Korean journal of applied entomology (한국응용곤충학회지)

Korean Society of Applied Entomology (한국응용곤충학회)
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Control efficacy of BtPlus against two mosquitoes, Aedes koreicus and Culex vagans

한국숲모기와 줄다리집모기에 대한 비티플러스 방제 효과

  • Kim, Yonggyun (Department of Plant Medicals, College of Life Sciences, Andong National University) ;
  • Minoo, Sajjadian (Department of Plant Medicals, College of Life Sciences, Andong National University) ;
  • Ahmed, Shabbir (Department of Plant Medicals, College of Life Sciences, Andong National University)
  • Received : 2020.02.03
  • Accepted : 2020.02.13
  • Published : 2020.03.01
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Abstract

Two mosquito species were collected in still-water near farming area in Andong, Korea. Based on morphological characters, these two mosquitoes were identified as Aedes koreicus and Culex vagans, respectively. DNA barcode analyses supported the identification. An entomopathogenic bacterium, Bacillus thuringiensis subsp. israelensis (BtI), exhibited insecticidal activities against the two mosquito species and its virulence was more potent than that of B. thuringiensis subsp. kurstaki. It has been known that the bacterial metabolites of Xenorhabdus spp. suppress insect immunity and enhance pathogenicity of B. thuringiensis. This study tested the effect of the bacterial culture broth of Xenorhabdus spp. on enhancing BtI pathogenicity. Among three Xenorhabdus spp., culture broth of X. ehlersii (Xe) was relatively effective to enhance BtI pathogenicity against both mosquito species. Indeed, organic extracts of Xe culture broth suppressed the hemocyte-spreading behavior, suggesting the presence of immunosuppressant in the culture broth. These results suggest a formulation of BtPlus by mixing BtI spore and Xe culture broth to be applied to control the two mosquito species.

안동지역 농가 주변의 정수에서 두 종의 모기가 채집되었다. 형태적 특징을 바탕으로 이들이 한국숲모기(Aedes koreicus)와 줄다리집모기(Culex vagans)로 각각 동정되었다. 또한, DNA 바코드 서열을 분석한 결과 이러한 동정 결과를 뒷받침하였다. 이들 모기류 유충에 대해 곤충병원세균인 Bacillus thuringiensis subsp. israelensis (BtI)가 살충효과를 보였으며 유사한 B. thuringiensis subsp. kurstaki에 비해 우수하였다. 한편 곤충의 면역억제를 유발하여 B. thuringiensis의 병원력을 높인다고 알려진 Xenorhabdus 세균류의 배양액을 BtI에 첨가하여 이들 모기류에 대한 살충력 증가 효과 유무를 확인하였다. 분석에 이용된 3 종류의 Xenorhabdus 세균배양액 가운데 X. ehlersii (Xe)의 배양액이 비교적 다른 세균배양액에 비해 두 종의 모기류에 대해서 BtI의 살충력을 높이는 것으로 나타났다. 이를 바탕으로 Xe 세균배양액으로부터 유기용매 추출물의 생물활성을 분석한 결과 모기의 혈구 활착행동을 뚜렷이 억제시키는 면역억제자가 존재한다는 것을 확인하였다. 본 연구는 BtI와 Xe의 두 세균을 혼합한 비티플러스 미생물제제가 한국숲모기와 줄다리집모기의 방제에 효과적이라는 것을 제시한다.

Keywords

References

  1. Ahmed, S., Kim, Y., 2019. $PGE_2$ mediates cytoskeletal rearrangement of hemocytes via Cdc42, a small G protein, to activate actin remodeling factors in Spodoptera exigua (Lepidoptera: Noctuidae). Arch. Insect Biochem. Physiol. e21607, 1-17.
  2. Ahn, Y., 2011. Evaluation of insecticide resistance of vector mosquitoes. Seoul National University, Seoul, Korea.
  3. Apte-Deshpande, A., Paingankar, M., Gokhale, M.D., Deobagkar, D.N., 2012. Serratia odorifera a midgut inhabitant of Aedes aegypti mosquito enhances its susceptibility to dengue-2 virus. PLoS One 7, e40401. https://doi.org/10.1371/journal.pone.0040401
  4. Blandin, S., Shiao, S.-H., Moita, L.F., Janse, C.J., Waters, A.P., Kafatos, F.C., Levashina, E.A., 2004. Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116, 661-670 https://doi.org/10.1016/S0092-8674(04)00173-4
  5. Brown, L.D., Shapiro, L.L.M., Thompson, G.A., Estevez-Lao, T.Y., Hillyer, J.F., 2019. Transstadial immune activation in a mosquito: adults that emerge from infected larvae have stronger antibacterial activity in their hemocoel yet increased susceptibility to malaria infection. Ecol. Evol. 9, 6082-6095. https://doi.org/10.1002/ece3.5192
  6. Choi, S.Y., Oh, S.C., Cho, M.S., Paek, S.K., Kim, J.S., Kim, D.A., Gill, M.R., Youn, Y.N., Yu, Y.M., 2007. Bioassay of environment-friendly insecticides for management of mosquito, Culex pipiens molestus. Korean J. Appl. Entomol. 46, 261-267. https://doi.org/10.5656/KSAE.2007.46.2.261
  7. Ciocchetta, S., Prow, N.A., Darbro, J.M., Frentiu, F.D., Savino, S., Montarsi, F., Capelli, G., Aaskov, J.G., Devine, G.J., 2018. The new European invader Aedes (Finlaya) koreicus: a potential vector of chikungunya virus. Pathog. Glob. Health 112, 107-114. https://doi.org/10.1080/20477724.2018.1464780
  8. Dong, S., Kantor, A.M., Lin, J., Passarelli, A.L., Clem, R.J., Franz, A.W.E., 2016. Infection pattern and transmission potential of chikungunya virus in two New World laboratory-adapted Aedes aegypti strains. Sci. Rep. 6, 24729. https://doi.org/10.1038/srep24729
  9. Eom, S., Park, Y., Kim, H., Kim, Y., 2014. Development of a high efficient dual Bt-Plus insecticide using a primary form of an entomopathogenic bacterium, Xenorhabdus nematophila. J. Microbiol. Biotechnol. 24, 507-521. https://doi.org/10.4014/jmb.1310.10116
  10. Harbach, R.E., 2007. The Culicidae (Diptera): a review of taxonomy, classification and phylogeny. Zootaxa 1668, 591-638. https://doi.org/10.11646/zootaxa.1668.1.28
  11. Jegal, S., Jun, H., Kim-Jeon, M.D., Park, S.H., Ahn, S.K., Lee, J., Gong, Y.W., Joo, K., Kwon, M.J., Roh, J.Y., Lee, W.G., Lee, W., Bahk, Y.Y., Kim, T.S., 2019. Three-year surveillance of culicine mosquitoes (Diptera: Culicidae) for flavivirus infections in Incheon Metropolitan City and Hwaseong-si of Gyeonggi-do Province, Republic of Korea. Acta Trop. 202, 105258.
  12. Jeong, Y.S., Lee, D.K., 2003. Prevalence and seasonal abundance of the dominant mosquito species in a large march near coast of Ulsan. Korean J. Appl. Entomol. 42, 125-132.
  13. Jung, S., Kim, Y., 2006. Synergistic effect of Xenorhabdus nematophila K1 and Bacillus thuringiensis subsp. aizawai against Spodoptera exigua (Lepidoptera: Noctuidae). Biol. Control 39, 201-209. https://doi.org/10.1016/j.biocontrol.2006.07.002
  14. Kang, S.H., Jang, S.A., Han, J.B., Seo, D.K., Song, C.H., Kim, M.K., Kim, Y.L., Choi, S.H., Kim, I.K., Kim, G.H., 2005. Comparative efficacy of mosquito repellents against Aedes albopictus (Diptera: Culicidae). Korean J. Appl. Entomol. 44, 243-249.
  15. Kil, M.R., Kim, D.A., Paek, S.K., Kim, J.S., Choi, S.Y., Jin, D.Y., Yu, Y.N., 2008. Characterization of Bacillus thuringiensis subsp. tohokuensis CAB167 isolate against mosquito larva. Korean J. Appl. Entomol. 47, 457-465. https://doi.org/10.5656/KSAE.2008.47.4.457
  16. Kim, E., Kim, Y., 2014. A report on mixed occurrence of tobacco whitefly (Bemisia tabaci) biotypes B and Q in Oriental melon farms in Kyungpook province, Korea. Korean J. Appl. Entomol. 53, 465-472. https://doi.org/10.5656/KSAE.2014.09.0.038
  17. Kim, H.C., Lee, K.W., Richards, R.S., Schleich, S.S., Herman, W.E., Klein, T.A., 2003. Seasonal prevalence of mosquitoes collected from light traps in Korea (1999-2000). Korean J. Entomol. 33, 9-16. https://doi.org/10.1111/j.1748-5967.2003.tb00043.x
  18. Kim, Y.K., Lee, C.M., Lee, J.B., Bae, S.B., 2012. Seasonal prevalence of mosquitoes and ecological characteristics of Anopheline larval occurrence in Gimpo, Gyeonggi Province, Republic of Korea. Korean J. Appl. Entomol. 51, 305-312. https://doi.org/10.5656/KSAE.2012.07.0.017
  19. Kim, Y., Stanley, D., Ahmed, S., An, C., 2018. Eicosanoid-mediated immunity in insects. Dev. Comp. Immunol. 83, 130-143. https://doi.org/10.1016/j.dci.2017.12.005
  20. King, J.G., 2020. Developmental and comparative perspectives on mosquito immunity. Dev. Comp. Immunol. 103, 103458. https://doi.org/10.1016/j.dci.2019.103458
  21. King, J.G., Hillyer, J.F., 2012. Infection-induced interaction between the mosquito circulatory and immune systems. PLoS Pathog. 8, e1003058. https://doi.org/10.1371/journal.ppat.1003058
  22. Kudom, A.A., 2015. Larval ecology of Anopheles coluzzii in Cape Coast, Ghana: water quality, nature of habitat and implication for larval control. Malar. J. 14, 447. https://doi.org/10.1186/s12936-015-0989-4
  23. Kurucz, K., Kiss, V., Zana, B., Jacab, F., Kemenesi, G., 2018. Filarial nematode (order: Spirurida) surveillance in urban habitats, in the city of Pecs (Hungary) Parasitol. Res. 117, 3355-3360. https://doi.org/10.1007/s00436-018-6066-5
  24. Kwon, H., Arends, B.R., Smith, R.C., 2017. Late-phase immune responses limiting oocyst survival are independent of TEP1 function yet display strain specific differences in Anopheles gambiae. Parasites Vectors 10, 1-9. https://doi.org/10.1186/s13071-016-1943-1
  25. League, G.P., Hillyer, J.F., 2016. Functional integration of the circulatory, immune, and respiratory systems in mosquito larvae: pathogen killing in the hemocyte-rich tracheal tufts. BMC Biol. 14.
  26. Lee, H.I., 2003. Taxonomic review and revised keys of the Korean mosquitoes (Diptera: Culicidae). Korean J. Entomol. 33, 39-52. https://doi.org/10.1111/j.1748-5967.2003.tb00047.x
  27. Lee, K.W., Gupta, R.K., Wilde, J.A., 1984. Collection of adult and larval mosquitoes in U.S. army compounds in the Republic of Korea during 1979-1983. Korean J. Parasitol. 22, 102-108. https://doi.org/10.3347/kjp.1984.22.1.102
  28. Lima, E.P., Goulart, M.O., Rolim Neto, M.L., 2015. Meta-analysis of studies on chemical, physical and biological agents in the control of Aedes aegypti. BMC Public Health 15, 858. https://doi.org/10.1186/s12889-015-2199-y
  29. Luplertlop, N., Surasombatpattana, P., Patramool, S., Dumas, E., Wasinpiyamongkol, L., Saune, L., Hamel, R., Bernard, E., Sereno, D., Thomas, F., Piquemal D, Yssel H, Briant L, Misse D., 2011. Induction of a peptide with activity against a broad spectrum of pathogens in the Aedes aegypti salivary gland, following infection with dengue virus. PLoS Pathog. 7, e1001252. https://doi.org/10.1371/journal.ppat.1001252
  30. Marini, G., Arnoldi, D., Baldacchino, F., Capelli, G., Guzzetta, G., Merler, S., Montarsi, F., Rizzoli, A., Rosa, R., 2019. First report of the influence of temperature on the bionomics and population dynamics of Aedes koreicus, a new invasive alien species in Europe. Parasit. Vectors 12, 524. https://doi.org/10.1186/s13071-019-3772-5
  31. Miles, J.A., 1964. Some ecological aspects of the problem of arthropod-borne animal viruses in the Western Pacific and South-East Asia regions. Bull. World Health Organ. 30, 197-210.
  32. Montarsi, F., Martini, S., Dal Pont, M., Delai, N., Ferro Milone, N., Mazzucato, M., Soppelsa, F., Cazzola, L., Cazzin, S., Ravagnan, S., Ciocchetta, S., Russo, F., Capelli, G., 2013. Distribution and habitat characterization of the recently introduced invasive mosquito Aedes koreicus [Hulecoeteomyia koreica], a new potential vector and pest in north-eastern Italy. Parasit. Vectors 6, 292. https://doi.org/10.1186/1756-3305-6-292
  33. Montarsi, F., Ciocchetta, S., Devine, G., Ravagnan, S., Mutinelli, F., Frangipane di Regalbono, A., Otranto, D., Capelli, G., 2015. Development of Dirofilaria immitis within the mosquito Aedes (Finlaya) koreicus, a new invasive species for Europe. Parasit. Vectors 8, 177. https://doi.org/10.1186/s13071-015-0800-y
  34. Moreno-Garcia, M., Vargas, V., Ramirez-Bello, I., Hernandez-Martinez, G., Lanz-Mendoza, H., 2015. Bacterial exposure at the larval stage induced sexual immune dimorphism and priming in adult Aedes aegypti mosquitoes. PLoS One 10, e0133240. https://doi.org/10.1371/journal.pone.0133240
  35. Pakpour, N., Camp, L., Smithers, H.M., Wang, B., Tu, Z., Nadler, S.A., Luckhart, S., 2013. Protein kinase C-dependent signaling controls the midgut epithelial barrier to malaria parasite infection in anopheline mosquitoes. PLoS One 8, e76535. https://doi.org/10.1371/journal.pone.0076535
  36. Park, Y., 2015. Entomopathogenic bacterium, Xenorhabdus nematophila and Photorhabdus luminescens, enhances Bacillus thuringiensis Cry4Ba toxicity against yellow fever mosquito, Aedes aegypti (Diptera: Culicidae). J. Asia Pac. Entomol. 18, 459-463. https://doi.org/10.1016/j.aspen.2015.05.002
  37. Park, Y., Kim, Y., Yi, Y., 1999. Identification and characterization of a symbiotic bacterium associated Steinernema carpocapsae in Korea. J. Asia Pac. Entomol. 2, 105-111. https://doi.org/10.1016/S1226-8615(08)60038-2
  38. Park, Y., Jung, J., Kim, Y., 2016. A mixture of Bacillus thuringiensis subsp. israelensis with Xenorhabdus nematophila-cultured broth enhances toxicity against mosquitoes Aedes albopictus and Culex pipiens pallens. J. Econ. Entomol. 109, 1086-1093. https://doi.org/10.1093/jee/tow063
  39. Sadekuzzaman, M.D., Kim, Y., 2017. Specific inhibition of Xenorhabdus hominickii, an entomopathogenic bacterium, against different types of host insect phospholipase $A_2$. J. Invertebr. Pathol. 149, 97-105. https://doi.org/10.1016/j.jip.2017.08.009
  40. SAS Institute, Inc., 1989. SAS/STAT User's Guide, release 6.03 Ed. SAS Institute, Cary, NC.
  41. Seo, S., Kim, Y., 2011. Development of "Bt-Plus" biopesticide using entomopathogenic bacteria (Xenorhabdus nematophila, Photorhabdus temperata ssp. temperata) metabolites. Korean J. Appl. Entomol. 50, 171-178. https://doi.org/10.5656/KSAE.2011.07.0.24
  42. Seo, M.J., Gil, Y.J., Kim, T.H., Kim, H.J., Youn, Y.N., Yu, Y.M., 2010. Control effects against mosquitoes larva of Bacillus thuringiensis subsp. israelensis CAB199 isolate according to different formulations. Korean J. Appl. Entomol. 49, 151-158. https://doi.org/10.5656/KSAE.2010.49.2.151
  43. Seo, S., Lee, S., Hong, Y., Kim, Y., 2012. Phospholipase $A_2$ inhibitors synthesized by two entomopathogenic bacteria, Xenorhabdus nematophila and Photorhabdus temperata subsp. temperata. Appl. Environ. Microbiol. 78, 3816-3823. https://doi.org/10.1128/AEM.00301-12
  44. Sim, S., Ramirez, J.L., Dimopoulos, G., 2012. Dengue virus infection of the Aedes aegypti salivary gland and chemosensory apparatus induces genes that modulate infection and blood-feeding behavior. PLoS Pathog. 8, e1002631. https://doi.org/10.1371/journal.ppat.1002631
  45. Stanley, D., Kim Y. 2019. Prostaglandins and other eicosanoids in insects: biosynthesis and biological actions. Front. Physiol. 9, 1927. https://doi.org/10.3389/fphys.2018.01927
  46. Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., 2013. MEGA6: molecular evolutionary genetics analysis, version 6.0. Mol. Biol. Evol. 30, 2725-2729. https://doi.org/10.1093/molbev/mst197
  47. Wang, Z.Q., Perumaisamy, H., Wang, M., Shu, S., Ahn, Y.J., 2016. Larvicidal activity of Magnolia denudata seed hydrodistillate constituents and related compounds and liquid formulations towards two susceptible and two wild mosquito species. Pest Manag. Sci. 72, 897-906. https://doi.org/10.1002/ps.4064
  48. Whitfield, J., 2002. Portrait of a serial killer: a roundup of the history and biology of the malaria parasite. Nature https://doi.org/10.1038/news021001-6.
  49. Yeom, Y.S., 2017. Current status and outlook of mosquito-borne diseases in Korea. J. Korean Med. Assoc. 60, 468-474. https://doi.org/10.5124/jkma.2017.60.6.468
  50. Yu, H.S., Kim, H.C., 1989. Integrated control of vector mosquitoes with native fishes (Aplocheilus and Aphyocypris) and Bacillus thuringiensis (H-14) in natural rice fields of Korea. Korean J. Appl. Entomol. 28, 167-174.