Abstract
Aspergillus is a promising source of bioactive secondary metabolites. The addition of insect-derived material in the broth culture could trigger the biosynthesis of insecticidal and antimicrobial compounds by entomopathogenic fungus (EF). Insects inhabit diverse niches and interact with various bacteria, for this reason, when a fungus kills an insect should inhibit the insect’s gut bacteria to prevent the insect consumption by bacteria. According with this hypothesis, the EF is able to produce substances that inhibit bacteria growth or bacteria virulence strategies. In the present, investigation is demonstrated that the addition of Tribolium castaneum Herbst (Coleoptera: Tenebrionidae) components (2 % w/v) in a culture of saprophytic fungus Aspergillus parasiticus MOR 3 induces the production of a novel compound present inside mycelium 2-(4-bromophenyl)-2-oxoethyl benzoate, that is reported here for the first time as a natural product of A. parasiticus. In addition, increased significantly the fungal extracellular production of undecyl 4-fluorobenzoate. The mycelium extract (ME) at 250 μg per g of diet on adult population of T. castaneum produced an alteration of the feeding behavior of coleopteran insects (Repellency index = +30). The fraction derived from ME (Fr2) that contained the organobromine compound, 2-(4-bromophenyl)-2-oxoethyl benzoate had the highest inhibition of the Pseudomonas aeruginosa virulence factors like elastase enzyme (49 %) at 5 μg/ml and biofilm formation (43 %) at 100 μg/ml. The results suggest that the extract from mycelium of a non-aflatoxigenic A. parasiticus MOR 3 strain is a potential candidate as food coleopteran repellent as well as an anti-virulence strategy of P. aeruginosa.
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References
Akello J, Dubois T, Coyne D, Kyamanywa S (2008) Effect of endophytic Beauveria bassiana on populations of the banana weevil, Cosmopolites sordidus, and their damage in tissue-cultured banana plants. Entomol Exp Appl 129:157–165
Amaya S, Pereira JA, Borkosky SA, Valdez JC, Bardón A, Arena ME (2012) Inhibition of quorum sensing in Pseudomonas aeruginosa by sesquiterpene lactones. Phytomedicine 19:1173–1177
Barra P, Rosso L, Nesci A, Etcheverry M (2013) Isolation and identification of entomopathogenic fungi and their evaluation against Tribolium confusum, Sitophilus zeamais, and Rhyzopertha dominica in stored maize. J Pest Sci 86:217–226
Braga SM, de Medeiros FD, de Oliveira EJ, Macedo RO (2005) Development and validation of a method for the quantitative determination of aflatoxin contaminants in Maytenus ilicifolia by HPLC with fluorescence detection. Phytochem Anal 16:267–271
Caballero AR, Moreau JM, Engel LS, Marquart ME, Hill JM, O’Callaghan RJ (2001) Pseudomonas aeruginosa protease IV enzyme assays and comparison to other Pseudomonas proteases. Anal Biochem 290:330–337
Caballero-Gallardo K, Olivero-Verbel J, Stashenko EE (2011) Repellent activity of essential oils and some of their individual constituents against Tribolium castaneum herbst. J Agric Food Chem 9:1690–1696
Cathcart GR, Gilmore BF, Greer B, Harriott P, Walker B (2009) Inhibitor profiling of the Pseudomonas aeruginosa virulence factor LasB using N-alpha mercaptoamide template-based inhibitors. Bioorg Med Chem Lett 19:6230–6232
Cherry AJ, Banito A, Djegui D, Lomer C (2004) Suppression of the stem-borer Sesamia calamistis (Lepidoptera: Noctuidae) in maize following seed dressing, topical application and stem injection with African isolates of Beauveria bassiana. Int J Pest Manag 50:67–73
Daisy BH, Strobel GA, Castillo U, Ezra D, Sears J, Weaver DK, Runyon JB (2002) Naphthalene an insect repellent is produced by Muscodor vitigenus, a novel endophytic fungus. Microbiology 148:3737–3741
Degola F, Berni E, Spotti E, Ferrero I, Restivo FM (2009) Facing the problem of false positives: re-assessment and improvement of a multiplex RT-PCR procedure for diagnosis of A. flavus mycotoxin producers. Int J Food Microbiol 19:300–305
Frank HA (2013) Dosage rate, temperature, and food source provisioning affect susceptibility of Tribolium castaneum and Tribolium confusum to chlorfenapyr. J Pest Sci 86:507–513
Gilabert M, Ramos AN, Schiavone MM, Arena ME, Bardón A (2011) Bioactive sesqui-and diterpenoids from the Argentine liverwort Porella chilensis. J Nat Prod 74:574–579
Gribble GW (2000) The natural production of organobromine compounds. Environ Sci Pollut Res 7:37–49
Guruligappa P, Sword GA, Murdoch G, McGee PA (2010) Colonization of crop plants by fungal entomopathogens and their effects on two insect pests when in planta. Biol Control 55:34–41
Hagstrum DW, Flinn PW (1995) Integrated pest management. In: Subramanyam B, Hagstrum DW (eds) Integrated management of insects in stored products. Marcel Dekker, New York, pp 399–408
Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66
Inglis GD, Goettel MS, Strasser H (2001) Use of hyphomycetous fungi for managing insect pests. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents progress, problems and potential. CABI Publishing, Wallingford, pp 23–70
Jankov D, Inđić D, Kljajić P, Almaši R, Andrić G, Vuković S, Grahovac M (2013) Initial and residual efficacy of insecticides on different surfaces against rice weevil Sitophilus oryzae (L.). J Pest Sci 86:211–216
Jeffs LB, Khachatourians GG (1997) Toxic properties of Beauveria pigments on erythrocyte membranes. Toxicon 35:1351–1356
Kaur HP, Singh B, Kaur A, Kaur S (2013) Antifeedent and toxic activity of endophytic Alternaria alternate against tobacco caterpillar Spodoptera litura. J Pest Sci 86:543–550
Kikuchi H, Miyagawa Y, Nakamura K, Sahashi Y, Inatomi S, Oshima Y (2004) A novel carbon skeletal trichothecane, tenuipesine A, isolated from an entomopathogenic fungus, Paecilomyces tenuipes. Org Lett 6:4531–4533
Kumar R, Kumar A, Shekhar Prasa C, Kishore Dubey N, Samant R (2008) Insecticidal activity Aegle marmelos (L.) Correa essential oil against four stored grain insect pests. Int J Food Saf 10:39–49
Lee S, Nakajima I, Ihara F, Kinoshita H, Nihira T (2005) Cultivation of entomopathogenic fungi for the search of antibacterial compounds. Mycopathologia 160:321–325
Lee S, Nakajima I, Ihara F, Kinoshita H, Nihira T (2008) Identification of novel derivative of helvolic acid from Metarhizium anisopliae grown in medium with insect component. J Biosci Bioeng 105:476–480
MBTOC (2010) Montreal protocol on substances that deplete the ozone layer. http://ozone.unep.org/teap/Reports/MBTOC/MBTOC-Assesment-Report-2010.pdf. Accessed 28 Dec 2012
Michalaki M, Athanassiou C, Steenberg T, Buchelos C (2007) Effect of Paecilomyces fumosoroseus (Wise) Brown and Smith (Ascomycota: Hypocreales) alone or in combination with Diatomaceous Earth against Tribolium confusum Jacquelin du Val (Coleoptera: Tenebrionidae) and Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Biol Control 40:280–286
Moore D, Lord J, Smith S (2000) Pathogens. In: Subramanyam Bh, Hagstrum DW (eds) Alternatives to pesticides in stored-product, IPM. Kluwer, Dordrecht, pp 193–227
Navarro S (2012) The use of modified and controlled atmospheres for the disinfestation of stored products. J Pest Sci 85:301–322
Nugroho BW, Schwarz B, Wray V, Proksch P (1996) Insecticidal constituents from rhizomes of Zingiber cassumunar and Kaempferia rotunda. Phytochemistry 41:129–132
O’Toole GA, Kolter R (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signaling pathways: a genetic analysis. Mol Microbiol 28:449–461
Otto M (2004) Quorum-sensing control in Staphylococci—a target for antimicrobial drug therapy? FEMS Microbiol Lett 241:135–141
Padín SB, Fusé C, Urrutia MI, Dal Bello GM (2013) Toxicity and repellency of nine medicinal plants against Tribolium castaneum in stored wheat. Bull Insectol 66:45–49
Pascual-Villalobos MJ (1998) Repelencia, inhibición del crecimiento y toxicidad de extractos vegetales en larvas de Tribolium castaneum Herbst (Coleoptera: Tenebrinidae). Bol Sanid Veg 24:143–154
Pereira de Oliveira SM, Aguiar de Morais B, Abrantes Gonçalves C, Giordano-Dias CM, Luiz Vilela M, Peçanha Brazil R, d’Almeida JM, Dutra Asensi M, Pinto Mello R (2001) Digestive tract microbiota in female Lutzomyia longipalpis (Lutz & Neiva, 1912) (Diptera: Psychodidae) feeding on blood meal and sacarose plus blood meal. Cad Saúde Pública 17:229–232
Pitt JI, Hocking AD (2009) Fungi and Food Spoilage, 3rd edn. Springer Dordrecht, Heidelberg, New York
Prenafeta-Boldú FX, Luykx DMAM, Vervoort J, de Bont JAM (2001) Fungal metabolism of toluene: monitoring of fluorinated analogs by 19F nuclear magnetic resonance spectroscopy. Appl Environ Microbiol 67:1030–1034
Procopio S, Vendramin J, Ribeiro J, Santos J (2003) Bioactibidade de diversos pós de origen vegetal em relacáo a Sitophilus seamaiz Mots (Coleoptera: Curculionidae). Ciência Agrotéc 27:1231–1236
Quesada-Moraga E, Vey A (2004) Bassiacridin, a protein toxic for locusts secreted by the entomopathogenic fungus Beauveria bassiana. Mycol Res 108:441–452
Quesada-Moraga E, Munoz-Ledesma FJ, Santiago-Alvarez C (2009) Systemic protection of Papaver somniferum L., against Iraella luteipes (Hymenoptera: Cynipidae) by an endophytic strain of Beauveria bassiana (Ascomycota: Hypocreales). Environ Entomol 38:723–730
Soni N, Prakash S (2011) Aspergillus parasiticus metabolites efficacies against the mosquito larval (Culex quinquefasciatus, Anopheles stephensi and Aedes aegypti) population after column chromatography. Am J Microbiol 2:15–20
Stefanazzi N, Stadler T, Ferrero A (2011) Repellent and feeding deterrent activity of essential oils against the stored–grain pests Tribolium castaneum (Coleoptera: Tenebrionidae) and Sitophilus oryzae (Coleoptera: Curculionidae). Pest Manag Sci 67:639–646
Stewart PS, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358:135–138
Tanada Y, Kaya HK (1993) Insect pathology. Academic Press, San Diego
Tateda K, Comte R, Pechere JC, Koher T, Yamaguchi K, Van Delden C (2001) Azithromycin inhibits quorum sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother 45:1930–1933
Wijayaratne LKW, Fields PG, Arthur FH (2012) Effect of methoprene on the progeny production of Tribolium castaneum (Coleoptera: Tenebrionidae). Pest Manag Sci 68:217–224
Woerdenbag HJ, Windono T, Bos R, Riswan S, Quax WJ (2004) Composition of the essential oils of Kaempferia rotunda L. and Kaempferia angustifolia Roscoe rhizomes from Indonesia. Flavour Fragr J 19:145–148
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The authors thank ANCyT (PICT 2011 N°1202) and CIUNT for their grants as well as to entomologist Prof. Susana Beatriz Popich and mycologist Prof. Isabel Borges for their assistances.
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Communicated by C. G. Athanassiou.
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Cartagena, E., Marcinkevicius, K., Luciardi, C. et al. Activity of a novel compound produced by Aspergillus parasiticus in the presence of red flour beetle Tribolium castaneum against Pseudomonas aeruginosa and coleopteran insects. J Pest Sci 87, 521–530 (2014). https://doi.org/10.1007/s10340-014-0559-5
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DOI: https://doi.org/10.1007/s10340-014-0559-5