Production of two entomopathogenic Aspergillus species and insecticidal activity against the mosquito Culex quinquefasciatus compared to Metarhizium anisopliae
[en] Entomopathogenic micro-organisms including fungi have become increasingly studied for integrated pest management. The spore productivity and insecticidal activity of two opportunistic insect pathogenic Aspergillus species (namely: Aspergillus clavatus Desmazieres and Aspergillus flavus Link (Ascomycota: Eurotiales, Trichocomaceae)) were compared to Metarhizium anisopliae sensu lato (Metchnikoff) Sorokin (Ascomycota: Hypocreales, Clavicipitaceae) for mosquito (Diptera: Culicidae) control. The production of aerial spores on wheat bran and white rice was investigated in solid-, semi-solid-, and liquid-state media supplemented with a nutritive solution. Wheat bran-based media were suitable for spore production and increased the spore yield in solid-state from 3 to 7 fold: A. clavatus produced 48.4 ± 5.2 and 15.7 ± 1.6 x 10^8 spores/g, A. flavus produced 22.3 ± 4.1 and 3.1 ± 2.5 x 10^8 spores/g, and M. anisopliae produced 39.6 ± 6.5 and 13.1 ± 2.6 x 10^8 spores/g of wheat bran or white rice, respectively. A. clavatus, A. flavus and M. anisopliae spores harvested from wheat bran-based solid-state media showed lethal concentrations (LC50) of 1.1, 1.8, and 1.3 x 10^8 spores/ml against Culex quinquefasciatus Say larvae in 72 h. Because A. clavatus and M. anisopliae displayed similar features when cultured under these conditions, our results suggest that insect pathogenic Aspergillus species may be as productive and virulent against mosquito larvae as a well-recognized entomopathogenic fungus. Wheat bran could advantageously be used in large-scale fermentation for a possible cost-effective pest control using these fungi.
Disciplines :
Entomology & pest control Microbiology
Author, co-author :
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
Zune, Quentin ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Bio-industries
Ndiaye, Mady; University Cheik Anta Diop > Faculté des Sciences et Techniques > Laboratoire de Biologie de la Reproduction
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
✱ These authors have contributed equally to this work.
Language :
English
Title :
Production of two entomopathogenic Aspergillus species and insecticidal activity against the mosquito Culex quinquefasciatus compared to Metarhizium anisopliae
W.Abbott, (1925). A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18, 265–267. doi:10.1093/jee/18.2.265a
S.B.Alves, (1986). Fungos entomopatogenicos. In S.Alves (Ed.), Controle microbiano de insetos (pp. 73–126). Sao Paulo: Manole.
S.B.Alves,, L.F.A.Alves,, R.B.Lopes,, R.M.Pereira,, & S.A.Vieira, (2002). Potential of some Metarhizium anisopliae isolates for control of Culex quinquefasciatus (Dipt., Culicidae). Journal of Applied Entomology, 126, 504–509. Retrieved from http://doi.org/10.1046/j.1439-0418.2002.00674.x doi: 10.1046/j.1439-0418.2002.00674.x
U.Amala,, T.Jiji,, & A.Naseema, (2012). Mass multiplication of entomopathogenic fungus, Paecilomyces lilacinus (Thom) Samson with solid substrates. Journal of Biopesticides, 5, 168–170.
T.Bawin,, F.Seye,, S.Boukraa,, J.Y.Zimmer,, F.Delvigne,, & F.Francis, (2015). La lutte contre les moustiques (Diptera: Culicidae): diversité des approches et application du contrôle biologique. The Canadian Entomologist, 147, 476–500. Retrieved from http://doi.org/10.4039/tce.2014.56 doi: 10.4039/tce.2014.56
N.Becker,, D.Petric,, M.Zgomba,, C.Boase,, M.Madon,, C.Dahl,, & A.Kaiser, (2010). Mosquitoes and their control. Berlin: Springer Berlin Heidelberg. Retrieved from http://doi.org/10.1007/978-3-540-92874-4
B.Bhadauria,, S.Puri,, & P.Singh, (2012). Mass production of entomopathogenic fungi using agricultural products. The Bioscan, an International Quarterly Journal of Life Sciences, 7, 229–232.
S.Brase,, A.Encinas,, J.Keck,, & C.F.Nising, (2009). Chemistry and biology of mycotoxins and related fungal metabolites. Chemical Reviews, 109, 3903–3990. Retrieved from http://doi.org/10.1021/cr050001f doi: 10.1021/cr050001f
F.R.van Breukelen,, S.Haemers,, R.H.Wijffels,, & A.Rinzema, (2011). Bioreactor and substrate selection for solid-state cultivation of the malaria mosquito control agent Metarhizium anisopliae. Process Biochemistry, 46, 751–757. Retrieved from http://doi.org/10.1016/j.procbio.2010.11.023 doi: 10.1016/j.procbio.2010.11.023
T.M.Butt,, & L.G.Copping, (2000). Fungal biological control agents. Pesticide Outlook, 11, 186–191. Retrieved from http://doi.org/10.1039/b008009h doi: 10.1039/b008009h
T.M.Butt,, B.P.J.Greenfield,, C.Greig,, T.G.G.Maffeis,, J.W.D.Taylor,, J.Piasecka,, … D.C.Eastwood, (2013). Metarhizium anisopliae pathogenesis of mosquito larvae: A verdict of accidental death. PLoS ONE, 8, e81686. Retrieved from http://doi.org/10.1371/journal.pone.0081686 doi: 10.1371/journal.pone.0081686
R.S.Cavalcante,, H.L.S.Lima,, G.A.S.Pinto,, C.A.T.Gava,, & S.Rodrigues, (2008). Effect of moisture on Trichoderma conidia production on corn and wheat bran by solid state fermentation. Food and Bioprocess Technology, 1, 100–104. Retrieved from http://doi.org/10.1007/s11947-007-0034-x doi: 10.1007/s11947-007-0034-x
B.Dorta,, A.Bosch,, J.A.Arcas,, & R.J.Ertola, (1990). High level of sporulation of Metarhizium anisopliae in a medium containing by-products. Applied Microbiology and Biotechnology, 33, 712–715. Retrieved from http://doi.org/10.1007/BF00604944 doi: 10.1007/BF00604944
H.C.Gugnani, (2003). Ecology and taxonomy of pathogenic aspergilli. Frontiers in Bioscience, 8, s346–s357. Retrieved from http://doi.org/10.2741/1002 doi: 10.2741/1002
U.Hölker,, M.Höfer,, & J.Lenz, (2004). Biotechnological advantages of laboratory-scale solid-state fermentation with fungi. Applied Microbiology and Biotechnology, 64, 175–186. Retrieved from http://doi.org/10.1007/s00253-003-1504-3 doi: 10.1007/s00253-003-1504-3
S.T.Jaronski, (2014). Mass production of entomopathogenic fungi: State of the art. In Mass production of beneficial organisms (pp. 357–413). San Diego: Elsevier. Retrieved from http://doi.org/10.1016/B978-0-12-391453-8.00011-X
S.M.Kanzok,, & M.Jacobs-Lorena, (2006). Entomopathogenic fungi as biological insecticides to control malaria. Trends in Parasitology, 22, 49–51. Retrieved from http://doi.org/10.1016/j.pt.2005.12.008 doi: 10.1016/j.pt.2005.12.008
S.Kar,, S.Sona Gauri,, A.Das,, A.Jana,, C.Maity,, A.Mandal,, … K.C.Mondal, (2013). Process optimization of xylanase production using cheap solid substrate by Trichoderma reesei SAF3 and study on the alteration of behavioral properties of enzyme obtained from SSF and SmF. Bioprocess and Biosystems Engineering, 36, 57–68. Retrieved from http://doi.org/10.1007/s00449-012-0761-x doi: 10.1007/s00449-012-0761-x
M.D.Leena,, S.Easwaramoorthy,, & R.Nirmala, (2003). In vitro production of entomopathogenic fungi Paecilomyces farinosus (Hotmskiold) and Paecilomyces lilacinus (Thom.) Samson using byproducts of sugar industry and other agro-industrial byproducts and wastes. Sugar Tech, 5, 231–236. Retrieved from http://doi.org/10.1007/BF02942478 doi: 10.1007/BF02942478
T.M.Lopez-Diaz,, & B.Flannigan, (1997). Production of patulin and cytochalasin E by Aspergillus clavatus during malting of barley and wheat. International Journal of Food Microbiology, 35, 129–136. Retrieved from http://doi.org/10.1016/S0168-1605(96)01211-1 doi: 10.1016/S0168-1605(96)01211-1
M.Maketon,, A.Amnuaykanjanasin,, & A.Kaysorngup, (2014). A rapid knockdown effect of Penicillium citrinum for control of the mosquito Culex quinquefasciatus in Thailand. World Journal of Microbiology and Biotechnology, 30, 727–736. Retrieved from http://doi.org/10.1007/s11274-013-1500-4 doi: 10.1007/s11274-013-1500-4
T.T.Mar,, N.Suwannarach,, & S.Lumyong, (2012). Isolation of entomopathogenic fungi from Northern Thailand and their production in cereal grains. World Journal of Microbiology and Biotechnology, 28, 3281–3291. Retrieved from http://doi.org/10.1007/s11274-012-1139-6 doi: 10.1007/s11274-012-1139-6
W.Marshall,, & J.Wadsworth, (1993). Rice science and technology. New York, NY: CRC Press.
S.S.Mohanty,, & S.Prakash, (2010). Comparative efficacy and pathogenicity of keratinophilic soil fungi against Culex quinquefasciatus larvae. Indian Journal of Microbiology, 50, 299–302. Retrieved from http://doi.org/10.1007/s12088-010-0051-8 doi: 10.1007/s12088-010-0051-8
A.M.L.de Moraes,, G.L.D.Costa,, M.Z.C.de Barcellos,, R.L.de Oliveira,, & P.C.de Oliveira, (2001). The entomopathogenic potential of Aspergillus spp. in mosquitoes vectors of tropical diseases. Journal of Basic Microbiology, 41, 45–49. Retrieved from http://doi.org/10.1002/1521-4028(200103)41:1 < 45::AID-JOBM45 > 3.0.CO;2-5 doi: 10.1002/1521-4028(200103)41:1<45::AID-JOBM45>3.0.CO;2-5
C.R.Pereira,, A.R.de Paula,, S.A.Gomes,, P.C.O.Pedra,, & R.I.Samuels, (2009). The potential of Metarhizium anisopliae and Beauveria bassiana isolates for the control of Aedes aegypti (Diptera: Culicidae) larvae. Biocontrol Science and Technology, 19, 881–886. Retrieved from http://doi.org/10.1080/09583150903147659 doi: 10.1080/09583150903147659
E.D.S.Pereira, E. da S., M.I.M.Sarquis,, R.L.Ferreira-Keppler,, N.Hamada,, & Y.B.Alencar, (2009). Filamentous fungi associated with mosquito larvae (Diptera: Culicidae) in municipalities of the Brazilian Amazon. Neotropical Entomology, 38, 352–359. Retrieved from http://doi.org/S1519-566X2009000300009 doi: 10.1590/S1519-566X2009000300009
J.I.Pitt, (2000). Toxigenic fungi and mycotoxins. British Medical Bulletin, 56, 184–192. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10885115 doi: 10.1258/0007142001902888
D.Robl,, L.B.Sung,, J.H.Novakovich,, P.R.D.Marangoni,, M.A.C.Zawadneak,, P.R.Dalzoto,, … I.C.Pimentel, (2009). Spore production in Paecilomyces lilacinus (Thom.) Samson strains on agro-industrial residues. Brazilian Journal of Microbiology, 40, 296–300. Retrieved from http://doi.org/10.1590/S1517-83822009000200016 doi: 10.1590/S1517-83822009000200016
M.Sabater-Vilar,, R.F.M.Maas,, H.De Bosschere,, R.Ducatelle,, & J.Fink-Gremmels, (2004). Patulin produced by an Aspergillus clavatus isolated from feed containing malting residues associated with a lethal neurotoxicosis in cattle. Mycopathologia, 158, 419–426. Retrieved from http://doi.org/10.1007/s11046-005-2877-x doi: 10.1007/s11046-005-2877-x
K.Sahayaraj,, & S.Namasivayam, (2008). Mass production of entomopathogenic fungi using agricultural products and by products. African Journal of Biotechnology, 7, 1907–1910.
E.Scholte,, B.G.J.Knols,, R.A.Samson,, & W.Takken, (2004). Entomopathogenic fungi for mosquito control: A review. Journal of Insect Science (Online), 4, 19. Retrieved from http://www.insectscience.org/4.19/ doi: 10.1093/jis/4.1.19
F.Seye,, T.Bawin,, S.Boukraa,, J.Y.Zimmer,, M.Ndiaye,, F.Delvigne,, & F.Francis, (2014a). Effect of entomopathogenic Aspergillus strains against the pea aphid, Acyrthosiphon pisum (Hemiptera: Aphididae). Applied Entomology and Zoology, 49, 453–458. Retrieved from http://doi.org/10.1007/s13355-014-0273-z doi: 10.1007/s13355-014-0273-z
F.Seye,, T.Bawin,, S.Boukraa,, J.Y.Zimmer,, M.Ndiaye,, F.Delvigne,, & F.Francis, (2014b). Pathogenicity of Aspergillus clavatus produced in a fungal biofilm bioreactor toward Culex quinquefasciatus (Diptera: Culicidae). Journal of Pesticide Science, 39, 127–132. Retrieved from http://doi.org/10.1584/jpestics.D14-006 doi: 10.1584/jpestics.D14-006
F.Seye,, O.Faye,, M.Ndiaye,, E.Njie,, & J.Marie Afoutou, (2009). 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, 9, 1–7. Retrieved from http://doi.org/10.1673/031.009.5301 doi: 10.1673/031.009.5301
F.Seye,, & M.Ndiaye, (2008). Compatibilité entre Aspergillus clavatus (Hyphomycètes) et l'huile de neem (Azadirachta indica) contre le moustique vecteur de filarioses Culex quinquefasciatus (Say, 1823) (Diptera: Culicidae). Bacteriologia, Virusologia, Parazitologia, Epidemiologia, 53, 43–48.
F.Seye,, M.Ndiaye,, O.Faye,, & J.M.Afoutou, (2012). Evaluation of entomopathogenic fungus Metarhizium anisopliae formulated with suneem (neem oil) against Anopheles gambiae s.l. and Culex quinquefasciatus adults. Malaria Chemotherapy, Control and Elimination, 1, 1–6. Retrieved from http://doi.org/10.4303/mcce/235494 doi: 10.4303/mcce/235494
F.Seye,, R.D.Ndione,, M.Touré,, M.Ndiaye,, S.Boukraa,, T.Bawin,, … F.Francis, (2013). 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, 1, 46–52. Retrieved from http://doi.org/10.15413/ajb.2013.0102
P.A.Shah,, & J.K.Pell, (2003). Entomopathogenic fungi as biological control agents. Applied Microbiology and Biotechnology, 61, 413–423. Retrieved from http://doi.org/10.1007/s00253-003-1240-8 doi: 10.1007/s00253-003-1240-8
L.C.A.da Silva,, T.L.Honorato,, T.T.Franco,, & S.Rodrigues, (2012). Optimization of chitosanase production by Trichoderma koningii sp. under solid-state fermentation. Food and Bioprocess Technology, 5, 1564–1572. Retrieved from http://doi.org/10.1007/s11947-010-0479-1 doi: 10.1007/s11947-010-0479-1
M.Thrake,, M.Thakur,, N.Malik,, & S.Ganger, (2011). Mass scale cultivation of entomopathogenic fungus Nomuraea rileyi using agricultural products and agro wastes. Journal of Biopesticides, 4, 176–179.
J.Varga,, K.Rigó,, J.Molnár,, B.Tóth,, S.Szencz,, J.Téren,, & Z.Kozakiewicz, (2003). Mycotoxin production and evolutionary relationships among species of Aspergillus section Clavati. Antonie van Leeuwenhoek, 83, 191–200. Retrieved from http://doi.org/10.1023/A:1023355707646 doi: 10.1023/A:1023355707646
WHO. (2005). Guidelines for laboratory and field testing of mosquito larvicides (No. WHO/CDS/WHOPES/GCDPP/2005.13). Geneva: Author.
Q.Zune,, A.Delepierre,, S.Gofflot,, J.Bauwens,, J.C.Twizere,, P.J.Punt,, … F.Delvigne, (2015). A fungal biofilm reactor based on metal structured packing improves the quality of a Gla::GFP fusion protein produced by Aspergillus oryzae. Applied Microbiology and Biotechnology, 99, 6241–6254. Retrieved from http://doi.org/10.1007/s00253-015-6608-z doi: 10.1007/s00253-015-6608-z
