Korean journal of applied entomology (한국응용곤충학회지)

Korean Society of Applied Entomology (한국응용곤충학회)
권호 표지
DOI QR코드

DOI QR Code

Study on Development of Novel Biopesticides Using Entomopathogenic Bacterial Culture Broth of Xenorhabdus and Photorhabdus

Xenorhabdus 및 Photorhabdus 세균 배양액을 이용한 생물농약 개발에 관한 연구

  • Seo, Sam-Yeol (Department of Bioresource Sciences, Andong National University) ;
  • Kim, Yong-Gyun (Department of Bioresource Sciences, Andong National University)
  • 서삼열 (안동대학교 자연과학대학 생명자원과학과) ;
  • 김용균 (안동대학교 자연과학대학 생명자원과학과)
  • Received : 2010.07.08
  • Accepted : 2010.09.06
  • Published : 2010.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Two groups of entomopathogenic bacteria, Xenorhabdus and Photorhabdus, are known to suppress insect immune responses by inhibiting eicosanoid biosynthesis. This study used these bacterial culture broths to develop novel biochemical insecticides against the diamondback moth, Plutella xylostella. Though the bacterial culture broths alone showed little insecticidal activity, they significantly enhanced pathogenicity of Bacillus thuringiensis against the fourth instar larvae of P. xylostella. Sterilization of the bacterial culture broth by autoclaving or $0.2\;{\mu}m$ membrane filtering did not influence the synergistic effect on the pathogenicity of B. thuringiensis. Three metablites identified in the culture broth of X. nematophila also showed similar synergistic effects. In field test, both entomopathogenic bacterial culture broth also enhanced the control efficacy of B. thuringiensis against P. xylostella.

Xenorhabdus 및 Photorhabdus 두 곤충병원세균은 곤충의 아이코사노이드 생합성을 억제하여 면역작용을 저하시키는 인자로 알려지고 있다. 본 연구는 이들 세균의 배양액을 이용하여 배추좀나방(Plutella xylostella)을 방제하는 새로운 생화학농약을 개발하려 추진되었다. 두 세균 배양액의 단독 처리는 배추좀나방의 생존력에 뚜렷한 영향을 주지 않았다. 그러나 비티(Bacillus thuringiensis) 생물농약과 혼합하여 처리할 경우 비티 단독 처리에 비해 배추좀나방 4령충에 대해서 현격하게 높은 병원성 증가효과를 주었다. 배양액의 세균 활성을 조사하기 위해 이 세균 배양액을 고온 멸균 및 $0.2\;{\mu}m$ 여과 멸균 처리하였다. 이렇게 처리된 멸균 배양액은 세균이 생존했던 배양액과 차이 없이 비티 생물농약의 병원력을 상승시켰다. X. nematophila 배양액에서 유래된 세 가지 대사물질도 세균배양액과 유사한 비티 병원력 상승효과를 보였다. 야외 배추좀나방 방제 시험에서도 세균배양액은 비티 생물농약의 방제가를 상승시키는 효과를 나타냈다.

Keywords

References

  1. Adams, B.J. and K.B. Nguyen. 2002. Taxonomy and systematics. pp. 1-33. In Entomopathogenic nematology, ed. by R. Gaugler. CABI Publishing, New York.
  2. Akhurst, R.J. 1980. Morphological and functional dimorphism in Xenorhabdus spp., bacteria symbiotically associated with the insect pathogenic nematodes Neoaplectana and Heterorhabditis. J. Gen. Microbiol. 121: 303-309.
  3. Broderick, N.A., K.F. Raffa and J. Handelsman. 2006. Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc. Natl. Acad. Sci. USA 103: 15196-15199. https://doi.org/10.1073/pnas.0604865103
  4. Corpping, L.G. and J.J. Menn. 2000. Biopesticides: a review of their action, application and efficacy. Pest Manage. Sci. 56: 651-676. https://doi.org/10.1002/1526-4998(200008)56:8<651::AID-PS201>3.0.CO;2-U
  5. Corpping, L.G. 2004. The manual of biocontrol agents. BCPC, Hampshire, UK.
  6. Dionne, M.S., L.N. Pham, M. Shirasu-Hiza and D.S. Schneider. 2006. Akt and FOXO dysregulation contribute to infection induced wasting in Drosophila. Curr. Biol. 16: 1977-1985. https://doi.org/10.1016/j.cub.2006.08.052
  7. Dunphy, G.B. and J.M. Webster. 1991. Antihemocytic surface components of Xenorhabdus nematophilus var. dutki and their modification by serum of nonimmune larvae of Galleria mellonella. J. lnvertebr. Pathol. 58: 40-51. https://doi.org/10.1016/0022-2011(91)90160-R
  8. Dunphy, G.B. and J.M. Webster. 1994. Interaction of Xenorhabdus nematophila subsp. nematophilus with the haemolymph of Galleria mellonella. J. lnsect Physiol. 30: 883-889.
  9. Ferre J. and J. Van Rie. 2002. Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 47: 501-533. https://doi.org/10.1146/annurev.ento.47.091201.145234
  10. ffrench-Constant, R.H., N. Waterfield and P. Dabom. 2005. lnsecticidal toxins from Photorhabdus and Xenorhabdus. pp. 239-253, In Comprehensive molecular insect science, eds. by L.I. Gilbert, I. Kostas and S.S. Gill. Elsevier, New York.
  11. Forcada, C., E. Alcacer, M.D. Garcera, A. Tato and R. Martinez. 1999. Resistance to Baciilus thuringiensis Cry Ac toxin in three strains of Heliothis virescent proteolytic and SIM study of the larval midgut. Arch. lnsect Bitchen. Physiol. 42: 51-63. https://doi.org/10.1002/(SICI)1520-6327(199909)42:1<51::AID-ARCH6>3.0.CO;2-6
  12. Forst, S. B. Dedos, N. Boemare and E. Stackebrandt. 1997. Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu. Rev. Microbiol. 51: 47-72. https://doi.org/10.1146/annurev.micro.51.1.47
  13. Gahan, L.J., F. Gould and D.G. Heckel. 2001. Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293: 857-86l. https://doi.org/10.1126/science.1060949
  14. Gassmann, A.J., J.A. Fabrick, M.S. Sisterson, E.R. Hannon, S.P. Stock, Y. Carriere and B.E. Tabashnik. 2009. Effects of pink bollworm resistance to Bacillus thuringiensis on phenoloxidase activity and susceptibility to entomopathogenic nematodes. J. Econ. Entomol. 102: 1224-1232. https://doi.org/10.1603/029.102.0348
  15. Gill, S.S., E.A. Cowles and P.V. Pietrantonio. 1992. The mode of action of Bacillus thuringiensis endotoxins. Annu. Rev. Entomol. 37: 615-636. https://doi.org/10.1146/annurev.en.37.010192.003151
  16. Gillespie, J.P., M.R. Kanost and T. Trenczek. 1997. Biological mediators of insect immunity. Annu Rev. Entomol. 42: 611-643. https://doi.org/10.1146/annurev.ento.42.1.611
  17. Harrison, D.A., R. Binari, T.S. Nahreini, M. Gilman and N. Perrimon. 1995. Activation of a Drosophila Janus kinase (JAK) causes hematopoietic neoplasia and developmental defects. EMBO J. 14: 2857-2865.
  18. Hoffman, C., H. Vanderbruggen, H. Hofte, J. Van Rie, S. Jansens and H. Van Mellaert. 1988. Specificity of Bacillus thuringiensis delta-endotoxins is correlated with the presence of high-affinity binding sites in the brush border membrane of target insect midguts. Proc. Natl. Acad. Sci. USA 85: 7844-7848. https://doi.org/10.1073/pnas.85.21.7844
  19. Jacot, A., H. Scheuber, J. Kurtz and M.W. Brinkhof. 2005. Juvenile immune system activation induces a costly upregulation of adult immunity in field crickets, Gryllus campestris. Proc. Biol. Sci. 272: 63-69. https://doi.org/10.1098/rspb.2004.2919
  20. Jenkins, J.I. and D.H. Dean. 2000. Exploring the mechanism of action of insecticidal proteins by genetic engineering methods. pp. 33-54. In Genetic engineering: principles and methods, vol. 22. eds. by K. Setlow. Plenum, New York.
  21. Ji, D., Y. Yi, G.H. Kang, Y.H. Choi, P. Kim, N.I. Baek and Y. Kim. 2004. Identification of an antibacterial compound, benzylideneacetone, from Xenorhabdus nematophila against major plant-pathogenic bacteria. FEMS Microbiol. Lett. 239: 241-248. https://doi.org/10.1016/j.femsle.2004.08.041
  22. Kang, S., S. Han and Y. Kim. 2004. Identification of an entomopathogenic bacterium, Photorhabdus temperata subsp. temperata, in Korea. J. Asia Pac. Entomol. 7: 331-337. https://doi.org/10.1016/S1226-8615(08)60235-6
  23. Kaya, H.K. and R. Gaugler. 1993. Entomopathogenic nematodes. Annu. Rev. Entomol. 38: 181-206. https://doi.org/10.1146/annurev.en.38.010193.001145
  24. Kim, H.H., Y.S. Seo, J.H. Lee and K.Y. Cho. 1990. Development of fenvalerate resistance in the diamondback moth, Plutella xylostella L. (Lepidoptera: Yponomeutidae) and its cross resistance. Kor. J. Appl. Entomol. 29: 194-200.
  25. Kim, J. 2009. Research trend in biopesticide development. www. bioin. co.kr.
  26. Kim, Y., D. Ji, S. Cho and Y. Park. 2005. Two groups of entomopathogenic bacteria, Photorhabdus and Xenorhabdusk, share an inhibitory action against Phospholipase $A_{2}$ to induce host innunodepression. J. Invertebr. Pathol. 89: 258-264. https://doi.org/10.1016/j.jip.2005.05.001
  27. Kwon, S. and Y. Kim. 2007. Immunosuppressive action of pyriproxyfen, a juvenile hormone analog, enhances pathogenicity of Bacillus thuringiensis subsp. kurstaki against diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae). Biol. Control. 42: 72-76. https://doi.org/10.1016/j.biocontrol.2007.03.006
  28. Kwon, S. and Y. Kim. 2008. Benzylideneacetone, an immunosuppressant, enhances virulence of Bacillus thuringiensis against beet armyworm (Lepidoptera: Noctuidae). J. Econ. Entomol. 101: 36-41. https://doi.org/10.1603/0022-0493(2008)101[36:BAIEVO]2.0.CO;2
  29. Luo, H., W.P. Hanratty and C.R. Dearolf. 1995. An amino acid substitution in the Drosophila hopTum-l Jak kinase causes leukemia-like hematopoietic defects. EMBO J. 14: 1412-1420.
  30. Oppert, B., K.J. Krammer, R. W. Beeman, D. Johnson and W.H. McGaughey. 1997. Proteinase-mediated insect resistance to Bacillus thuringiensis toxins. J. Biol. Chem. 272: 23473-23476. https://doi.org/10.1074/jbc.272.38.23473
  31. Park, N.J., S.C. Oh, Y.H. Choi, K.R. Choi and K.Y. Cho. 2004. lnheritance and cross resistance of phenthoate-selected diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae). J. Asia Pac. Entomol. 7: 233-237. https://doi.org/10.1016/S1226-8615(08)60221-6
  32. Park, Y., Y. Yi and Y. Kim. 1999. Identification and characterization of a symbiotic bacterium associated with Steinernema carpocapsae in Korea. J. Asia Pac. Entomol. 2: 105-111. https://doi.org/10.1016/S1226-8615(08)60038-2
  33. Park, Y. and Y. Kim. 2000. Eicosanoids rescue Spodoptera exigua infected with Xenorhabdus nematophila, the symbiotic bacteria to the entomopathogenic nematode Steinernema carpocapsae. J. Insect Physiol. 46: 1469-1476. https://doi.org/10.1016/S0022-1910(00)00071-8
  34. Pham, L.N. and D.S. Schneider. 2008. Evidence for specificity and memory in the insect innate immune response. pp. 97-127.In Insect Immunology, ed. by N.E. Beckage. 348 pp. Academic Press. New York.
  35. Pigott, C. and D.J. Ellar. 2007. Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol. Mol. Biol. Rev. 71: 255-281. https://doi.org/10.1128/MMBR.00034-06
  36. Qiu, P., P. Pan and S. Govind. 1998. A role for the Drosophila Toll/Cactus pathway in larval hematopoiesis. Development 125: 1909-1920.
  37. Rahman, M.M, H.L.S. Roberts, M. Sarjan, S. Asgari and O. Schmidt. 2004. Induction and transmission of Bacillus thuringiensis tolerance in the flour moth. Ephestia kuehniella. Proc. Natl. Acad. Sci. USA 101: 2696-2699. https://doi.org/10.1073/pnas.0306669101
  38. SAS Institute, Inc. 1989. SAS/STAT user's guide, Release 6.03, Ed. Cary, N.C.
  39. Schnepf, E., N. Crickmore, J. Van Rie, D. Lereclus, J. Baum, J. Feitelson, D.R. Zeigler and D.H. Dean. 1998. Bacillus thuringiensis and its pesticidal crystal proteins. J. Microbiol. Mol. Biol. Rev. 62: 775-806.
  40. Seo, S. and Y. Kim. 2009. Two entomopathogenic bacteria, Xenorhabdus nematophila K1 and Photorhabdus temperata subsp. temperata ANU101 secrete factors enhancing Bt pathogenicity against the diamondback moth, Plutella xylostella. Kor. J. Appl. Entomol. 38: 385-392. https://doi.org/10.5656/KSAE.2009.48.3.385
  41. Shrestha, S. and Y. Kim. 2008. Eicosanoids mediate prophenoloxidase release from oenocytoids in the beet armyworm Spodoptera exigua. Insect Biochem. Mol. Biol. 38: 99-112. https://doi.org/10.1016/j.ibmb.2007.09.013
  42. Shrestha, S. and Y. Kim. 2009. Biochemical characteristics of immune-associated phospholipase $A_{2}$ and its inhibition by an entomopathogenic bacterium, Xenorhabdus nematophila. J. Microbiol. 47: 774-782. https://doi.org/10.1007/s12275-009-0145-3
  43. Silva, C.P., N.R. Waterfield, P.J. Daborn, P. Dean, T. Chilver, C.P. Au, S. Sharma, U. Potter, S.E. Reynolds and R.H. ffrench-Constant. 2002. Bacterial infection of a model insect: Photorhabdus luminescens and Manduca sexta. Cell. Microbiol. 6: 329-339.
  44. Tabashnik, B.E., R.T. Roush, E.D. Earle and A.M. Shelton. 2000. Resistance to Bt toxins. Science 287: 42.
  45. Tabashnik, B.E., G.C. Unnithan., L. Masson., D.W. Crowder., X. Li and Y. Carriere. 2009. Asymmetrical cross-resistance between Bacillus thuringiensis toxins Cry1Ac and Cry2Ab in pink bollworm. Proc. Natl. Acad. Sci. USA 29: 11889-11894
  46. Talekar, N.S. and A.M. Shelton. 1993. Biology, ecology, and management of the diamondback moth. Annu. Rev. Entomol. 38: 275-301. https://doi.org/10.1146/annurev.en.38.010193.001423
  47. Tanada, Y. and Kaya, H.K. 1993. Insect pathology, Academic Press, San Diego.
  48. Wang, P., J-Z. Zhao, A. Rodrico-Simon, W. Kain, A.F Janmaat, A.M. Shelton, J. Ferre and J.H. Myers. 2007. Mechanism of resistance to Bacillus thuringiensis toxin Cry1Ac in a greenhouse population of the cabbage looper, Trichoplusia ni. Appl. Environ. Microbiol. 73: 1199-1207. https://doi.org/10.1128/AEM.01834-06
  49. Zhang, X., M. Candas, N. B. Griko, L. Rose-Young and L. A. Bulla Jr. 2005. Cytotoxicity of Bacillus thuringiensis Cry1Ab toxin depends on specific binding of the toxin to the cadherin receptor Bt-R1 expressed in insect cells. Cell Death Differ 12: 1407-1416. https://doi.org/10.1038/sj.cdd.4401675
  50. Zhang, X., N.B. Griko, S.K. Corona and L.A. Bulla, Jr. 2008. Enhanced exocytosis of the receptor BT-R(I) induced by the Cry1Ab toxin of Bacillus thuringiensis directly correlates to the execution of cell death. Comp. Biochem. Physiol. B. 149: 581-588. https://doi.org/10.1016/j.cbpb.2007.12.006

Cited by

  1. Comparative Analysis of Immunosuppressive Metabolites Synthesized by an Entomopathogenic Bacterium, Photorhabdus temperata ssp. temperata, to Select Economic Bacterial Culture Media vol.49, pp.4, 2010, https://doi.org/10.5656/KSAE.2010.49.4.409
  2. Toxicity Evaluation of 'Bt-Plus' on Parasitoid and Predatory Natural Enemies vol.51, pp.1, 2012, https://doi.org/10.5656/KSAE.2012.01.0.001
  3. Enhancement of Bt-Plus Toxicity by Unidentified Biological Response Modifiers Derived from the Bacterial Culture Broth of Xenornabdus nematiphila vol.54, pp.2, 2015, https://doi.org/10.5656/KSAE.2015.03.1.073
  4. Effect of Solubility of Thiamine Dilauryl Sulfate Solution through the Manufacture of the Nano Paticles on Antifungal Activity vol.19, pp.6, 2011, https://doi.org/10.7783/KJMCS.2011.19.6.464
  5. Structure-activity Analysis of Benzylideneacetone for Effective Control of Plant Pests vol.50, pp.2, 2011, https://doi.org/10.5656/KSAE.2011.04.0.15
  6. Effect of Cellular Phospholipase A2Inhibition on Enhancement of Bt Insecticidal Activity vol.53, pp.3, 2014, https://doi.org/10.5656/KSAE.2014.08.0.027
  7. Enhanced Pathogenicity of Bacillus thuringiensis Mixed with a Culture Broth of an Entomopathogenic Bacterium, Xenorhabdus sp. vol.51, pp.1, 2012, https://doi.org/10.5656/KSAE.2011.12.0.076
  8. Inhibitors Synthesized by Two Entomopathogenic Bacteria, Xenorhabdus nematophila and Photorhabdus temperata subsp. temperata vol.78, pp.11, 2012, https://doi.org/10.1128/AEM.00301-12