Identification of Two Entomopathogenic Bacteria from a Nematode Pathogenic to the Oriental Beetle, Blitopertha orientalis

  • Yi, Young-Keun (Department of Bioresources Sciences, College of Natural Sciences, Andong National University) ;
  • Park, Hae-Woong (Department of Biotechnology, College of Engineering, Yonsei University) ;
  • Shrestha, Sony (Department of Bioresources Sciences, College of Natural Sciences, Andong National University) ;
  • Seo, Ji-Ae (Department of Bioresources Sciences, College of Natural Sciences, Andong National University) ;
  • Kim, Yong-Ook (Department of Biotechnology, College of Engineering, Yonsei University) ;
  • Shin, Chul-Soo (Department of Biotechnology, College of Engineering, Yonsei University) ;
  • Kim, Yong-Gyun (Department of Bioresources Sciences, College of Natural Sciences, Andong National University)
  • Published : 2007.06.30

Abstract

A pathogenic nematode, Butlerius sp., was isolated from Oriental beetle, Blitopertha orientalis. The infective juveniles exhibited dose-as well as time-dependent entomopathogenicity on the larvae of B. orientalis. Two bacterial species, Providencia vermicola (KACC 91278) and Flavobacterium sp. (KACC 91279), were isolated from the infective juveniles and identified. P. vermicola outnumbered Flavobacterium sp. in the nematode host, in which the colony density of P. vermicola was found to be 21 times higher than that of Flavobacterium sp. However, when the two bacterial species were cocultured in culture media without the nematode host, they showed similar growth rates. Both bacteria induced significant entomopathogenicity against Spodoptera exigua larvae infesting economically important vegetable crops, where P. vermicola was more potent than Flavobacterium sp.

Keywords

References

  1. Adams, B. J., A. M. Burnell, and T. O. Powers. 1998. A phylogenetic analysis of Heterorhabditis (Nemata: Rhabditidae) based on internal transcribed spacer 1 DNA sequence data. J. Nematol. 30: 22-39
  2. Aguillera, M. and G. Smart. 1993. Development, reproduction and pathogenicity of Steinernema scapterisci in monoxenic culture with different species of bacteria. J. Invertebr. Pathol. 62: 289-294 https://doi.org/10.1006/jipa.1993.1115
  3. 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
  4. Benson, H. G. 1990. Microbiological Applications, 4th Ed. Wm. C. Brown Publishers, Dubuque, IA
  5. Blaxter, M. L., P. De Ley, J. R. Garey, L. X. Liu, P. Scheldeman, A. Vierstraete, J. R. Vanflateran, L. Y. Mackey, M. Dorris, L. M. Frisse, J. T. Vida, and W. K. Thomas. 1998. A molecular framework for the phylum Nematoda. Nature 392: 71-75 https://doi.org/10.1038/32160
  6. Boemare, N. E. 2002. Biology, taxonomy and systematics of photorhabdus and xenorhabdus, pp. 35-56. In R. Gaugler (ed.). Entomopathogenic Nematology. CABI Publishing, New York, NY
  7. Brenner, D. J. 1984. Family I. Enterobacteriaceae, pp. 408- 516. In N. R. Krieg and J. G. Holt (eds.). Bergey's Manual of Systematic Bacteriology, Vol. 1. Williams & Wilkins, Baltimore, MD
  8. Brewer, M. J. and J. T. Trumble. 1989. Field monitoring for insecticide resistance in beet armyworm (Lepidoptera: Noctuidae). J. Econ. Entomol. 82: 1520-1526 https://doi.org/10.1093/jee/82.6.1520
  9. Brillard, J., C. Ribeiro, N. Boemare, M. Brehelin, and A. Givaudan. 2001. Two distinct hemolytic activities in Xenorhabdus nematophila are active against immunocompetent insect cells. Appl. Environ. Microbiol. 67: 2515-2525 https://doi.org/10.1128/AEM.67.6.2515-2525.2001
  10. Cho, S. and Y. Kim. 2004. Hemocyte apoptosis induced by entomopathogenic bacteria, Xenorhabdus and Photorhabdus, in Bombyx mori. J. Asia-Pacific Entomol. 7: 195-200 https://doi.org/10.1016/S1226-8615(08)60215-0
  11. Cho, S. J., K. M. Cho, E. C. Shin, W. J. Lim, S. Y. Hong, B. R. Choi, J. M. Kang, S. M. Lee, Y. H. Kim, H. Kim, and H. D. Yun. 2006. 16S rDNA analysis of bacterial diversity in three fractions of cow rumen. J. Microbiol. Biotechnol. 16: 92-101
  12. Converse, V. and P. S. Grewal. 1998. Virulence of entomopathogenic nematodes to the Western masked chafer Cyclocephala hirta (Coleoptera: Scarabaeidae). J. Econ. Entomol. 91: 428-432 https://doi.org/10.1093/jee/91.2.428
  13. Dowds, B. C. A. and A. Peters. 2002. Virulence mechanisms, pp. 79-98. In R. Gaugler (ed.). Entomopathogenic Nematology. CABI Publishing, New York
  14. Dunphy, G. B. and J. M. Webster. 1984. Interaction of Xenorhabdus nematophilus subsp. nematophilus with the haemolymph of Galleria mellonella. J. Insect Physiol. 30: 883-889 https://doi.org/10.1016/0022-1910(84)90063-5
  15. Dunphy, G. B. and J. M. Webster. 1987. Partially characterized components of the epicuticle of dauer juvenile, Steinernema feltiae, and their influence on haemocyte activity in Galleria mellonella. J. Parasitol. 73: 584-588 https://doi.org/10.2307/3282140
  16. 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. Invertebr. Pathol. 58: 40- 51 https://doi.org/10.1016/0022-2011(91)90160-R
  17. Forst, S., B. Dowds, 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
  18. Gho, H. G., S. G. Lee, B. P. Lee, K. M. Choi, and J. H. Kim. 1990. Simple mass-rearing of beet armyworm, Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae), on an artificial diet. Kor. J. Appl. Entomol. 29: 180-183
  19. Grewal, P. S., E. E. Lewis, R. Gaugler, and J. F. Campbell. 1994. Host-finding behaviour as a predictor of foraging strategy in entomopathogenic nematodes. Parasitology 108: 207-215 https://doi.org/10.1017/S003118200006830X
  20. Hwang, S. Y., S. Paik, S. H. Park, H. S. Kim, I. S. Lee, S. P. Kim, W. K. Baek, M. H. Suh, T. K. Kwon, J. W. Park, J. B. Park, J. J. Lee, and S. I. Suh. 2003. N-Phenethyl-2- phenylacetamide isolated from Xenorhabdus nematophilus induced apoptosis through caspases activation and calpainmediated Bax cleavage in U937 cells. Int. J. Oncol. 22: 151-157
  21. Holmes, B., R. J. Owen, and T. A. McMeekin. 1984. Genus Flavobacterium, pp. 353-361. In N. R. Krieg and J. G. Holt (eds.). Bergey's Manual of Systematic Bacteriology, Vol. 1. Williams & Wilkins, Baltimore, MD
  22. Holt, J. G., N. R. Krieg, P. H. A. Sneath, J. T. Staley, and S. T. Williams. 1994. Bergey's Manual of Determinative Bacteriology, 9th Ed. Williams & Wilkins, Baltimore, MD
  23. Humason, G. L. 1972. Animal Tissue Techniques, 3rd Ed. W. H. Freeman and Company, San Francisco, CA
  24. Hunt, D. J. 1980. Butlerius macrospiculum n. sp. and Cylindrocorpus walkeri n. sp. (Nematoda: Diplogastroidea) from St. Lucia, West Indies. Revue Nematol. 3: 155-160
  25. 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
  26. Jung, S. and Y. Kim. 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
  27. Jung, S. and Y. Kim. 2006. Synergistic effect of entomopathogenic bacteria (Xenorhabdus sp. and Photorhabdus temperata ssp. temperata) on the pathogenicity of Bacillus thuringiensis ssp. aizawai against Spodoptera exigua (Lepidoptera: Noctuidae). Environ. Entomol. 35: 1584- 1589 https://doi.org/10.1603/0046-225X(2006)35[1584:SEOEBX]2.0.CO;2
  28. Jung, S. and Y. Kim. 2007. Potentiating effect of Bacillus thuringiensis subsp. kurstaki on pathogenicity of entomopathogenic bacterium Xenorhabdus nematophila K1 against diamondback moth (Lepidoptera: Plutellae). J. Econ. Entomol. 100: 246-250 https://doi.org/10.1603/0022-0493(2007)100[246:PEOBTS]2.0.CO;2
  29. Kaya, H. K. 1990. Soil ecology, pp. 215-231. In R. Gaugler and H. K. Kaya (eds.), Entomopathogenic Nematodes in Biological Control. CRC, Boca Raton, FL
  30. 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
  31. Kim, J. S., J. Y. Choi, J. H. Chang, H. J. Shim, J. Y. Rho, B. R. Jin, and Y. H. Je. 2005. Characterization of an improved recombinant baculovirus producing polyhedra that contain Bacillus thuringiensis Cry1Ac crystal protein. J. Microbiol. Biotechnol. 15: 710-715
  32. Kim, Y., D. Ji, S. Cho, and Y. Park. 2005. Two groups of entomopathogenic bacteria, Photorhabdus and Xenorhabdus, share an inhibitory action against phospholipase $A_{2}$ to induce host immunodepression. J. Insect Physiol. 89: 258-264
  33. Lee, S., Y. Kim, and S. Han. 2000. An improved collecting method of the infective juveniles of the entomopathogenic nematode, Steinernema carpocapsae Weiser. Kor. J. Soil Zool. 5: 97-100
  34. Lee, Y. O., J. H. Park, and J. K. Park. 2005. Microbial characterization of excessive growing biofilm in sewer lines using molecular technique. J. Microbiol. Biotechnol. 15: 938-945
  35. Mahar, A. N., M. Munir, S. Elawad, S. R. Gowen, and N. G. M. Hague. 2004. Microbial control of diamondback moth, Plutella xylostella L. (Lepidoptera: Yponomeutidae) using bacteria (Xenorhabdus nematophila) and its metabolites from the entomopathogenic nematode Steinernema carpocapsae. J. Zhejiang Univ. Sci. 5: 1183-1190 https://doi.org/10.1631/jzus.2004.1183
  36. Martens, E. C. and H. Goodrich-Blair. 2005. The Steinernema carpocapsae intestinal vesicle contains a subcellular structure with which Xenorhabdus nematophila associates during colonization initiation. Cell Microbiol. 7: 1723-1735 https://doi.org/10.1111/j.1462-5822.2005.00585.x
  37. Martens, E. C., K. Heungens, and H. Goodrich-Blair. 2003. Early colonization events in the mutualistic association between Steinernema carpocapsae nematodes and Xenorhabdus nematophila bacteria. J. Bacteriol. 185: 3147-3154 https://doi.org/10.1128/JB.185.10.3147-3154.2003
  38. Navon, A., S. Keren, L. Salame, and I. Glazer. 1998. An edible-to-insects calcium alginate gel as a carrier for entomopathogenic nematodes. Biocon. Sci. Tech. 8: 429- 437 https://doi.org/10.1080/09583159830225
  39. Paik, S., Y. H. Park, S. I. Suh, H. S. Kim, I. S. Lee, M. K. Park, C. S. Lee, and S. H. Park. 2001. Unusual cytotoxic phenethylamides from Xenorhabdus nematophilus. Bull. Korean Chem. Soc. 22: 372-374
  40. Park, Y. and Y. Kim. 2000. Eicosanoids rescue Spodoptera exigua infected with Xenorhabdus nematophilus, the symbiotic bacteria to the entomopathogenic nematode Steinernema carpocapsae. J. Insect Physiol. 11: 1469-1476
  41. Penner, J. L. 1984. Genus XII. Providencia, pp. 494-496, In N. R. Krieg and J. G. Holt (eds.). Bergey's Manual of Systematic Bacteriology, Vol. 1. Williams & Wilkins, Baltimore, MD
  42. Raymond, M. 1985. Presentation d'un programme d'analyse log-probit pour micro-ordinateur. Cah. ORSTOM. Ser. Ent. Med. Parasitol. 22: 117-121
  43. Ribeiro, C., B. Duvic, P. Oliveira, A. Givaudan, F. Palha, N. Simoes, and M. Brehelin. 1999. Insect immunity - effects of factors produced by a nematobacterial complex on immunocompetent cells. J. Insect Physiol. 45: 677-685 https://doi.org/10.1016/S0022-1910(99)00043-8
  44. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular Cloning, A Laboratory Manual, 2nd Ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
  45. Schaad, N. M. 1988. Laboratory Guide for Identification of Plant Pathogenic Bacteria, 2nd Ed. APS Press, St. Paul, MN
  46. Somvanshi, V. S., E. Lang, B. Straubler, C. Sproer, P. Schumann, S. Ganguly, A. K. Saxena, and E. Stackebrandt. 2006. Providencia vermicola sp. nov., isolated from infective juveniles of the entomopathogenic nematode Steinernema thermophilum. Int. J. Syst. Evol. Microbiol. 56: 629-633 https://doi.org/10.1099/ijs.0.63973-0
  47. Somvanshi, V. S., E. Lang, S. Ganguly, J. Swiderski, A. K. Saxena, and E. Stackebrandt. 2006. A novel species of Xenorhabdus, family Enterobacteriaceae: Xenorhabdus indica sp. nov., symbiotically associated with entomopathogenic nematode Steinernema thermophilum Ganguly and Singh, 2000. Syst. Appl. Microbiol. 56: 629-633
  48. Stanley, D. W. 2000. Eicosanoids in Invertebrate Signal Transduction Systems. Princeton University Press, Princeton, NJ
  49. Stock, S. P., J. F. Campbell, and S. A. Nadler. 2001. Phylogeny of Steinernema Travassos, 1927 (Cephalobina: Steinernematidae) inferred from ribosomal DNA sequences and morphological characters. J. Parasitol. 87: 877-889 https://doi.org/10.1645/0022-3395(2001)087[0877:POSTCS]2.0.CO;2
  50. Van Laecke, K. and D. Degheele. 1991. Synergism of diflubenzuron and teflubenzuron in larvae of beet armyworm (Lepidoptera: Noctuidae). J. Econ. Entomol. 84: 785-789 https://doi.org/10.1093/jee/84.3.785
  51. Vrain, T. C., D. A. Wakarchuk, A. C. Levesque, and R. I. Hamilton. 1992. Intraspecific rDNA restriction fragment length polymorphism in the Xiphinema americanum group. Fund. Appl. Nematol. 15: 563-574
  52. Walsh, K. T. and J. M. Webster. 2003. Interaction of microbial populations in Steinernema (Steinernematidae, Nematoda) infected Galleria mellonella larvae. J. Invertebr. Pathol. 83: 118-126 https://doi.org/10.1016/S0022-2011(03)00079-X
  53. Wang, Y., J. F. Campbell, and R. Gaugler. 1995. Infection of entomopathogenic nematodes Steinernema glaseri and Heterorhabditis bacteriophora against Popillia japonica (Coleoptera: Scarabaeidae) larvae. J. Invertebr. Pathol. 66: 178-184 https://doi.org/10.1006/jipa.1995.1081
  54. Webster, J. M., G. Chen, and J. Li. 1998. Parasitic worms: An ally in the wax against the superbugs. Parasitol. Today 14: 161-163 https://doi.org/10.1016/S0169-4758(97)01220-9
  55. Weisburg, G. W., S. M. Barns, D. A. Pelletier, and D. J. Lane. 1991. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173: 697-703 https://doi.org/10.1128/jb.173.2.697-703.1991