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Insecticidal activity of a Moroccan strain of Streptomyces phaeochromogenes LD-37 on larvae, pupae and adults of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae)

Published online by Cambridge University Press:  04 November 2016

S.E. Samri ,
M. Baz ,
I. Ghalbane ,
S. El Messoussi ,
A. Zitouni ,
A. El Meziane  and
M. Barakate
S.E. Samri
Affiliation:
Laboratory of Biology and Biotechnology of Microorganisms, Department of Biology, Faculty of Sciences Semlalia, Cadi Ayyad University, P.O. Box. 2390 Marrakech 40000, Morocco Laboratory of Biotechnology Valorisation and Protection of Agro-Resources, Faculty of Science and Techniques Gueliz, Cadi Ayyad University, P.O. Box 549 Marrakech 40000, Morocco
M. Baz
Affiliation:
Laboratory of Biology and Biotechnology of Microorganisms, Department of Biology, Faculty of Sciences Semlalia, Cadi Ayyad University, P.O. Box. 2390 Marrakech 40000, Morocco
I. Ghalbane
Affiliation:
Laboratory of Molecular and Ecophysiological Modelisation, Faculty of Sciences Semlalia, Cadi Ayyad University, P.O. Box. 2390 Marrakech 40000, Morocco
S. El Messoussi
Affiliation:
Laboratory of Molecular and Ecophysiological Modelisation, Faculty of Sciences Semlalia, Cadi Ayyad University, P.O. Box. 2390 Marrakech 40000, Morocco
A. Zitouni
Affiliation:
Department of Natural Sciences, Ecole Normale Supérieure, Algers, Algeria
A. El Meziane
Affiliation:
Laboratory of Biotechnology Valorisation and Protection of Agro-Resources, Faculty of Science and Techniques Gueliz, Cadi Ayyad University, P.O. Box 549 Marrakech 40000, Morocco
M. Barakate*
Affiliation:
Laboratory of Biology and Biotechnology of Microorganisms, Department of Biology, Faculty of Sciences Semlalia, Cadi Ayyad University, P.O. Box. 2390 Marrakech 40000, Morocco
*
*Author for correspondence Phone: +212 524 43 46 49 ext. 433/436/517 Fax: +212 524 43 74 12 E-mail: [email protected]
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Abstract

The Mediterranean fruit fly (medfly), Ceratitis capitata, is considered the most important fruit pest worldwide. Its management is mainly based on the use of chemical insecticides. Although these conventional pesticides are effective at high doses, they cause considerable human health and environment problems. Thus, the aim of this study was to assess insecticidal activity of Moroccan actinobacteria against C. capitata. A total of 12 preselected actinobacteria isolated from various Moroccan habitats were screened for their insecticidal activity against larvae, pupae and adults of C. capitata. Four actinobacteria isolates were significantly active against the first-instar larvae, and nine were active against the medfly adult, while no significant mortality was obtained against the third-instar larval and pupal stages. Among the selected isolates, the biological screening revealed that strain Streptomyces LD-37, which showed 99.4% similarity with Streptomyces phaeochromogenes, exhibited the maximal corrected larval mortality of 98%. Moreover, the isolates AS1 and LD-37 showed the maximum significant corrected mortality against adults of 32.5 and 28.2%, respectively. The crude extract obtained from a fermented culture of strain S. phaeochromogenes LD-37 was separated into six fractions by thin layer chromatography. Fractions F3 and F4 caused a significant corrected larval mortality of 66.7 and 53.3%, respectively; whereas the maximum reduction in adult emergence was obtained with fraction F4. This finding could be useful for utilizing S. phaeochromogenes LD-37 as an alternative to chemical insecticides in pest management of C. capitata.

Keywords

Moroccan ActinobacteriascreeningbioinsecticideCeratitis capitata
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 107 , Issue 2 , April 2017 , pp. 217 - 224
Copyright
Copyright © Cambridge University Press 2016 

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References

Ababutain, I.M., Aziz, Z.K.A. & Al-Meshhen, N.A. (2012) Lincomycin antibiotic biosynthesis produced by Streptomyces sp. isolated from Saudi Arabia soil: I-Taxonomical, antimicrobial and insecticidal studies on the producing organism. Canadian Journal of Pure and Applied Sciences 6, 1905–1911.Google Scholar
Abbas, N., Khan, H.A. & Shad, S.A. (2014) Cross-resistance, genetics, and realized heritability of resistance to fipronil in the house fly, Musca domestica (Diptera: Muscidae): a potential vector for disease transmission. Parasitology Research 113, 1343–1352.Google Scholar
Abbott, W.S. (1925) A method of computing the effectiveness of an insecticide. Journal of Economic Entomology 18, 265–267.Google Scholar
Aboussaid, H., El-Aouame, L., El-Messoussi, S. & Oufdou, K. (2010) Biological activity of Bacillus thuringiensis (Berliner) strains on larvae and adults of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Journal of Environmental Protection 1, 337–345.Google Scholar
Aboussaid, H., Vidal-Quist, J. C., Oufdou, K., El Messoussi, S., Castañera, P. & González-Cabrera, J. (2011) Occurrence, characterization and insecticidal activity of Bacillus thuringiensis strains isolated from Argan fields in Morocco. Environmental Technology 32, 1383–1391.Google Scholar
Aluja, M. & Mangan, R.L. (2008) Fruit fly (Diptera: Tephritidae) host status determination: critical conceptual, methodological, and regulatory considerations. Annual Review of Entomology 53, 473–502.CrossRefGoogle ScholarPubMed
Barakate, M., Ouhdouch, Y., Oufdou, K. & Beaulieu, C. (2002) Characterization of rhizospheric soil streptomycetes from Moroccan habitats and their antimicrobial activities. World Journal of Microbiology and Biotechnology 18, 49–54.CrossRefGoogle Scholar
Basuki, W., Ilzuka, M., Ito, K., Furuichi, K. & Minamiura, N. (1992) Evidence for the existence of isozymes of glucose isomerase from Stretpomyces phaeochromogenes . Bioscience, Biotechnology, and Biochemistry 56, 180–185.Google Scholar
Becker, B., Lechevalier, M.P., Gordon, R.E. & Lechevalier, H. (1964) Rapid differentiation between Nocardia and Streptomyces by paper chromatography of whole-cell hydrolysates. Applied Microbiology 12, 421–423.Google Scholar
Benziane, T., Abbassi, M. & Bihi, E.T. (2003) Evaluation of two methods for integrated control against pests in citrus orchards. Journal of Applied Entomology 127, 51–63.Google Scholar
Berdy, J. (2005) Bioactive microbial metabolites. Journal of Antibiotics 58, 1–26.Google Scholar
Biondi, A., Mommaerts, V., Smagghe, G., Viñuela, E., Zappalà, L. & Desneux, N. (2012) The non-target impact of spinosyns on beneficial arthropods. Pest Management Science 68, 1523–1536.Google Scholar
Burns, R., Harris, D., Moreno, D. & Eger, J. (2001) Efficacy of spinosad bait sprays to control Mediterranean and Caribbean fruit flies (Diptera: Tephritidae) in commercial citrus in Florida. Florida Entomologist, 672–678.Google Scholar
Chang, C.L. (2004) Effect of amino acids on larvae and adults of Ceratitis capitata (Diptera: Tephritidae). Annals of the Entomological Society of America 97, 529–535.CrossRefGoogle Scholar
Demain, A.L. & Sanchez, S. (2009) Microbial drug discovery: 80 years of progress. Journal of Antibiotics 62, 5–16.Google Scholar
Demirel, N. (2007) Behavior paradigms in the Mediterranean fruit fly, Ceratitis capitata (Wiedemann). Journal of Entomology 4, 129–135.Google Scholar
Dhanasekaran, D. & Thangaraj, R. (2014) Microbial secondary metabolites are an alternative approaches against insect vector to prevent zoonotic diseases. Asian Pacific Journal of Tropical Disease 4, 253–261.CrossRefGoogle Scholar
Dow Agrosciences (2001) Spinosad Technical Bulletin. pp. 8. Indiana, Dow AgroSciences LLC.Google Scholar
Ekesi, S., Maniania, N. & Lux, S. (2002) Mortality in three African tephritid fruit fly puparia and adults caused by the entomopathogenic fungi, Metarhizium anisopliae and Beauveria bassiana . Biocontrol Science and Technology 12, 7–17.Google Scholar
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.Google Scholar
Ferencz, L. & Balog, A. (2010) A pesticide survey in soil, water and foodstuffs from central Romania. Journal of Earth and Environmental Sciences 5, 111–118.Google Scholar
Fitch, W.M. (1977) On the problem of discovering the most parsimonious tree. American Naturalist 111, 223–257.Google Scholar
Gassmann, A.J., Petzold-Maxwell, J.L., Clifton, E.H., Dunbar, M.W., Hoffmann, A.M., Ingber, D.A. & Keweshan, R.S. (2014) Field-evolved resistance by western corn rootworm to multiple Bacillus thuringiensis toxins in transgenic maize. Proceedings of the National Academy of Sciences 111, 5141–5146.Google Scholar
Gazit, Y., Gavriel, S., Akiva, R. & Timar, D. (2013) Toxicity of baited spinosad formulations to Ceratitis capitata: from the laboratory to the application. Entomologia Experimentalis et Applicata 147, 120–125.CrossRefGoogle Scholar
Goodfellow, M., Kämpfer, P., Busse, H., Trujillo, M., Suzuki, K., Ludwig, W. & Whitman, W. (2012) Bergey's Manual of Systematic Bacteriology, the Actinobacteria Part A. pp. 2083. New York, Springer.Google Scholar
Graziani, E.I., Ritacco, F.V., Bernan, V.S. & Telliez, J.-B. (2005) Phaeochromycins A−E, anti-inflammatory polyketides isolated from the soil Actinomycete Streptomyces phaeochromogenes LL-P018. Journal of Natural Products 68, 1262–1265.Google Scholar
Hafraoui, A., Harris, E.J. & Chakir, A. (1980) Plastic traps for detection and survey of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae) in Morocco. Proceedings of the Hawaiian Entomological Society 23, 199–204.Google Scholar
Harris, E.J., Hahrauni, A. & Toulouti, B. (1980) Mortality of nontarget insects by poison baits applied to control Mediterranean fruit fly (Ceratitis capitata) in Morocco. Proceedings of the Hawaiian Entomological Society 23, 227–229.Google Scholar
Hopwood, D.A., Bibb, M.J., Chater, K.F., Kieser, T., Bruton, C.J., Kieser, H.M., Lydiate, D.J., Smith, C.P., Ward, J.M. & Schrempf, H. (1985) Genetic Manipulation of Streptomyces – A Laboratory Manual. pp 196. Norwich, John Innes Foundation.Google Scholar
Hsu, J. & Feng, H. (2006) Development of resistance to spinosad in Oriental fruit fly (Diptera: Tephritidae) in laboratory selection and cross-resistance. Journal of Economic Entomology 99, 931–936.Google Scholar
Imoulan, A., Alaoui, A. & El Meziane, A. (2011) Natural occurrence of soil-borne entomopathogenic fungi in the Moroccan Endemic forest of Argania spinosa and their pathogenicity to Ceratitis capitata . World Journal of Microbiology and Biotechnology 27, 2619–2628.Google Scholar
Imoulan, A. & El Meziane, A. (2014) Pathogenicity of Beauveria bassiana isolated from Moroccan Argan forests soil against larvae of Ceratitis capitata (Diptera: Tephritidae) in laboratory conditions. World Journal of Microbiology and Biotechnology 30, 959–965.Google Scholar
Jemâa, J.M.-B. & Boushih, E. (2010) Cyromazine induced effects on larvae and adults of laboratory Tunisian strain of the Mediterranean fruit fly Ceratitis capitata . Tunisian Journal of Plant Protection 5, 213–221.Google Scholar
Karthik, L., Gaurav, K., Rao, K.V.B., Rajakumar, G. & Rahuman, A.A. (2011) Larvicidal, repellent, and ovicidal activity of marine actinobacteria extracts against Culex tritaeniorhynchus and Culex gelidus . Parasitology Research 108, 1447–1455.Google Scholar
Keller, B., Keller, E. & Lingens, F. (1985) Arogenate dehydrogenase from Streptomyces phaeochromogenes, Purification and properties. Biological Chemistry Hoppe-Seyler 366, 1063–1066.Google Scholar
Kheder, S.B., Trabelsi, I. & Aouadi, N. (2012) From chemicals to IPM against the Mediterranean fruit fly Ceratitis capitata (Diptera, Tephritidae). pp. 301–320 in Larramendy, M.L. & Soloneski, S. (Eds) Integrated Pest Management and Pest Control – Current and Future Tactics. Croatia, Intech.Google Scholar
Kim, O.-S., Cho, Y.-J., Lee, K., Yoon, S.-H., Kim, M., Na, H., Park, S.-C., Jeon, Y.S., Lee, J.-H. & Yi, H. (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. International Journal of Systematic and Evolutionary Microbiology 62, 716–721.Google Scholar
Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.Google Scholar
Kumari, B., Madan, V.K. & Kathpal, T.S. (2008) Status of insecticide contamination of soil and water in Haryana, India. Environmental Monitoring and Assessment 136, 239–244.Google Scholar
Lance, D.R., Woods, W.M. & Stefan, M. (2014) Invasive insects in plant biosecurity: case study – Mediterranean fruit fly. pp. 447–484 in Gordh, G. & McKirdy, S. (Eds) The Handbook of Plant Biosecurity. Netherlands, Springer.Google Scholar
Lane, D.J. (1991) 16S/23S rRNA sequencing. pp. 115–175 in Stackebrandt, E. & Goodfellow, M. (Eds) Nucleic Acid Techniques in Bacterial Systematics. NY, Wiley.Google Scholar
Larkin, M.A., Blackshields, G., Brown, N., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A. & Lopez, R. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.Google Scholar
Liquido, N.J., Shinoda, L.A. & Cunningham, R.T. (1991) Host Plants of the Mediterranean Fruit Fly (Diptera: Tephritidae): An Annotated World Review. pp. 52. US, Entomological Society of America.Google Scholar
Liu, H., Qin, S., Wang, Y., Li, W. & Zhang, J. (2008) Insecticidal action of Quinomycin A from Streptomyces sp. KN-0647, isolated from a forest soil. World Journal of Microbiology and Biotechnology 24, 2243–2248.Google Scholar
Magaña, C., Hernández-Crespo, P., Ortego, F. & Castañera, P. (2007) Resistance to Malathion in field populations of Ceratitis capitata . Journal of Economic Entomology 100, 1836–1843.Google Scholar
Mahajan, G. & Balachandran, L. (2014) Biodiversity in production of antibiotics and other bioactive compounds. Advances in Biochemical Engineering/Biotechnology 142, 1–22.Google Scholar
Malacrida, A.R., Gomulski, L.M., Bonizzoni, M., Bertin, S., Gasperi, G. & Guglielmino, C.R. (2007) Globalization and fruit fly invasion and expansion: the medfly paradigm. Genetica 131, 1–9.Google Scholar
Malan, A.P. & Manrakhan, A. (2009) Susceptibility of the Mediterranean fruit fly (Ceratitis capitata) and the Natal fruit fly (Ceratitis rosa) to entomopathogenic nematodes. Journal of Invertebrate Pathology 100, 47–49.Google Scholar
Mangan, R.L., Moreno, D.S. & Thompson, G.D. (2006) Bait dilution, spinosad concentration, and efficacy of GF-120 based fruit fly sprays. Crop Protection 25, 125–133.Google Scholar
Manrakhan, A., Kotze, C., Daneel, J.H., Stephen, P.R. & Beck, R.R. (2013) Investigating a replacement for Malathion in bait sprays for fruit fly control in South African citrus orchards. Crop Protection 43, 45–53.Google Scholar
Martinou, A.F., Seraphides, N. & Stavrinides, M.C. (2014) Lethal and behavioral effects of pesticides on the insect predator Macrolophus pygmaeus . Chemosphere 96, 167–173.Google Scholar
McSweeney, G.P. (1965) Two methods for the thin-layer chromatographic separation of terpene alcohols and identification by a colour reaction. Journal of Chromatography A 17, 183–185.Google Scholar
Molina, C.A., Cana-Roca, J.F., Osuna, A. & Vilchez, S. (2010) Selection of a Bacillus pumilus strain highly active against Ceratitis capitata (Wiedemann) larvae. Applied and Environmental Microbiology 76, 1320–1327.Google Scholar
Nagasawa, T., Kanzaki, H. & Yamada, H. (1984) Cystathionine gamma-lyase of Streptomyces phaeochromogenes. The occurrence of cystathionine gamma-lyase in filamentous bacteria and its purification and characterization. Journal of Biological Chemistry 259, 10393–10403.Google Scholar
Navarro-Llopis, V., Primo, J. & Vacas, S. (2013) Efficacy of attract-and-kill devices for the control of Ceratitis capitata . Pest Management Science 69, 478–482.Google Scholar
Nonomura, H. (1974) Key for classification and identification of 485 species of the Streptomyces included in the ISP. Journal of Fermentation Technology 52, 78–92.Google Scholar
Okami, Y. & Hotta, K. (1988) Search and discovery of new antibiotics. pp. 33–67 in Goodfellow, M., Williams, M. & Mordarski, S.T.M. (Eds) Actinomycetes in Biotechnology. New York, Academic Press.CrossRefGoogle Scholar
Ōmura, S. (2011) Microbial metabolites: 45 years of wandering, wondering and discovering. Tetrahedron 67, 6420–6459.Google Scholar
Osman, K.A. (2011) Pesticides and human health. pp. 205–230 in Stoytcheva, M. (Ed) Pesticides in the Modern World – Effects of Pesticides Exposure. Rijeka, InTech.Google Scholar
Ovruski, S.M. & Schliserman, P. (2012) Biological control of tephritid fruit flies in Argentina: historical review, current status, and future trends for developing a parasitoid mass-release program. Insects 3, 870–888.Google Scholar
Popp, J., Pető, K. & Nagy, J. (2013) Pesticide productivity and food security. A review. Agronomy for Sustainable Development 33, 243–255.Google Scholar
Price, N.R. & Stubbs, M.R. (1984) Some effects of CGA 72662 on larval development in the housefly, Musca domestica (L.). International Journal of Invertebrate Reproduction and Development 7, 119–126.Google Scholar
Quesada-Moraga, E., Martin-Carballo, I., Garrido-Jurado, I. & Santiago-Alvarez, C. (2008) Horizontal transmission of Metarhizium anisopliae among laboratory populations of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Biological Control 47, 115–124.Google Scholar
Saitou, N. & Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.Google Scholar
Samri, S.E., Baz, M., Jamjari, A., Aboussaid, H., El Messoussi, S., El Meziane, A. & Barakate, M. (2015) Preliminary assessment of insecticidal activity of Moroccan actinobacteria isolates against Mediterranean fruit fly (Ceratitis capitata). African Journal of Biotechnology 14, 859–866.Google Scholar
Sanchez, S. & Quinto, C.M. (1975) D-glucose isomerase: constitutive and catabolite repression-resistant mutants of Streptomyces phaeochromogenes . Applied Microbiology 30, 750–754.CrossRefGoogle ScholarPubMed
Shiomi, K., Hatae, K., Hatano, H., Matsumoto, A., Takahashi, Y., Jiang, C.-L., Tomoda, H., Kobayashi, S., Tanaka, H. & Ōmura, S. (2005) A new antibiotic, Antimycin A9, produced by Streptomyces sp. K01–0031. Journal of Antibiotics 58, 74–78.Google Scholar
Shirling, E.B. & Gottlieb, D. (1966) Methods for characterization of Streptomyces species. International Journal of Systematic Bacteriology 16, 313–340.CrossRefGoogle Scholar
Skelly, P.J. & Howells, A.J. (1987) Larval cuticle proteins of Lucilia cuprina: electrophoretic separation, quantification and developmental changes. Insect Biochemistry 17, 625–633.Google Scholar
Smaili, C., Wadjinny, J. & Bakri, A. (2010) Effect of spinosad, kaolin and protein bait spray on Ceratitis capitata (diptera: tephritidae) population in citrus orchards. p. 288 in Proceedings of the 8th International Symposium on fruit Flies of Economic Importance Organized by the Universitat of Politècnica, Valencia, 26 September–1 October 2010 Valencia, Universitat of Politècnica.Google Scholar
Su, T. & Cheng, M.L. (2013) Laboratory selection of resistance to Spinosad in Culex quinquefasciatus (Diptera: Culicidae). Journal of Medical Entomology 51, 297–488.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.Google Scholar
Tanaka, Y. & Omura, S. (1993) Agroactive compounds of microbial origin. Annual Review of Microbiology 47, 57–87.CrossRefGoogle ScholarPubMed
Thakur, I.S. (2011) Environmental Biotechnology: Basic Concepts and Applications. pp. 534. New Delhi, IK International Publishing House.Google Scholar
Van Pee, K.H. & Lingens, F. (1984) Detection of a bromoperoxidase in Streptomyces phaeochromogenes . FEBS Letters 173, 5–8.Google Scholar
Vijayabharathi, R., Kumari, B.R., Sathya, A., Srinivas, V., Abhishek, R., Sharma, H.C. & Gopalakrishnan, S. (2014) Biological activity of entomopathogenic actinomycetes against lepidopteran insects (Noctuidae: Lepidoptera). Canadian Journal of Plant Science 94, 759–769.CrossRefGoogle Scholar
Vinuela, E., Adan, A., Smagghe, G., Gonzalez, M., Medina, M.P., Budia, F., Vogt, H. & Estal, P.D. (2000) Laboratory effects of ingestion of Azadirachtin by two pests (Ceratitis capitata and Spodoptera exigua) and three natural enemies (Chrysoperla carnea, Opius concolor and Podisus maculiventris). Biocontrol Science and Technology 10, 165–177.Google Scholar
Vontas, J., Hernández-Crespo, P., Margaritopoulos, J.T., Ortego, F., Feng, H.-T., Mathiopoulos, K.D. & Hsu, J.-C. (2011) Insecticide resistance in Tephritid flies. Pesticide Biochemistry and Physiology 100, 199–205.Google Scholar
Wadjinny, J. & Bounfour, M. (2005) Management of the Mediterranean fruit fly, Ceratitis capitata (Wied.), in the Gharb area in Morocco. pp. 113–114 in Proceedings of the Area-Wide Control of Insect Pests organized by the FAO/IAEA, Vienna, Austria, 9–13 May 2005 Rome, FAO/IAEA.Google Scholar