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http://dx.doi.org/10.5941/MYCO.2015.43.2.137

Insecticidal Activity of Ethyl Acetate Extracts from Culture Filtrates of Mangrove Fungal Endophytes  

Abraham, Silva (Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Indonesia)
Basukriadi, Adi (Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Indonesia)
Pawiroharsono, Suyanto (Center for Bioindustrial Technology, Badan Pengkajian dan Penerapan Teknologi)
Sjamsuridzal, Wellyzar (Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Indonesia)
Publication Information
Mycobiology / v.43, no.2, 2015 , pp. 137-149 More about this Journal
Abstract
In the search for novel potent fungi-derived bioactive compounds for bioinsecticide applications, crude ethyl acetate culture filtrate extracts from 110 mangrove fungal endophytes were screened for their toxicity. Toxicity tests of all extracts against brine shrimp (Artemia salina) larvae were performed. The extracts with the highest toxicity were further examined for insecticidal activity against Spodoptera litura larvae and acetylcholinesterase (AChE) inhibition activity. The results showed that the extracts of five isolates exhibited the highest toxicity to brine shrimp at 50% lethal concentration ($LC_{50}$) values of 7.45 to 10.24 ppm. These five fungal isolates that obtained from Rhizophora mucronata were identified based on sequence data analysis of the internal transcribed spacer region of rDNA as Aspergillus oryzae (strain BPPTCC 6036), Emericella nidulans (strains BPPTCC 6035 and BPPTCC 6038), A. tamarii (strain BPPTCC 6037), and A. versicolor (strain BPPTCC 6039). The mean percentage of S. litura larval mortality following topical application of the five extracts ranged from 16.7% to 43.3%. In the AChE inhibition assay, the inhibition rates of the five extracts ranged from 40.7% to 48.9%, while eserine (positive control) had an inhibition rate of 96.8%, at a concentration of 100 ppm. The extracts used were crude extracts, so their potential as sources of AChE inhibition compounds makes them likely candidates as neurotoxins. The high-performance liquid chromatography profiles of the five extracts differed, indicating variations in their chemical constituents. This study highlights the potential of culture filtrate ethyl acetate extracts of mangrove fungal endophytes as a source of new potential bioactive compounds for bioinsecticide applications.
Keywords
Artemia salina; Ethyl acetate extracts; Insecticidal activity; Mangrove fungal endophytes; Spodoptera litura;
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1 Rukachaisirikul V, Rodglin A, Phongpaichit S, Buatong J, Sakayaroj J. $\alpha$-Pyrone and seiricuprolide derivatives from the mangrove-derived fungi Pestalotiopsis spp. PSU-MA92 and PSU-MA119. Phytochem Lett 2012;5:13-7.   DOI
2 Swe A, Jeewon R, Pointing SB, Hyde KD. Taxonomy and molecular phylogeny of Arthrobotrys mangrovispora, a new marine nematode-trapping fungal species. Bot Mar 2008;51:331-8.
3 Osono T. Colonization and succession of fungi during decomposition of Swida controversa leaf litter. Mycologia 2005;97:589-97.   DOI
4 Gibbons JG, Rokas A. The function and evolution of the Aspergillus genome. Trends Microbiol 2013;21:14-22.   DOI
5 Naikwade P, Mogle U, Sankpal S. Phyloplane mycoflora associated with mangrove plant Ceriops tagal (Perr.). Sci Res Rep 2012;2:85-7.
6 Bhimba BV, Agnel Defora Franco DA, Jose GM, Mathew JM, Joel EL. Characterization of cytotoxic compound from mangrove derived fungi Irpex hydnoides VB4. Asian Pac J Trop Biomed 2011;1:223-6.   DOI
7 White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. New York: Academic Press; 1990. p. 315-22.
8 An CY, Li XM, Luo H, Li CS, Wang MH, Xu GM, Wang BG. 4-Phenyl-3,4-dihydroquinolone derivatives from Aspergillus nidulans MA-143, an endophytic fungus isolated from the mangrove plant Rhizophora stylosa. J Nat Prod 2013;76:1896-901.   DOI
9 Elavarasi A, Rathna GS, Kalaiselvam M. Taxol producing mangrove endophytic fungi Fusarium oxysporum from Rhizophora annamalayana. Asian Pac J Trop Biomed 2012;2: S1081-5.   DOI
10 Ananda K, Sridhar KR. Diversity of endophytic fungi in the roots of mangrove species on the west coast of India. Can J Microbiol 2002;48:871-8.   DOI
11 Schulz B, Wanke U, Draeger S, Aust HJ. Endophytes from herbaceous plants and shrubs: effectiveness of surface sterilization methods. Mycol Res 1993;97:1447-50.   DOI
12 Poyton RO. The isolation and occurrence of Hyalochlorella marina. J Gen Microbiol 1970;62:189-94.   DOI
13 Torzilli AP, Sikaroodi M, Chalkley D, Gillevet PM. A comparison of fungal communities from four salt marsh plants using automated ribosomal intergenic spacer analysis (ARISA). Mycologia 2006;98:690-8.   DOI
14 Polishook JD, Bills GF, Lodge DJ. Microfungi from decaying leaves of two rain forest trees in Puerto Rico. J Ind Microbiol 1996;17:284-94.   DOI
15 Meyling NV. Methods for isolation of entomopathogenic fungi from the soil environment. Frederiksberg: University of Copenhagen; 2007.
16 Burtseva YV, Verigina NS, Sova VV, Pivkin MV, Zvyagintseva TN. O-glycosylhydrolases of marine filamentous fungi: ${\beta}$-1,3-glucanases of Trichoderma aureviride. Appl Biochem Microbiol 2003;39:475-81.   DOI
17 Kang SC, Park S, Lee DG. Purification and characterization of a novel chitinase from the entomopathogenic fungus, Metarhizium anisopliae. J Invertebr Pathol 1999;73:276-81.   DOI
18 Delalibera I Jr, Hajek AE, Humber RA. Use of cell culture media for cultivation of the mite pathogenic fungi Neozygites tanajoae and Neozygites floridana. J Invertebr Pathol 2003;84: 119-27.   DOI
19 Michaelsen A, Pinzari F, Ripka K, Lubitz W, Pinar G. Application of molecular techniques for identification of fungal communities colonizing paper material. Int Biodeterior Biodegrad 2006;58:133-41.   DOI
20 Brock PM, Doring H, Bidartondo MI. How to know unknown fungi: the role of a herbarium. New Phytol 2009;181:719-24.   DOI
21 Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997;25:4876-82.   DOI
22 Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987;4:406-25.
23 Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985;39:783-91.   DOI
24 Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980;16:111-20.   DOI
25 Supriyono A. Biologische aktive naturstoffe aus tropischen schammen Sudostasiens [dissertation]. Wurzburg: Bayerischen Julius-Maximilians-Universitat; 1997.
26 Ladhari A, Laarif A, Omezzine F, Haouala R. Effect of the extracts of the spiderflower, Cleome arabica, on feeding and survival of larvae of the cotton leafworm, Spodoptera littoralis. J Insect Sci 2013;13:61.
27 Ellman GL, Courtney KD, Andres V Jr, Featherstone RM. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 1961;7:88-95.   DOI
28 Paz Z, Bilkis I, Gerson U, Kerem Z, Sztejnberg A. Argovin, a novel natural product secreted by the fungus Meira argovae, is antagonistic to mites. Entomol Exp Appl 2011;140:247-53.   DOI
29 Abbott WS. A method of computing the effectiveness of an insecticide. J Econ Entomol 1925;18:265-7.
30 Finney DJ. Probit analysis. 3rd ed. London: Cambridge University Press; 1971.
31 Chen Y, Mao W , Tao H, Zhu W, Qi X, Chen Y, Li H, Zhao C, Yang Y, Hou Y, et al. Structural characterization and antioxidant properties of an exopolysaccharide produced by the mangrove endophytic fungus Aspergillus sp. Y16. Bioresour Technol 2011;102:8179-84.   DOI
32 Bhimba BV, Agnel Defora Franco DA, Mathew JM, Jose GM, Joel EL, Thangaraj M. Anticancer and antimicrobial activity of mangrove derived fungi Hypocrea lixii VB1. Chin J Nat Med 2012;10:77-80.   DOI
33 Joel EL, Bhimba BV. Evaluation of secondary metabolites from mangrove associated fungi Meyerozyma guilliermondii. Alex J Med 2013;49:189-94.   DOI
34 Bai ZQ, Lin X, Wang Y, Wang J, Zhou X, Yang B, Liu J, Yang X, Wang Y, Liu Y. New phenyl derivatives from endophytic fungus Aspergillus flavipes AIL8 derived of mangrove plant Acanthus ilicifolius. Fitoterapia 2014;95:194-202.   DOI
35 Liu D, Li XM, Meng L, Li CS, Gao SS, Shang Z, Proksch P, Huang CG, Wang BG. Nigerapyrones A-H, $\alpha$-pyrone derivatives from the marine mangrove-derived endophytic fungus Aspergillus niger MA-132. J Nat Prod 2011;74:1787-91.   DOI
36 Qiao MF, Ji NY, Liu XH, Li K, Zhu QM, Xue QZ. Indoloditerpenes from an algicolous isolate of Aspergillus oryzae. Bioorg Med Chem Lett 2010;20:5677-80.   DOI
37 Miao FP, Li XD, Liu XH, Cichewicz RH, Ji NY. Secondary metabolites from an algicolous Aspergillus versicolor strain. Mar Drugs 2012;10:131-9.   DOI
38 Meyer BN, Ferrigni NR, Putnam JE, Jacobsen LB, Nichols DE, McLaughlin JL. Brine shrimp: a convinient general bioassay for active plant constituents. Planta Med 1982;45:31-4.   DOI
39 Busi S, Peddikotla P, Upadyayula SM, Yenamandra V. Isolation and biological evaluation of two bioactive metabolites from Aspergillus gorakhpurensis. Rec Nat Prod 2009;3:161-4.
40 Busi S, Rajkumari J, Hnamte S. Feeding deterrence, acute toxicity and sublethal growth effects of kojic acid isolated from Aspergillus funiculosus. Nat Prod J 2014;4:18-22.
41 Hummelbrunner LA, Isman MB. Acute, sublethal, antifeedant, and synergistic effects of monoterpenoid essential oil compounds on the tobacco cutworm, Spodoptera litura (Lep., Noctuidae). J Agric Food Chem 2001;49:715-20.   DOI
42 Klaiklay S, Rukachaisirikul V, Phongpaichit S, Pakawatchai C, Saithong S, Buatong J, Preedanon S, Sakayaroj J. Anthraquinone derivatives from the mangrove-derived fungus Phomopsis sp. PSU-MA214. Phytochem Lett 2012;5:738-42.   DOI
43 Kumar S. Biopesticides: a need for food and environmental safety. J Biofertil Biopestic 2012;3:e107.
44 Arasu MV, Al-Dhabi NA, Saritha V, Duraipandiyan V, Muthukumar C, Kim SJ. Antifeedant, larvicidal and growth inhibitory bioactivities of novel polyketide metabolite isolated from Streptomyces sp. AP-123 against Helicoverpa armigera and Spodoptera litura. BMC Microbiol 2013;13:105.   DOI
45 Joel EL, Bhimba BV. Biological activity of secondary metabolites isolated from mangrove fungi Neurospora crassa. J Environ Biol 2013;34:729-32.
46 Casella TM, Eparvier V, Mandavid H, Bendelac A, Odonne G, Dayan L, Duplais C, Espindola LS, Stien D. Antimicrobial and cytotoxic secondary metabolites from tropical leaf endophytes: isolation of antibacterial agent pyrrocidine C from Lewia infectoria SNB-GTC2402. Phytochemistry 2013;96:370-7.   DOI
47 Quarles W. New biopesticides for IPM and organic production. IPM Pract 2013;33:1-20.
48 Nambiar GR, Raveendran K. Manglicolous marine fungi on Avicennia and Rhizophora along Kerala Coast (India). Middle East J Sci Res 2009;4:48-51.
49 Tarman K, Lindequist U, Wende K, Porzel A, Arnold N, Wessjohann LA. Isolation of a new natural product and cytotoxic and antimicrobial activities of extracts from fungi of Indonesian marine habitats. Mar Drugs 2011;9:294-306.   DOI
50 Sumampouw M, Bara R, Awaloei H, Posangi J. Uji efek antibakteri jamur endofit akar bakau Rhizophora stylosa terhadap bakteri Staphylococcus aureus dan Escherichia coli. J e-Biomedik 2014:2.
51 Chaeprasert S, Piapukiew J, Whalley AJ, Sihanonth P. Endophytic fungi from mangrove plant species of Thailand: their antimicrobial and anticancer potentials. Bot Mar 2010;53:555-64.
52 Kartika R, Bodhi W, Kepel B, Bara R. Uji daya hambat jamur endofit akar bakau Rhizophora apiculata terhadap bakteri Staphylococcus aureus dan Escherichiae coli. J e-Biomedik 2014:2.
53 Li H, Huang H, Shao C, Huang H, Jiang J, Zhu X, Liu Y, Liu L, Lu Y, Li M, et al. Cytotoxic norsesquiterpene peroxides from the endophytic fungus Talaromyces flavus isolated from the mangrove plant Sonneratia apetala. J Nat Prod 2011;74:1230-5.   DOI
54 Phoanda TC, Bara R, Wowor PM, Posangi J. Uji efek antibakteri jamur endofit akar tumbuhan bakau (Bruguiera gymnorrhiza) terhadap bakteri Escherichia coli dan Staphylococcus aureus. J e-Biomedik 2014:2.
55 Chen G, Lin Y, Vrijmoed LL, Fong WF. A new isochroman from the marine endophytic fungus 1893. Chem Nat Compd 2006;42:138-41.   DOI
56 Alongi DM. Present state and future of the world's mangrove forests. Environ Conserv 2002;29:331-49.
57 FAO Regional Forestry Commissions. The state of forest resource: a regional analysis [Internet]. Rome: Food and Agriculture Organization; 2010 [cited 2015 Feb 20]. Available from: http://www.fao.org/docrep/013/i2000e/i2000e01.pdf.
58 Holler U. Isolation, biological activity and secondary metabolite investigations of marine-derived fungi and selected host sponges [dissertation]. Braunschweig: Universitat Carolo-Wilhelmina; 1999.
59 Harwig J, Scott PM. Brine shrimp (Artemia salina L.) larvae as a screening system for fungal toxins. Appl Microbiol 1971; 21:1011-6.