Histopathological effects of Aspergillus clavatus (Ascomycota: Trichocomaceae) on larvae of the southern house mosquito, Culex quinquefasciatus (Diptera: Culicidae) - 2016
Histopathological effects of Aspergillus clavatus (Ascomycota: Trichocomaceae) on larvae of the southern house mosquito, Culex quinquefasciatus (Diptera: Culicidae)
Microbial control; Entomopathogenic fungi; Aspergillosis; Bioassay; Histopathology; Electron microscopy
Résumé :
[en] Aspergillus clavatus (Ascomycota: Trichocomaceae) was previously found to be an opportunistic pathogen of mosquitoes (Diptera: Culicidae). In the present study, the mechanism leading to its insecticidal activity was investigated regarding histological damages on Culex quinquefasciatus larvae exposed to A. clavatus spores. Multiple concentration assays using spore suspensions (0.5 x 10^8 to 2.5 x 10^8 spores/ml) revealed 17.0% to 74.3% corrected mortalities after 48 h exposure. Heat-deactivated spores induced a lower mortality compared to non-heated spores suggesting that insecticidal effects are actively exerted. Spore-treated and untreated larvae were prepared for light microscopy as well as for scanning and transmission electron microscopy. Spores failed to adhere to the external body surface (except the mouth parts) of these aquatic immature stages but progressively filled the digestive tract where their metabolism seemed to activate. In parallel, the internal tissues of the larvae, i.e. the midgut wall, the skeletal muscles, and the cuticle-secreting epidermis, were progressively destroyed between 8 and 24 h of exposure. These observations suggest that toxins secreted by active germinating spores of A. clavatus in the digestive tract altered the larval tissues, leading to their necrosis and causing larval death. Fungal proliferation and sporulation then occurred during a saprophytic phase. A. clavatus enzymes or toxins responsible for these pathogenic effects need to be identified in further studies before any use of this fungus in mosquito control.
Disciplines :
Microbiologie Entomologie & lutte antiravageur
Auteur, co-auteur :
Bawin, Thomas ; Université de Liège - ULiège > Doct. sc. agro. & ingé. biol.
Seye, Fawrou; Université Cheik Anta Diop > Faculté des Sciences et Techniques > Laboratoire de Biologie de la Reproduction
Zimmer, Jean-Yves ; Université de Liège - ULiège > Sciences agronomiques > Entomologie fonctionnelle et évolutive
Raharimalala, Fara Nantenaina; Institut Pasteur de Madagascar > Unité d'entomologie médicale
Ndiaye, Mady; University Cheik Anta Diop > Faculté des Sciences et Techniques > Laboratoire de Biologie de la Reproduction
Compère, Philippe ; Université de Liège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Delvigne, Frank ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Bio-industries
Francis, Frédéric ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Entomologie fonctionnelle et évolutive
Langue du document :
Anglais
Titre :
Histopathological effects of Aspergillus clavatus (Ascomycota: Trichocomaceae) on larvae of the southern house mosquito, Culex quinquefasciatus (Diptera: Culicidae)
Abbott W.S. A method of computing effectiveness of insecticides. Journal of Economic Entomology 1925, 18:265-267.
Almehmadi R.M. Larvicidal, histopathological and ultra-structure studies of Matricharia chamomella extracts against the Rift Valley Fever mosquito Culex quinquefasciatus (Culicidae: Diptera). Journal of Entomology 2011, 8:63-72.
Bawin T., Seye F., Boukraa S., Zimmer J.-Y., Delvigne F., Francis F. La lutte contre les moustiques (Diptera: Culicidae): diversité des approches et application du contrôle biologique. The Canadian Entomologist 2015, 147:476-500. 10.4039/tce.2014.56.
Becker N., Petric D., Zgomba M., Dahl C., Boase C., Lane J., Kaiser A. Mosquitoes and Their Control 2010, Springer-Verlag, Heidelberg. 2nd edn.
Bergel F., Morrison A.L., Moss A.R., Rinderknecht H. An antibacterial substance from Aspergillus clavatus. Journal of the Chemical Society, 1944, 415-421.
Boukraa S., Raharimalala F.N., Zimmer J.-Y., Schaffner F., Bawin T., Haubruge E., Francis F. Reintroduction of the invasive mosquito species Aedes albopictus in Belgium in July 2013. Parasite 2013, 20:54. 10.1051/parasite/2013054.
Bräse S., Encinas A., Keck J., Nising C.F. Chemistry and biology of mycotoxins and related fungal metabolites. Chemical Reviews 2009, 109:3903-3990.
Brenner S.L., Korn E.D. The effect of cytochalasins on actin polymerization and actin ATPase provide insights into the mechanism of polymerization. The Journal of Biological Chemistry 1980, 255:841-844.
Bukhari T., Middelman A., Koenraadt C.J.M., Takken W., Knols B.G.J. Factors affecting fungus-induced larval mortality in Anopheles gambiae and Anopheles stephensi. Malaria Journal 2010, 9:22. 10.1186/1475-2875-9-22.
Bukhari T., Takken W., Koenraadt J.M.C. Development of Metarhizium anisopliae and Beauveria bassiana formulations for control of malaria mosquito larvae. Parasites & Vectors 2011, 4:23. 10.1186/1756-3305-4-23.
Butt T.M., Greenfield B.P.J., Greig C., Maffeis T.G.G., Taylor J.W.D., Piasecka J., Dudley E., Abdulla A., Dubovskiy I.M., Garrido-Jurado I., Quesada-Moraga E., Penny M.W., Eastwood D.C. Metarhizium anisopliae pathogenesis of mosquito larvae: a verdict of accidental death. PLOS ONE 2013, 8:e81686. 10.1371/journal.pone.0081686.
Cavados C.F.G., Majerowicz S., Chaves J.Q., Araújo-Coutinho C.J.P.C., Rabinovitch L. Histopathological and ultrastructural effects of δ-endotoxins of Bacillus thuringiensis serovar israelensis in the midgut of Simulium pertinax larvae (Diptera, Simuliidae). Memorias do Instituto Oswaldo Cruz 2004, 99:493-498.
Charnley A.K., Collins S.A. Entomopathogenic fungi and their role in pest control. The Mycota: environmental and microbial relationships 2007, 159-187. Springer-Verlag, Heidelberg. C.P. Kubicek, I.S. Druzhinina (Eds.).
Clardy J., Springer J.P., Büchi G., Matsuo K., Wrightman R. Tryptoquivaline and tryptoquivalone, two new tremorgenic metabolites of Aspergillus clavatus. Journal of the American Chemical Society 1975, 97:663-665.
Dagnelie P. Théorie et méthodes statistiques: applications agronomiques. Les méthodes d'inférence statistique 1970, vol. 2. Duculot, Gembloux.
de Moraes A.M., da Costa G.L., Barcellos M.Z., de Oliveira R.L., de Oliveira P.C. The entomopathogenic potential of Aspergillus spp. in mosquitoes vectors of tropical diseases. Journal of Basic Microbiology 2001, 41:45-49.
Federici B.A. Mosquito control by the Fungi Culicinomyces, Lagenidium and Coelomomyces. Microbial Control of Pests and Plant Diseases 1970-1980 1981, 555-572. Academic Press, London. H.D. Burges (Ed.).
Flannigan B., Pearce A.R. Aspergillus spoilage: spoilage of cereals and cereal products by the hazardous species Aspergillus clavatus. The Genus Aspergillus: from taxonomy and genetics to industrial application 1994, 115-127. Plenum Press, NY. K.A. Powell, A. Renwick, J.F. Peberdy (Eds.).
Goddard J. Mosquito-borne diseases. Infectious Diseases and Arthropods 2008, 31-79. Humana Press, Totowa. J. Goddard (Ed.).
Golebiowski M., Cerkowniaka M., Urbanek A., Dawgul M., Kamysz W., Bogus M.I., Stepnowski P. Identification and antifungal activity of novel organic compounds found in cuticular and internal lipids of medically important flies. Microbiological Research 2015, 170:213-222.
Gugnani H.C. Ecology and taxonomy of pathogenic aspergilli. Frontiers in Bioscience 2003, 8:s346-s357.
Hajek A.E., St Leger R.J. Interactions between fungal pathogens and insect hosts. Annual Review of Entomology 1994, 39:293-322.
Kanzok S.M., Jacobs-Lorena M. Entomopathogenic fungi as biological insecticides to control malaria. Trends in Parasitology 2006, 22:49-51. 10.1016/j.pt.2005.12.008.
Kerwin J.L. Oomycetes: Lagenidium giganteum. Journal of the American Mosquito Control Association 2007, 23:50-57.
Khachatourians G.G., Qazi S.S. Entomopathogenic fungi: biochemistry and molecular biology. The Mycota VI, Human and Animal Relationships 2008, 33-61. Springer-Verlag, Heidelberg. A.A. Brakhage, P.F. Zipfel (Eds.).
Koidsumi K. Antifungal action of cuticular lipids in insects. Journal of Insect Physiology 1957, 1:40-51.
Koua H.K., Han S.H., d'Almeida M.-A. Histopathologie d'Anopheles gambiae s.l. Giles, 1902 (Diptera, Culicidae) soumis à l'activité larvicide de l'extrait aqueux de Persea americana Miller, 1768 (Lauraceae). Bulletin de la Société de Pathologie Exotique 1998, 91:252-256.
Kubacki S.J. The analysis and occurrence of patulin in apple juice. Mycotoxins and Phytotoxins 1986, 293-304. Elsevier Science, Amsterdam. P.S. Steyn, Vleggaar (Eds.).
Kumar V., Singh G.P., Babu A.M. Surface ultrastructural studies on the germination, penetration and conidial development of Aspergillus flavus Link:Fries infecting silkworm, Bombyx mori Linn. Mycopathologia 2004, 157:127-135.
Lacey C.M., Lacey L.A., Roberts D.R. Route of invasion and histopathology of Metarhizium anisopliae in Culex quinquefasciatus. Journal of Invertebrate Pathology 1988, 52:108-118.
Lopez-Diaz T.M., Flannigan B. Production of patulin and cytochalasin E by Aspergillus clavatus during malting of barley and wheat. International Journal of Food Microbiology 1997, 35:129-136.
Lord J.C., Howard R.W. A proposed role for the cuticular fatty amides of Liposcelis bostrychophila (Psocoptera: Liposcelidae) in preventing adhesion of entomopathogenic fungi with dry-conidia. Mycopathologia 2004, 158:211-217.
Maketon M., Amnuaykanjanasin A., Kaysorngup A. A rapid knockdown effect of Penicillium citrinum for control of the mosquito Culex quinquefasciatus in Thailand. World Journal of Microbiology and Biotechnology 2014, 30:727-736.
Medlock J.M., Hansford K.M., Schaffner F., Versteirt V., Hendrickx G., Zeller H., Van Bortel W. A review of the invasive mosquitoes in Europe: ecology, public health risks, and control options. Vector-Borne and Zoonotic Diseases 2012, 12:435-447.
Miranpuri G.S., Khachatourians G.G. Infection sites of the entomopathogenic fungus Beauveria bassiana in the larvae of the mosquito Aedes aegypti. Entomologia Experimentalis et Applicata 1991, 59:19-27.
Mohanty S.S., Prakash S. Comparative efficacy and pathogenicity of keratinophilic soil fungi against Culex quinquefasciatus larvae. Indian Journal of Microbiology 2010, 50:299-302.
Mullen G., Durden L. Medical and Veterinary Entomology 2009, Elsevier Academic Press, Amsterdam. 2nd edn.
Nauen R. Insecticide resistance in disease vectors of public health importance. Pest Management Science 2007, 63:628-633.
Penn J., Mantle P.G., Bilton J.N., Sheppard R.N. Glyantrypine, a novel anthranilic acid-containing metabolite of Aspergillus clavatus. Journal of the Chemical Society, Perkin Transactions 1992, 1:1495-1496.
Pereira A.da S., Sarquis MI.de M., Ferreira-Keppler R.L., Hamada N., Alencar Y.B. Filamentous fungi associated with mosquito larvae (Diptera: Culicidae) in municipalities of the Brazilian Amazon. Neotropical Entomology 2009, 38:352-359.
Pitt J.I. Toxigenic fungi and mycotoxins. British Medical Bulletin 2000, 56:184-192.
Powell K., Renwick A., Pebordy J. The Genus Aspergillus: from taxonomy and genetics to industrial applications 1994, Springer US, Boston. http://doi.org/10.1007/978-1-4899-0981-7.
Rattner B.A. History of wildlife toxicology. Ecotoxicology 2009, 18:773-783.
Reiter P. Climate change and mosquito-borne disease. Environmental Health Perspectives 2001, 109:141-161.
Rivero A., Vézilier J., Weill M., Read A.F., Gandon S. Insecticide control of vector-borne diseases: when is insecticide resistance a problem?. PLOS Pathogens 2010, 6:e1001000. 10.1371/journal.ppat.1001000.
Sabater-Vilar M., Maas R.F.M., De Bosschere H., Ducatelle R., Johanna F.G. Patulin produced by an Aspergillus clavatus isolated from feed containing malting residues associated with a lethal neurotoxicosis in cattle. Mycopathologia 2004, 158:419-426.
Scholte E.J., Knols B.G.J., Samson R.A., Takken W. Entomopathogenic fungi for mosquito control: a review. Journal of Insect Science 2004, 4:19.
Schrank A., Vainstein M.H. Metarhizium anisopliae enzymes and toxins. Toxicon 2010, 56:1267-1274.
Seye F., Ndiaye M. Compatibilité entre Aspergillus clavatus (Hyphomycetes) et l'huile de neem (Azadirachta indica) contre le moustique vecteur de filarioses Culex quinquefasciatus (Say, 1823) (Diptera: Culicidae). Bacteriologia, Virusologia, Parazitologia, Epidemiologia 2008, 53:43-48.
Seye F., Faye O., Ndiaye M., Njie E., Afoutou J.M. Pathogenicity of the fungus, Aspergillus clavatus, isolated from the locust, Oedaleus senegalensis, against larvae of the mosquitoes Aedes aegypti, Anopheles gambiae and Culex quinquefasciatus. Journal of Insect Science 2009, 9:53.
Seye F., Ndione R.D., Touré M., Ndiaye M., Boukraa S., Bawin T., Zimmer J.-Y., Francis F. Laboratory and semi-field environment tests for the control efficacy of Metarhizium anisopliae formulated with neem oil (suneem) against Anopheles gambiae s.l. adult emergence. Academia Journal of Biotechnology 2013, 1:46-52.
Seye F., Bawin T., Boukraa S., Zimmer J.-Y., Ndiaye M., Delvigne F., Francis F. Pathogenicity of Aspergillus clavatus in a fungal biofilm bioreactor toward Culex quinquefasciatus (Diptera: Culicidae). Journal of Pesticide Science 2014, 39:127-132.
Seye F., Bawin T., Boukraa S., Zimmer J.-Y., Ndiaye M., Delvigne F., Francis F. Effect of entomopathogenic Aspergillus strains against the pea aphid, Acyrthosiphon pisum (Hemiptera: Aphididae). Applied Entomology and Zoology 2014, 49:453-458.
Shah P.A., Pell J.K. Entomopathogenic fungi as biological control agents. Applied Microbiology and Biotechnology 2003, 61:413-423.
Silva V.C., Pinheiro N.L., Scherer P.O., Falcão S.S., Ribeiro V.R., Mendes R.M., Chagas R., Cardozo-De-Almeida M., Dos Santos-Mallet J.R. Histology and ultrastructure of Aedes albopictus larval midgut infected with Bacillus thuringiensis var. israelensis. Microscopy Research and Technique 2008, 71:663-668.
Soares G.G. Pathogenesis of infection by the hyphomycetous fungus, Tolypocladium cylindrosporum in Aedes sierrensis and Culex tarsalis [Dip.: Culicidae]. Entomophaga 1982, 27:283-300.
Sosa-Gomez D.R., Boucias D.G., Nation J.L. Attachment of Metarhizium anisopliae to the southern green stink bug Nezara viridula cuticle and fungistatic effect of cuticular lipids and aldehydes. Journal of Invertebrate Pathology 1997, 69:31-39.
Suzuki T., Takeda M., Tanabe H. A new mycotoxin produced by Aspergillus clavatus. Chemical and Pharmaceutical Bulletin 1971, 19:1786-1788.
Urbanek A., Szadziewski R., Stepnowski P., Boros-Majewska J., Gabriel I., Dawgul M., Kamysz W., Sosnowska D., Gołebiowski M. 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 2012, 58:1265-1276.
Varga J., Rigo K., Molnar J., Toth B., Szencz S., Teren J., Kozakiewicz Z. Mycotoxin production and evolutionary relationships among species of Aspergillus section Clavati. Antonie van Leeuwenhoek 2003, 83:191-200.
World Health Organization Guidelines for Laboratory and Field Testing of Mosquito Larvicides 2005, World Health Organization, Geneva, Document WHO/CDS/WHOPES/GCDPP/13.
