Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Nematicidal and Plant Growth-Promoting Activity of Enterobacter asburiae HK169: Genome Analysis Provides Insight into Its Biological Activities

  • Oh, Mira (Center for Eco-friendly New Materials, Korea Research Institute of Chemical Technology) ;
  • Han, Jae Woo (Center for Eco-friendly New Materials, Korea Research Institute of Chemical Technology) ;
  • Lee, Chanhui (Department of Plant and Environmental New Resources, Kyung Hee University) ;
  • Choi, Gyung Ja (Center for Eco-friendly New Materials, Korea Research Institute of Chemical Technology) ;
  • Kim, Hun (Center for Eco-friendly New Materials, Korea Research Institute of Chemical Technology)
  • Received : 2018.01.18
  • Accepted : 2018.03.24
  • Published : 2018.06.28
Download PDF
⟨ Previous Next ⟩

Abstract

In the course of screening for microbes with nematicidal activity, we found that Enterobacter asburiae HK169 displayed promising nematicidal activity against the root-knot nematode Meloidogyne incognita, along with plant growth-promoting properties. Soil drenching of a culture of HK169 reduced gall formation by 66% while also increasing root and shoot weights by 251% and 160%, respectively, compared with an untreated control. The cell-free culture filtrate of the HK169 culture killed all juveniles of M. incognita within 48 h. In addition, the nematicidal activity of the culture filtrate was dramatically reduced by a protease inhibitor, suggesting that proteolytic enzymes contribute to the nematicidal activity of HK169. In order to obtain genomic information about the HK169 isolate related to its nematicidal and plant growth-promoting activities, we sequenced and analyzed the whole genome of the HK169 isolate, and the resulting information provided evidence that the HK169 isolate has nematicidal and plant growth-promoting activities. Taken together, these observations enable the future application of E. asburiae HK169 as a biocontrol agent for nematode control and promote our understanding of the beneficial interactions between E. asburiae HK169 and plants.

Keywords

References

  1. Sasser JN. 1977. Worldwide dissemination and importance of the root-knot nematodes, Meloidogyne spp. J. Nematol. 9: 26-29.
  2. Bird AF. 1974. Plant response to root-knot nematode. Annu. Rev. Phytopathol. 12: 69-85. https://doi.org/10.1146/annurev.py.12.090174.000441
  3. Brown CR, Mojtahedi H, Santo GS, Williamson VM. 1997. Effect of the Mi gene in tomato on reproductive factors of Meloidogyne chitwoodi and M. hapla. J. Nematol. 29: 416-419.
  4. Tom T, David R. 1986. In vitro testing for nonfumigant nematicide resistance in Meloidogyne incognita and Pratylenchus vulnus. Rev. Nematol. 9: 385-390.
  5. Vu TT, Kim H, Tran VK, Dang QL, Nguyen HT, Kim H, et al. 2016. In vitro antibacterial activity of selected medicinal plants traditionally used in Vietnam against human pathogenic bacteria. BMC Complement. Altern. Med. 16: 32-37.
  6. Kerry BR. 2000. Rhizosphere interactions and the exploitation of microbial agents for the biological control of plantparasitic nematodes. Annu. Rev Phytopathol. 38: 423-441. https://doi.org/10.1146/annurev.phyto.38.1.423
  7. Vessey JK. 2003. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255: 571-586. https://doi.org/10.1023/A:1026037216893
  8. Costa JM, Loper JE. 1994. Characterization of siderophore production by the biological control agent Enterobacter cloacae. Mol. Plant Microbe Interact. 7: 440-448. https://doi.org/10.1094/MPMI-7-0440
  9. Dahiya N, Tewari R, Tiwari RP, Hoondal GS. 2005. Production of an antifungal chitinase from Enterobacter sp. NRG4 and its application in protoplast production. World J. Microbiol. Biotechnol. 21: 1611-1616. https://doi.org/10.1007/s11274-005-8343-6
  10. Li J, Daniel H, Charles TC, Glick BR. 2000. An ACC deaminase minus mutant of Enterobacter cloacae UW4 no longer promotes root elongation. Curr. Microbiol. 41: 101-105. https://doi.org/10.1007/s002840010101
  11. Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, et al. 2003. Bacterial volatiles promote growth in Arabidopsis. Proc. Nat. Acad. Sci. USA 100: 4927-4932. https://doi.org/10.1073/pnas.0730845100
  12. Abbott SL. 2011. Klebsiella, Enterobacter, Citrobacter, Serratia, Plesiomonas, and other Enterobacteriaceae, pp. 639-657. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (eds.), Manual of Clinical Microbiology, 10th Ed. American Society of Microbiology, Washington, DC.
  13. Peng G, Zhang W, Luo H, Xie H, Lai W, Tan Z. 2009. Enterobacter oryzae sp. nov., a nitrogen-fixing bacterium isolated from the wild rice species Oryza latifolia. Int. J. Syst. Evol. Microbiol. 59: 1650-1655. https://doi.org/10.1099/ijs.0.005967-0
  14. Saleh SS, Glick BR. 2001. Involvement of gacS and rpoS in enhancement of the plant growth-promoting capabilities of Enterobacter cloacae CAL2 and UW4. Can. J. Microbiol. 47: 698-705. https://doi.org/10.1139/w01-072
  15. Shoebitz M, Ribaudo CM, Pardo MA, Cantore ML, Ciampi L, Cura JA. 2009. Plant growth promoting properties of a strain of Enterobacter ludwigii isolated from Lolium perenne rhizosphere. Soil Biol. Biochem. 41: 1768-1774. https://doi.org/10.1016/j.soilbio.2007.12.031
  16. Siddiqui ZA, Futai K. 2009. Biocontrol of Meloidogyne incognita on tomato using antagonistic fungi, plant-growth-promoting rhizobacteria and cattle manure. Pest Manag. Sci. 65: 943-948. https://doi.org/10.1002/ps.1777
  17. Hwang SM, Park MS, K im JC, J ang KS, Choi YH, Choi GJ. 2014. Occurrence of Meloidogyne incognita infecting resistant cultivars and development of an efficient screening method for resistant tomato to the Mi-virulent nematode. Korean J. Hort. Sci. Technol. 32: 217-226. https://doi.org/10.7235/hort.2014.13129
  18. Hooper DJ. 1986. Culturing nematodes and related experimental techniques, pp. 133-157. In Southey JF (ed.), Laboratory Methods for Work with Plant and Soil Nematodes. H. M. Stationery Office, London, UK.
  19. Abbott WS. 1925. A method of computing the effectiveness of an insecticide. J. Econ. Entomol. 18: 265-267.
  20. Jang JY, Choi YH, Shin TS, Kim TH, Shin K-S, Park HW, et al. 2016. Biological control of Meloidogyne incognita by Aspergillus niger F22 producing oxalic acid. PLoS One 11: e0156230. https://doi.org/10.1371/journal.pone.0156230
  21. Tamura K, Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10: 512-526.
  22. Castaneda-Alvarez C, Prodan S, Rosales IM, Aballay E. 2016. Exoenzymes and metabolites related to the nematicidal effect of rhizobacteria on Xiphinema index Thorne & Allen. J. Appl. Microbiol. 120: 413-424. https://doi.org/10.1111/jam.12987
  23. Paiva G, Proenca DN, Francisco R, Verissimo P, Santos SS, Fonseca L, et al. 2013. Nematicidal bacteria associated to pinewood nematode produce extracellular proteases. PLoS One 8: e79705. https://doi.org/10.1371/journal.pone.0079705
  24. Huang X, Tian B, Niu Q, Yang J, Zhang L, Zhang K. 2005. An extracellular protease from Brevibacillus laterosporus G4 without parasporal crystals can serve as a pathogenic factor in infection of nematodes. Res. Microbiol. 156: 719-727. https://doi.org/10.1016/j.resmic.2005.02.006
  25. Luo X, Chen L, Huang Q, Zheng J, Zhou W, Peng D, et al. 2013. Bacillus thuringiensis metalloproteinase Bmp1 functions as a nematicidal virulence factor. Appl. Environ. Microbiol. 79: 460-468. https://doi.org/10.1128/AEM.02551-12
  26. Haq SK, Atif SM, Khan RH. 2004. Protein proteinase inhibitor genes in combat against insects, pests, and pathogens: natural and engineered phytoprotection. Arch. Biochem. Biophys. 431: 145-159. https://doi.org/10.1016/j.abb.2004.07.022
  27. Duponnois R, Amadou M, Mateille T. 1999. Beneficial effects of Enterobacter cloacae and Pseudomonas mendocina for biocontrol of Meloidogyne incognita with the endosporeforming bacterium Pasteuria penetrans. Nematology 1: 95-101. https://doi.org/10.1163/156854199507901
  28. Kim KY, Jordan D, McDonald GA. 1997. Effect of phosphatesolubilizing bacteria and vesicular-arbuscular mycorrhizae on tomato growth and soil microbial activity. Biol. Fertil. Soils 26: 79-87. https://doi.org/10.1007/s003740050347
  29. Sikora RA, Hoffmann-Hergarten S. 1993. Biological control of plant parasitic nematodes with plant-health-promoting rhizobacteria, pp. 166-172. In Lumsden RD, Vaughn JL (eds.), Pest Management: Biotechnology Based Technologies. American Chemical Society, Washington, DC.
  30. Niu Q, Huang X, Zhang L, Xu J, Yang D, Wei K, et al. 2010. A Trojan horse mechanism of bacterial pathogenesis against nematodes. Proc. Nat. Acad. Sci. USA 107: 16631-16636. https://doi.org/10.1073/pnas.1007276107
  31. Siddiqui IA, Haas D, Heeb S. 2005. Extracellular protease of Pseudomonas fluorescens CHA0, a biocontrol factor with activity against the root-knot nematode Meloidogyne incognita. Appl. Environ. Microbiol. 71: 5646-5649 https://doi.org/10.1128/AEM.71.9.5646-5649.2005
  32. Peng D, Lin J, Huang Q, Zheng W, Liu G, Zheng J, et al. 2016. A novel metalloproteinase virulence factor is involved in Bacillus thuringiensis pathogenesis in nematodes and insects. Environ. Microbiol. 18: 846-862. https://doi.org/10.1111/1462-2920.13069
  33. Oostendorp M, Sikora RA. 1989. Seed treatment with antagonistic rhizobacteria for the suppression of Heterodera schachtii early root infection of sugar beet. Rev. Nematol. 12: 77-83.
  34. Schoner TA, Gassel S, Osawa A, Tobias NJ, Okuno Y, Sakakibara Y, et al. 2016. Aryl polyenes, a highly abundant class of bacterial natural products, are functionally related to antioxidative carotenoids. Chembiochem 17: 247-253 https://doi.org/10.1002/cbic.201500474
  35. Cimermancic P, Medema MH, Claesen J, Kurita K, Brown LCW, Mavrommatis K, et al. 2014. Insights into secondary metabolism from a global analysis of prokaryotic biosynthetic gene clusters. Cell 158: 412-421. https://doi.org/10.1016/j.cell.2014.06.034
  36. Schaefer AL, Val DL, Hanzelka BL, Cronan JE, Greenberg EP. 1996. Generation of cell-to-cell signals in quorum sensing: acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein. Proc. Nat. Acad. Sci. USA 93: 9505-9509. https://doi.org/10.1073/pnas.93.18.9505
  37. Wei HL, Zhang LQ. 2006. Quorum-sensing system influences root colonization and biological control ability in Pseudomonas fluorescens 2P24. Antonie Van Leeuwenhoek 89: 267-280. https://doi.org/10.1007/s10482-005-9028-8

Cited by

  1. Draft Genome Analysis Offers Insights Into the Mechanism by Which Streptomyces chartreusis WZS021 Increases Drought Tolerance in Sugarcane vol.9, pp.None, 2018, https://doi.org/10.3389/fmicb.2018.03262
  2. Genetic and functional characterization of the bacterial community on fruit of three raspberry (Rubus idaeus) cultivars vol.9, pp.2, 2018, https://doi.org/10.3233/jbr-180340
  3. Impact of Plant Growth Promoting Rhizobacteria in the Orchestration of Lycopersicon esculentum Mill. Resistance to Plant Parasitic Nematodes: A Metabolomic Approach to Evaluate Defense Responses Under vol.9, pp.11, 2018, https://doi.org/10.3390/biom9110676
  4. Seasonal dynamics in the number and composition of coliform bacteria in drinking water reservoirs vol.787, pp.None, 2018, https://doi.org/10.1016/j.scitotenv.2021.147539