastructure and chemical composition of the outer layers of the cuticle of the pea aphid Acyrthosiphon pisum (HARRIS). Comparative Biochemistry and Physiology A 82, 401411.CrossRefGoogle Scholar
Buckner, J. S. (1993). Cuticular polar lipids of insects. In Insect Lipids: Chemistry, Biochemistry and Biology (ed. Stanley-Samuelson, D. W. and Nelson, D. R.), pp. 227270. University of Nebraska Press, Lincoln, NE, USA.Google Scholar
Buckner, J. S., Nelson, D. R. and Mardaus, M. C. (1994). The lipid composition of the wax particles from adult whiteflies, Bemisia tabaci and Trialeurodes vaporariorum. Insect Biochemistry and Molecular Biology 24, 977987.CrossRefGoogle Scholar
Buckner, J. S., Mardaus, M. C. and Nelson, D. R. (1996). Cuticular lipid composition of Heliothis virescens and Helicoverpa zea pupae. Comparative Biochemistry and Physiology B 114, 207216.CrossRefGoogle Scholar
Buckner, J. S., Hagen, M. M. and Nelson, D. R. (1999). The composition of the cuticular lipids from nymphs and exuviae of the Silverleaf Whitefly, Bemisia argentifolii. Comparative Biochemistry and Physiology B 124, 201207.CrossRefGoogle Scholar
Buckner, J. S., Pitts-Singer, T. L., Guédot, Ch., Hagen, M. M., Fatland, Ch. L. and Kemp, W. P. (2009). Cuticular lipids of female solitary bees, Osmia lignaria Say and Megachile rotundata (F.) (Hymenoptera: Megachilidae). Comparative Biochemistry and Physiology 153, 200205.CrossRefGoogle ScholarPubMed
Caputo, B., Dani, F. R., Horne, G. L., Fale, S. N., Diabate, A., Turillazzi, S., Coluzzi, M., Costantini, C., Priestman, A. A., Petrarca, V. and della Torre, A. (2007). Comparative analysis of epicuticular lipid profiles of sympatric and allopatric field populations of Anopheles gambiae s.s. molecular forms and An. arabiensis from Burkina Faso (West Africa). Insect Biochemistry and Molecular Biology 37, 389398.CrossRefGoogle Scholar
Chernysh, S., Kim, S. I., Bekker, G., Pleskach, V. A., Filatova, N. A., Anikin, V. B., Platonov, V. G. and Bulet, P. (2002). Antiviral and antitumor peptides from insects. Proceedings of the National Academy of Sciences USA 99, 1262812632.CrossRefGoogle ScholarPubMed
Dani, F. R., Cannoni, S., Turillazzi, S. and Morgan, E. D. (1996). Ant repellent effect of the sternal gland secretion of Polistes dominulus (Christ) and P. sulcifer (Zimmermann) (Hymenoptera: Vespidae). Journal of Chemical Ecology 22, 3748.CrossRefGoogle Scholar
Deml, R. and Dettner, K. (1993). Biogenic amines and phenolics characterize the defensive secretion of saturniid caterpillars (Lepidoptera: Saturniidae): a comparative study. Journal of Comparative Physiology B 163, 123132.CrossRefGoogle Scholar
Domsch, K. H., Gams, W. and Anderson, T.-H. (2007). Compendium of Soil Fungi, 2nd Edn. IHW Verlag, Eching, Germany.Google Scholar
Fan, Y., Eliyahu, D. and Schal, C. (2008). Cuticular hydrocarbons as maternal provisions in embryos and nymphs of the cockroach Blattella germanica. Journal of Experimental Biology 211, 548554.CrossRefGoogle ScholarPubMed
Förster, M., Klimpel, S., Mehlhorn, H., Sievert, K., Messler, S. and Pfeffer, K. (2007). Pilot study on synanthropic flies (e.g. Musca, Sarcophaga, Calliphora, Fannia, Lucilia, Stomoxys) as vectors of pathogenic microorganisms. Parasitology Research 101, 243246.CrossRefGoogle ScholarPubMed
Gibbs, A. G., Chippindale, A. K. and Rose, M. R. (1997). Physiological mechanisms of the evolution of desiccation resistance in Drosophila melanogaster. Journal of Experimental Biology 200, 18211832.CrossRefGoogle ScholarPubMed
Gibbs, A. G., Louie, A. K. and Ayala, J. A. (1998). Effects of temperature on cuticular lipids and water balance in a desert Drosophila: is thermal acclimation beneficial? Journal of Experimental Biology 210, 7180.CrossRefGoogle Scholar
Gołębiowski, M. (2012). Comparison of free fatty acids composition of cuticular lipids of Calliphora vicina larvae and pupae. Lipids 47, 10011009.CrossRefGoogle ScholarPubMed
Gołębiowski, M., Maliński, E., Nawrot, J., Szafranek, J., Stepnowski, P. (2007). Identification of the cuticular lipid composition of the Western Flower Thrips Frankliniella occidentalis. Comparative Biochemistry and Physiology B 147, 288292.CrossRefGoogle ScholarPubMed
Gołębiowski, M., Maliński, E., Boguś, M. I., Kumirska, J. and Stepnowski, P. (2008 a). The cuticular fatty acids of Calliphora vicina, Dendrolimus pini and Galleria mellonella larvae and their role in resistance to fungal infection. Insect Biochemistry and Molecular Biology 38, 619627.CrossRefGoogle ScholarPubMed
Gołębiowski, M., Maliński, E., Nawrot, J. and Stepnowski, P. (2008 b). Identification and characterization of surface lipid components of the dried-bean beetle Acanthoscelides obtectus (Say) (Coleoptera: Bruchidae). Journal of Stored Product Research 44, 386388.CrossRefGoogle Scholar
Gołębiowski, M., Boguś, M. I., Paszkiewicz, M. and Stepnowski, P. (2010). The composition of the free fatty acids from Dendrolimus pini exuviae. Journal of Insect Physiology 56, 391397.CrossRefGoogle ScholarPubMed
Gołębiowski, M., Boguś, M. I., Paszkiewicz, M. and Stepnowski, P. (2011). Cuticular lipids of insects as potential biofungicides: methods of lipids composition analysis. Analytical and Bioanalytical Chemistry 399, 31773191.CrossRefGoogle ScholarPubMed
Gołębiowski, M., Boguś, M. I., Paszkiewicz, M., Wieloch, W., Włóka, E. and Stepnowski, P. (2012 a). The composition of the cuticular and internal free fatty acids and alcohols from Lucilia sericata males and females. Lipids 47, 613622.CrossRefGoogle ScholarPubMed
Gołębiowski, M., Paszkiewicz, M., Grubba, A., Gąsiewska, D., Boguś, M. I., Włóka, E., Wieloch, W. and Stepnowski, P. (2012 b). Cuticular and internal n-alkane composition of Lucilia sericata larvae, pupae, male and female imagines: application of HPLC-LLSD and GC/MS-SIM. Bulletin of Entomological Research 102, 453460.CrossRefGoogle ScholarPubMed
Gołębiowski, M., Dawgul, M., Kamysz, W., Boguś, M. I., Wieloch, W., Włóka, E., Paszkiewicz, M., Przybysz, E. and Stepnowski, P. (2012 c). The antimicrobial activity of the alcohols from Musca domestica. Journal of Experimental Biology 215, 34193428.Google ScholarPubMed
Gołębiowski, M., Cerkowniak, C., Boguś, M. I., Włóka, E., Dawgul, M., Kamysz, W. and Stepnowski, P. (2013). Free fatty acids in the cuticular and internal lipids of Calliphora vomitoria and their antimicrobial activity. Journal of Insect Physiology 59, 416429.CrossRefGoogle ScholarPubMed
Grassberger, M., Frank, C. (2004). Initial study of arthropod succession on pig carrion in a central European urban habitat. Journal of Medical Entomology 41, 511523.CrossRefGoogle Scholar
Green, P. W. C. (2009). The effects of insect extracts and some insect-derived compounds on the settling behavior of Liposcelis bostrychophila. Journal of Chemical Ecology 35, 10961107.CrossRefGoogle ScholarPubMed
Green, P. W. C. (2011). Insect-derived compounds affect the behaviour of Liposcelis bostrychophila: effects of combination and structure. Journal of Stored Product Research 47, 262266.CrossRefGoogle Scholar
Ikekawa, N., Morisaki, M. and Fujimoto, Y. (1993). Sterol metabolism in insects: dealkylation of phytosterol to cholesterol. Accounts of Chemical Research 26, 139146.CrossRefGoogle Scholar
Jankevica, L. (2004). Ecological associations between entomopathogenic fungi and pest insects recorded in Latvia. Latvijas Entomologs 41, 6065.Google Scholar
Jarrold, S., Moore, D., Potter, U. and Charnley, A. K. (2007). The contribution of surface waxes to pre-penetration growth of an entomopathogenic fungus on host cuticle. Mycological Research 111, 240249.CrossRefGoogle ScholarPubMed
Jiann-Tsyh, L., McKeon, T. A. and Stafford, A. E. (1995). Gradient reversed-phase high-performance liquid chromatography of saturated, unsaturated and oxygenated free fatty acids and their methyl esters. Journal of Chromatography 699, 8591.Google Scholar
Jones, T. H., Moran, M. D. and Hurd, L. E. (1997). Cuticular extracts of five common mantids (Mantodea: Mantidae) of the Eastern United States. Comparative Biochemistry and Physiology B 116, 419422.CrossRefGoogle ScholarPubMed
Kermasha, S., Kubow, S. and Goetghebeur, M. (1994). Comparative high-performance liquid chromatographic analyses of cholesterol and its oxidation products using diode-array ultraviolet and laser light-scattering detection. Journal of Chromatography 685, 229235.CrossRefGoogle Scholar
Kerwin, J. L. (1982). Chemical control of the germination of asexual spores of Entomophthora culicis, a fungus parasitic on dipterans. Journal of General Microbiology 128, 21792186.Google Scholar
Kerwin, J. L. (1984). Fatty acid regulation of the germination of Erynia variabilis conidia on adults and puparia of the lesser housefly, Fannia canicularis. Canadian Journal of Microbiology 30, 158161.CrossRefGoogle Scholar
Kühbandner, S., Sperling, S., Mori, K. and Ruther, J. (2012). Deciphering the signature of cuticular lipids with contact sex pheromone function in a parasitic wasp. Journal of Experimental Biology 215, 24712478.CrossRefGoogle Scholar
Le Conte, Y., Arnold, G., Trouiller, J. and Masson, C. (1990). Identification of a brood pheromone in honeybees. Naturwissenschaften 77, 334336.CrossRefGoogle Scholar
Lockey, K. H. (1980). Insect cuticular hydrocarbons. Comparative Biochemistry and Physiology 65, 457462.Google Scholar
Lockey, K. H. (1988). Lipids of the insect cuticle: origin, composition and function. Comparative Biochemistry and Physiology B 89, 595645.CrossRefGoogle Scholar
Mpuru, S., Blomquist, G. J., Schal, C., Roux, M., Kuenzli, M., Dusticier, G., Clément, J. L. and Bagnères, A. G. (2001). Effect of age and sex on the production of internal and external hydrocarbons and pheromones in the housefly, Musca domestica. Insect Biochemistry and Molecular Biology 31, 139155.CrossRefGoogle ScholarPubMed
Nelson, D. R., Guershon, M. and Gerling, D. (1998). The surface wax composition of the exuviae and adults of Aleyrodes singularis. Comparative Biochemistry and Physiology B 119, 655665.CrossRefGoogle Scholar
Nelson, D. R., Fatland, Ch.L., Buckner, J. S. and Freeman, T. P. (1999). External lipids of adults of the giant whitefly, Aleurodicus dugesii. Comparative Biochemistry and Physiology 123, 137145.CrossRefGoogle Scholar
O'Callagan, M., Garnham, M. L., Nelson, T. L., Baird, D. and Jackson, T. A. (1996). The pathogenicity of Serratia strains to Lucilia sericata (Diptera: Calliphoridae). Journal of Invertebrate Pathology 68, 2227.CrossRefGoogle Scholar
Ohara, V. S. and Lockey, K. H. (1990). Cuticular lipids of Locusta migratoria migratoriodes, Schistocerca gregaria (Acrididae) and other Orthopteran species – I. Polar components. Comparative Biochemistry and Physiology B 95, 603608.CrossRefGoogle Scholar
Oliveira, I., Pereira, J. A., Lino-Neto, T., Bento, A. and Baptista, P. (2012). Fungal diversity associated to the olive moth, Prays Oleae Bernard: a survey for potential entomopathogenic fungi. Microbial Ecology 63, 964974.CrossRefGoogle Scholar
Pedrini, N., Crespo, R. and Juárez, M. P. (2007). Biochemistry of insect epicuticle degradation by entomopathogenic fungi. Comparative Biochemistry and Physiology 146, 124137.Google ScholarPubMed
Pilorget, L., Buckner, J. and Lundgren, J. G. (2010). Sterol limitation in a pollen-fed omnivorous lady beetle (Coleoptera: Coccinellidae). Journal of Insect Physiology 56, 8187.CrossRefGoogle Scholar
Roux, O., Gers, Ch. and Legal, L. (2006). When, during ontogeny, waxes in the blowfly (Calliphoridae) cuticle can act as phylogenetic markers. Biochemical Systematics and Ecology 34, 406416.CrossRefGoogle Scholar
Saunders, D. D. (2000). Larval diapause duration and fat metabolism in three geographical strains of the blow fly, Calliphora vicina. Journal of Insect Physiology 46, 509517.CrossRefGoogle ScholarPubMed
Smallbridge, C. J., Cooper, D. J. and Pinnock, D. E. (1995). The effect of the microsporidium Octosporea muscaedomesticae on adult Lucilia cuprina (Diptera: Calliphoridae). Journal of Invertebrate Pathology 66, 196197.CrossRefGoogle Scholar
Somme, L. (1964). Effects of glycerol on cold-hardiness in insects. Canadian Journal of Zoology 42, 87101.CrossRefGoogle Scholar
Somme, L. (1965). Further observations on glycerol and cold-hardiness in insects. Canadian Journal of Zoology 43, 765770.CrossRefGoogle Scholar
Svoboda, J. A. and Weirich, G. F. (1995). Sterol metabolism in the tobacco hornworm, Manduca sexta. A review. Lipids 30, 263267.CrossRefGoogle ScholarPubMed
Trabalon, M., Campan, M., Clement, J. L., Lange, C. and Miquel, M. (1992). Cuticular hydrocarbons of Calliphora vomitoria (Diptera): relation to age and sex. General and Comparative Endocrinology 85, 208216.CrossRefGoogle ScholarPubMed
Urbanek, A., Szadziewski, R., Stepnowski, P., Boros-Majewska, J., Gabriel, I., Dawgul, M., Kamysz, W., Sosnowska, D. and Gołębiowski, M. (2012). Composition and antimicrobial activity of fatty acids detected in the hygroscopic secretion collected from the secretory setae of larvae of the biting midge Forcipomyia nigra (Diptera: Ceratopogonidae). Journal of Insect Physiology 58, 12651276.CrossRefGoogle ScholarPubMed
Vásquez, G. M., Schal, C. and Silverman, S. (2008). Cuticular hydrocarbons as queen adoption cues in the invasive Argentine ant. Journal of Experimental Biology 211, 12491256.CrossRefGoogle ScholarPubMed
Wall, R. and Shearer, D. (2001). Veterinary Ectoparasites: Biology, Pathology and Control, 2nd Edn. Oxford: Wiley Blackwell.CrossRefGoogle Scholar
Ye, G., Li, K., Zhu, J., Zhu, G. and Hu, C. (2007). Cuticular hydrocarbon composition in pupal exuviae for taxonomic differentiation of six necrophagous flies. Journal of Medical Entomology 44, 450456.CrossRefGoogle ScholarPubMed
Yoder, Y. A. and Denlinger, D. L. (1990). Water balance in flesh fly pupae and water vapor absorption associated with diapause. Journal of Experimental Biology 157, 273286.CrossRefGoogle Scholar
Yoder, Y. A., Benoit, J. B., Denlinger, D. L. and Rivers, D. B. (2006). Stress-induced accumulation of glycerol in the flesh fly, Sarcophaga bullata: evidence indicating anti-desiccant and cryoprotectant functions of this polyol and a role for the brain in coordinating the response. Journal of Insect Physiology 52, 202214.CrossRefGoogle Scholar