The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Biological Control Potential of Bacillus amyloliquefaciens KB3 Isolated from the Feces of Allomyrina dichotoma Larvae

  • Nam, Hyo-Song (Jeonnam Bioindustry Foundation, BioControl Research Center) ;
  • Yang, Hyun-Ju (Jeonnam Bioindustry Foundation, BioControl Research Center) ;
  • Oh, Byung Jun (Jeonnam Bioindustry Foundation, BioControl Research Center) ;
  • Anderson, Anne J. (Department of Biology, Utah State University) ;
  • Kim, Young Cheol (Institute of Environmentally-Friendly Agriculture, Jeonnam National University)
  • Received : 2015.12.24
  • Accepted : 2016.02.20
  • Published : 2016.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

Most biocontrol agents for plant diseases have been isolated from sources such as soils and plants. As an alternative source, we examined the feces of tertiary larvae of the herbivorous rhino beetle, Allomyrina dichotoma for presence of biocontrol-active microbes. The initial screen was performed to detect antifungal activity against two common fungal plant pathogens. The strain with strongest antifungal activity was identified as Bacillus amyloliquefaciens KB3. The inhibitory activity of this strain correlated with lipopeptide productions, including iturin A and surfactin. Production of these surfactants in the KB3 isolate varied with the culture phase and growth medium used. In planta biocontrol activities of cell-free culture filtrates of KB3 were similar to those of the commercial biocontrol agent, B. subtilis QST-713. These results support the presence of microbes with the potential to inhibit fungal growth, such as plant pathogens, in diverse ecological niches.

Keywords

References

  1. Arguelles-Arias, A., Ongena, M., Halimi, B., Lara, Y., Brans, A., Joris, B. and Fickers, P. 2009. Bacillus amyloliquefaciens GA1 as a source of potent antibiotics and other secondary metabolites for biocontrol of plant pathogens. Microb. Cell Fact. 8:63. https://doi.org/10.1186/1475-2859-8-63
  2. Bajpai, V. K. and Kang, S. C. 2012. In vitro and in vivo inhibition of plant pathogenic fungi by essential oil and extracts of Magnolia liliflora Desr. J. Agr. Sci. Tech. 14:845-856.
  3. Ben Khedher, S., Boukedi, H., Kilani-Feki, O., Chaib, I., Laarif, A., Abdelkefi-Mesrati, L. and Tounsi, S. 2015. Bacillus amyloliquefaciens AG1 biosurfactant: putative receptor diversity and histopathological effects on Tuta absoluta midgut. J. Invertebr. Pathol. 132:42-47. https://doi.org/10.1016/j.jip.2015.08.010
  4. Bodour, A. A. and Miller-Maier, R. M. 1998. Application for a modified drop-collapse technique for surfactant quantitation and screening of biosurfactant-producing microorganisms. J. Microbiol. Methods 32:273-280. https://doi.org/10.1016/S0167-7012(98)00031-1
  5. Breznak, J. A. and Brune, A. 1994. Role of microorganisms in the digestion of lignocellulose by termites. Annu. Rev. Entomol. 36:453-487.
  6. Brune, A. 2003. Symbionts aiding digestion. In: Encyclopedia of insects, eds. by V. H. Resh and R. T. Carde, pp. 1102-1107. Academic Press, New York, NY, USA.
  7. Buensanteai, N., Yuen, G. Y. and Prathuangwong, S. 2008. The biocontrol bacterium Bacillus amlyliquefaciens KPS46 produces auxin, surfactin and extracellular proteins for enhanced growth of soybean plant. Thai J. Agri. Sci. 41:101-116.
  8. Cawoy, H., Bettiol, W., Fickers, P. and Ongena, M. 2011. Bacillus-based biological control of plant diseases. In: Pesticides in the modern world: pesticides use and management, ed. by M. Stoytcheva. InTech, Rijeka, Croatia.
  9. Chen, X. H., Koumoutsi, A., Scholz, R., Eisenreich, A., Schneider, K., Heinemeyer, I., Morgenstern, B., Voss, B., Hess, W. R., Reva, O., Junge, H., Voigt, B., Jungblut, P. R., Vater, J., Süssmuth, R., Liesegang, H., Strittmatter, A., Gottschalk, G. and Borriss, R. 2007. Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat. Biotechnol. 25:1007-1014. https://doi.org/10.1038/nbt1325
  10. Chen, Y., Yan, F., Chai, Y., Liu, H., Kolter, R., Losick, R. and Guo, J. H. 2013. Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environ. Microbiol. 15:848-864. https://doi.org/10.1111/j.1462-2920.2012.02860.x
  11. Choudhary, D. K. and Johri, B. N. 2009. Interactions of Bacillus spp. and plants--with special reference to induced systemic resistance (ISR). Microbiol. Res. 164:493-513. https://doi.org/10.1016/j.micres.2008.08.007
  12. Chowdhury, S. P., Hartmann, A., Gao, X. and Borriss, R. 2015. Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42: a review. Front Microbiol. 6:780.
  13. Dietel, K., Beator, B., Budiharjo, A., Fan, B. and Borriss, R. 2013. Bacterial traits involved in colonization of Arabidopsis thaliana roots by Bacillus amyloliquefaciens FZB42. Plant Pathol. J. 29:59-66. https://doi.org/10.5423/PPJ.OA.10.2012.0155
  14. Ernst, R., Arditti, J. and Healey, N. P. 1971. Biological effects of surfactants. I. Influence on the growth of orchid seedlings. New Phytol. 70:457-475. https://doi.org/10.1111/j.1469-8137.1971.tb02547.x
  15. Gardener, B. B., Kim, I. S., Kim, K. Y. and Kim, Y. C. 2014. Draft genome sequence of a chitinase-producing biocontrol bacterium, Lysobacter antibioticus HS124. Res. Plant Dis. 20:216-218. https://doi.org/10.5423/RPD.2014.20.3.216
  16. Ghribi, D. and Ellouze-Chaabouni, S. 2011. Enhancement of Bacillus subtilis lipopeptide biosurfactants production through optimization of medium composition and adequate control of aeration. Biotechnol. Res. Int. 2011:653654.
  17. Gregersen, T. 1978. Rapid method for distinction of gram-negative from gram-positive bacteria. Eur. J. Appl. Microbiol. Biotechnol. 5:123-127. https://doi.org/10.1007/BF00498806
  18. Ha, B. D. 2013. Isolation of antagonistic microorganism against plant pathogen from feces of Allomyrina dichotoma larva and large scale fermentation of Bacillus amyloliquefaciens KB3. M.S. thesis. Chonnam National University, Gwangju, Korea.
  19. Hornby, D. 1983. Suppressive soils. Ann. Rev. Phytopathol. 21:65-85. https://doi.org/10.1146/annurev.py.21.090183.000433
  20. Kang, B. R. 2012. Biocontrol of tomato Fusarium wilt by a novel genotype of 2,4-diacetylphloroglucinol-producing Pseudomonas sp. NJ134. Plant Pathol. J. 28:93-100. https://doi.org/10.5423/PPJ.NT.10.2011.0202
  21. Kim, J. C., Choi, G. J., Park, J. H., Kim, H. T. and Cho, K. Y. 2001. Activity against plant pathogenic fungi of phomalactone isolated from Nigrospora sphaerica. Pest. Manag. Sci. 57:554-559. https://doi.org/10.1002/ps.318
  22. Kim, P. I., Ryu, J., Kim, Y. H. and Chi, Y. T. 2010. Production of biosurfactant lipopeptides iturin A, fengycin and surfactin A from Bacillus subtilis CMB32 for control of Colletotrichum gloeosporioides. J. Microbiol. Biotechnol. 20:138-145.
  23. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120. https://doi.org/10.1007/BF01731581
  24. King, E. O., Ward, M. K. and Raney, D. E. 1954. Two simple media for the demonstration of pyocyanin and fluorescin. J. Lab Clin. Med. 44:301-307.
  25. Kupferschmied, P., Maurhofer, M. and Keel, C. 2013. Promise for plant pest control: root-associated pseudomonads with insecticidal activities. Front. Plant Sci. 4:287.
  26. Lee, B., Lee, S. and Ryu, C. M. 2012. Foliar aphid feeding recruits rhizosphere bacteria and primes plant immunity against pathogenic and non-pathogenic bacteria in pepper. Ann. Bot. 110:281-290. https://doi.org/10.1093/aob/mcs055
  27. Li, H., Soares, M. A., Torres, M. S., Bergen, M. and White J. F. Jr. 2015. Endophytic bacterium, Bacillus amyloliquefaciens, enhances ornamental hosta resistance to diseases and insect pests. J. Plant Interact. 10:224-229. https://doi.org/10.1080/17429145.2015.1056261
  28. Martin, P. A. and Travers, R. S. 1989. Worldwide abundance and distribution of Bacillus thuringiensis isolates. Appl. Environ. Microbiol. 55:2437-2442.
  29. Mendes, R., Kruijt, M., de Bruijn, I., Dekkers, E., van der Voort, M., Schneider, J. H., Piceno, Y. M., DeSantis, T. Z., Andersen, G. L., Bakker, P. A. and Raaijmakers, J. M. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097-1100. https://doi.org/10.1126/science.1203980
  30. Mezghanni, H., Khedher, S. B., Tounsi, S. and Zouari, N. 2012. Medium optimization of antifungal activity production by Bacillus amyloliquefaciens using statistical experimental design. Prep. Biochem. Biotechnol. 42:267-278. https://doi.org/10.1080/10826068.2011.614989
  31. Moran, N. A., Russell, J. A., Koga, R. and Fukatsu, T. 2005. Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Appl. Environ. Microbiol. 71:3302-3310. https://doi.org/10.1128/AEM.71.6.3302-3310.2005
  32. Nadarasah, G. and Stavrinides, J. 2011. Insects as alternative hosts for phytopathogenic bacteria. FEMS Microbiol. Rev. 35:555-575. https://doi.org/10.1111/j.1574-6976.2011.00264.x
  33. Nihorimbere, V., Cawoy, H., Seyer, A., Brunelle, A., Thonart, P. and Ongena, M. 2012. Impact of rhizosphere factors on cyclic lipopeptide signature from the plant beneficial strain Bacillus amyloliquefaciens S499. FEMS Microbiol. Ecol. 79:176-191. https://doi.org/10.1111/j.1574-6941.2011.01208.x
  34. Nitschke, M. and Pastore, G. M. 2006. Production and properties of a surfactant obtained from Bacillus subtilis grown on cassava wastewater. Bioresour. Technol. 97:336-341. https://doi.org/10.1016/j.biortech.2005.02.044
  35. Olcott, M. H., Henkels, M. D., Rosen, K. L., Walker, F. L., Sneh, B., Loper, J. E. and Taylor, B. J. 2010. Lethality and developmental delay in Drosophila melanogaster larvae after ingestion of selected Pseudomonas fluorescens strains. PLoS One 5:e12504. https://doi.org/10.1371/journal.pone.0012504
  36. Ongena, M. and Jacques, P. 2008. Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol. 16:115-125. https://doi.org/10.1016/j.tim.2007.12.009
  37. Park, J. Y., Oh, S. A., Anderson, A. J., Neiswender, J., Kim, J. C. and Kim, Y. C. 2011. Production of the antifungal compounds phenazine and pyrrolnitrin from Pseudomonas chlororaphis O6 is differentially regulated by glucose. Lett. Appl. Microbiol. 52:532-537. https://doi.org/10.1111/j.1472-765X.2011.03036.x
  38. Pérez-García, A., Romero, D. and de Vicente, A. 2011. Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture. Curr. Opin. Biotechnol. 22:187-193. https://doi.org/10.1016/j.copbio.2010.12.003
  39. Ruffner, B., Péchy-Tarr, M., Ryffel, F., Hoegger, P., Obrist, C., Rindlisbacher, A., Keel, C. and Maurhofer, M. 2013. Oral insecticidal activity of plant-associated pseudomonads. Environ. Microbiol. 15:751-763. https://doi.org/10.1111/j.1462-2920.2012.02884.x
  40. Sambrook, J. and Russell. D. 2001. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA.
  41. Schroth, M. N. and Hancock, J. G. 1982. Disease-suppressive soil and root-colonizing bacteria. Science 216:1376-1381. https://doi.org/10.1126/science.216.4553.1376
  42. Shanchez-Contreras, M. and Vlisidou, I. 2008. The diversity of insect-bacteria interactions and its applications for disease control. Biotechnol. Genet. Eng. Rev. 25:203-243. https://doi.org/10.5661/bger-25-203
  43. Siripornvisal, S. 2010. Biocontrol efficacy of Bacillus subtilis BCB3-19 against tomato gray mold. KMITL Sci. Tech. J. 10:37-44.
  44. Song, G. C., Lee, S., Hong, J., Choi, H. K., Hong, G. H., Bae, D. W., Mysore, K. S., Park, Y. S. and Ryu, C. M. 2015. Aboveground insect infestation attenuates belowground Agrobacterium-mediated genetic transformation. New Phytol. 207:148-158. https://doi.org/10.1111/nph.13324
  45. Sreerag, R. S., Jayaprakas, C. A., Ragesh, L. and Kumar, S. N. 2014. Endosymbiotic bacteria associated with the mealy bug, Rhizoecus amorphophallis (Hemiptera: Pseudococcidae). Int. Sch. Res. Not. 2014:268491.
  46. Tamura, K., Stecher, G., Peterson, D., Filipski, A. and 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, Y., Lu, Z. X., Bie, X. M. and Fengxia, L. 2010. Separation and extraction of antimicrobial lipopeptides produced by Bacillus amyloliquefaciens ES-2 with macroporous resin. Eur. Food Res. Technol. 231:189-196. https://doi.org/10.1007/s00217-010-1271-1
  48. Weisburg, W. G., Barns, S. M., Pelletier, D. A. and Lane, D. J. 1991. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173:697-703. https://doi.org/10.1128/jb.173.2.697-703.1991
  49. Yun, D. C., Yang, S. Y., Kim, Y. C. and Kim, I. S. 2013. Identification of surfactins as aphicidal metabolite produced by Bacillus amyloliquefaciens G1. J. Korean Soc. Appl. Biol. Chem. 56:751-753. https://doi.org/10.1007/s13765-013-3238-y

Cited by

  1. Synthesis and characterization of silver nanoparticles using Bacillus amyloliquefaciens and Bacillus subtilis to control filarial vector Culex pipiens pallens and its antimicrobial activity 2016, https://doi.org/10.1080/21691401.2016.1241793
  2. Enhanced Iron and Selenium Uptake in Plants by Volatile Emissions of Bacillus amyloliquefaciens (BF06) vol.7, pp.1, 2017, https://doi.org/10.3390/app7010085
  3. Construction of a recombinant strain of Pseudomonas fluorescens producing both phenazine-1-carboxylic acid and cyclic lipopeptide for the biocontrol of take-all disease of wheat 2017, https://doi.org/10.1007/s10658-017-1217-6
  4. Pumilacidin-Like Lipopeptides Derived from Marine Bacterium Bacillus sp. Strain 176 Suppress the Motility of Vibrio alginolyticus vol.83, pp.12, 2017, https://doi.org/10.1128/AEM.00450-17