Journal of Microbiology and Biotechnology

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

DOI QR Code

Antagonistic Efficacy of Symbiotic Bacterium Xenorhabdus sp. SCG against Meloidogyne spp.

  • Jong-Hoon Kim (Microbiome Convergence Research Center, Korea Research Institute of Bioscience and Biotechnology) ;
  • Byeong-Min Lee (Microbiome Convergence Research Center, Korea Research Institute of Bioscience and Biotechnology) ;
  • Hyung Chul Lee (ECOWIN Co., Ltd.) ;
  • In-Soo Choi (Nematode Research Center, Life and Industry Convergence Research Institute, Pusan National University) ;
  • Kyung-Bon Koo (ECOWIN Co., Ltd.) ;
  • Kwang-Hee Son (Microbiome Convergence Research Center, Korea Research Institute of Bioscience and Biotechnology)
  • Received : 2024.04.01
  • Accepted : 2024.07.01
  • Published : 2024.08.28
Download PDF
⟨ Previous Next ⟩

Abstract

The inhabitation and parasitism of root-knot nematodes (RKNs) can be difficult to control, as its symptoms can be easily confused with other plant diseases; hence, identifying and controlling the occurrence of RKNs in plants remains an ongoing challenge. Moreover, there are only a few biological agents for controlling these harmful nematodes. In this study, Xenorhabdus sp. SCG isolated from entomopathogenic nematodes of genus Steinernema was evaluated for nematicidal effects under in vitro and greenhouse conditions. The cell-free filtrates of strain SCG showed nematicidal activity against Meloidogyne species J2s, with mortalities of > 88% at a final concentration of 10%, as well as significant nematicidal activity against the three other genera of plant-parasitic nematodes in a dose-dependent manner. Thymine was isolated as active compounds by assay-guided fractionation and showed high nematicidal activity against M. incognita. Greenhouse experiments suggested that cell-free filtrates of strain SCG efficiently controlled the nematode population in M. incognita-infested tomatoes (Solanum lycopersicum L., cv. Rutgers). In addition, a significant increase in host plant growth was observed after 45 days of treatment. To our knowledge, this is the first to demonstrate the nematicidal activity spectrum of isolated Xenorhabdus species and their application to S. lycopersicum L., cv. Rutgers under greenhouse conditions. Xenorhabdus sp. SCG could be a promising biological nematicidal agent with plant growth-enhancing properties.

Keywords

Acknowledgement

This work was supported by Korea Institute of Planning and Evaluation for Technology in Food, Agriculture and Forestry (IPET) through "Crop Viruses and Pests Response Industry Technology Development" Program (No. 321110-4) funded by Ministry of Agriculture, Food and Rural Af-fairs (MAFRA).

References

  1. Li GH, Zhang KQ. 2023. Natural nematicidal metabolites and advances in their biocontrol capacity on plant parasitic nematodes. Nat. Prod. Rep. 40: 646-675. 
  2. Siddique S, Coomer A, Baum T, Williamson VM. 2022. Recognition and response in plant-nematode interactions. Annu. Rev. Phytopathol. 60: 143-162. 
  3. Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EGJ, Deleury E, et al. 2008. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat. Biotechnol. 26: 909-915. 
  4. Siddique S, Radakovic ZS, Hiltl C, Pellegrin C, Baum TJ, Beasley H, et al. 2022. The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5. Nat. Commun. 13: 6190. 
  5. Li J, Zou C, Xu J, Ji X, Niu X, Yang J, et al. 2015. Molecular mechanisms of nematode-nematophagous microbe interactions: basis for biological control of plant-parasitic nematodes. Annu. Rev. Phytopathol. 53: 67-95. 
  6. Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, Jones MGK, et al. 2013. Top 10 plant-parasitic nematodes in molecular plant pathology. Mol. Plant. Pathol. 14: 946-961. 
  7. Vos C, Schouteden N, van Tuinen D, Chatagnier O, Elsen A, De Waele D, et al. 2013. Mycorrhiza-induced resistance against the root-knot nematode Meloidogyne incognita involves priming of defense gene responses in tomato. Soil Biol. Biochem. 60: 45-54. 
  8. Subedi S, Thapa B, Shrestha J. 2020. Root-knot nematode (Meloidogyne incognita) and its management: a review. J. Agric. Nat. Resour. 3: 21-31. 
  9. Desaeger J, Wram C, Zasada I. 2020. New reduced-risk agricultural nematicides-rationale and review. J. Nematol. 52: 1-16. 
  10. Wang L, Qin Y, Fan Z, Gao K, Zhan J, Xing R, et al. 2022. Novel lead compound discovery from Aspergillus fumigatus 1T-2 against Meloidogyne incognita based on a chemical ecology study. J. Agric. Food Chem. 70: 4644-4657. 
  11. Migunova VD, Sasanelli N. 2021. Bacteria as biocontrol tool against phytoparasitic nematodes. Plants 10: 389. 
  12. Jang JY, Choi YH, Shin TS, Kim TH, Shin KS, Park HW, et al. 2016. Biological control of Meloidogyne incognita by Aspergillus niger F22 producing oxalic acid. PLos One 11: e0156230. 
  13. Khan A, Williams KL, Nevalainen HKM. 2004. Effects of Paecilomyces lilacinus protease and chitinase on the eggshell structures and hatching of Meloidogyne javanica juveniles. Biol. Control 31: 346-352. 
  14. Kiewnick S, Sikora RA. 2006. Biological control of the root-knot nematode Meloidogyne incognita by Paecilomyces lilacinus strain 251. Biol. Control 38: 179-187. 
  15. Pocurull M, Fullana AM, Ferro M, Valero P, Escudero N, Saus E, et al. 2020. Commercial formulates of Trichoderma induce systemic plant resistance to Meloidogyne incognita in tomato and the effect is additive to that of the Mi-1.2 resistance gene. Front. Microbiol. 10: 3042. 
  16. Zhao D, Zhao H, Zhao D, Zhu X, Wang Y, Duan Y, et al. 2018. Isolation and identification of bacteria from rhizosphere soil and their effect on plant growth promotion and root-knot nematode disease. Biol. Control 119: 12-19. 
  17. Antil S, Kumar R, Pathak DV, Kumar A, Panwar A, Kumari A, et al. 2022. Potential of Bacillus altitudinis KMS-6 as a biocontrol agent of Meloidogyne javanica. J. Pest Sci. 95: 1443-1452. 
  18. Siddiqui IA, Shaukat SS. 2003. Suppression of root-knot disease by Pseudomonas fluorescens CHA0 in tomato: importance of bacterial secondary metabolite, 2, 4-diacetylpholoroglucinol. Soil Biol. Biochem. 35: 1615-1623. 
  19. Maher AMD, Asaiyah M, Quinn S, Burke R, Wolff H, Bode HB, et al. 2021. Competition and co-existence of two Photorhabdus symbionts with a nematode host. Invertebr. Biol. 81: 223-239. 
  20. Abd-Elgawad MMM. 2021. Photorhabdus spp.: an overview of the beneficial aspects of Mutualistic bacteria of insecticidal nematodes. Plants 10: 1660. 
  21. Cimen H, Touray M, Gulsen SH, Hazir S. 2022. Natural products from Photorhabdus and Xenorhabdus: Mechanisms and impacts. Appl. Microbiol. Biotechnol. 106: 4387-4399. 
  22. El Aimani A, Houari A, Laasli SE, Mentag R, Iraqi D, Diria G, et al. 2022. Antagonistic potential of Moroccan entomopathogenic nematodes against root-knot nematodes, Meloidogyne javanica on tomato under greenhouse conditions. Sci. Rep. 12: 2915. 
  23. Abebew D, Sayedain FS, Bode E, Bode HB. 2022. Uncovering nematicidal natural products from Xenorhabdus bacteria. J. Agric. Food Chem. 70: 498-506. 
  24. Bi Y, Gao C, Yu Z. 2018. Rhabdopeptides from Xenorhabdus budapestensis SN84 and their nematicidal activities against Meloidogyne incognita. J. Agric. Food Chem. 66: 3833-3839. 
  25. Caccia M, Marro N, Duenas JR, Doucet ME, Lax P. 2018. Effect of the entomopathogenic nematode-bacterial symbiont complex on Meloidogyne hapla and Nacobbus aberrans in short-term greenhouse trials. Crop. Prot. 114: 162-166. 
  26. Bedding RA, Akhurst RJ. 1975. A simple technique for the detection of insect parasitic rhabditid nematodes in soil. Nematologica 21: 109-110. 
  27. Kulkarni N, Kushwaha DK, Mishra VK, Paunikar S. 2012. Effect of economical modification in artificial diet of greater wax moth Galleria mellonella (Lepidoptera: Pyralidae). Indian J. Entomol. 74: 369-374. 
  28. White GF. 1927. A method for obtaining infective nematode larvae from cultures. Science 66: 302-303. 
  29. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 218. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35: 1547. 
  30. Tailliez P, Pages S, Ginibre N, Boemare N. 2006. New insight into diversity in the genus Xenorhabdus, including the description of ten novel species. Int. J. Syst. Evol. Microbiol. 56: 2805-2818. 
  31. Saeki Y, Kawano E, Yamashita C, Akao S, Nagatomo Y. 2003. Detection of plant parasitic nematodes, Meloidogyne incognita and Pratylenchus coffeae by multiplex PCR using specific primers. Soil Sci. Plant Nutr. 49: 291-295. 
  32. Hussey RS, Barker KR. 1973. Comparison of methods of collecting inocula of Meloidogyne spp., including a new technique. Plant Disease Repo. 57: 1025-1028. 
  33. Abbott WS. 1925. A method of computing the effectiveness of an insecticide. J. Econ. Entomol. 18: 265-267. 
  34. Coolen WA. 1979. Methods for the extraction of Meloidogyne spp. and other nematodes from roots and soil, pp. 317-329. In Lamberti F, Taylor CE (eds.), Academic Press: London. 
  35. Mass Bank of North America. Availabe from https://mona.fiehnlab.ucdavis.edu/spectra/display/PS036101/. Accessed June 01, 2024. 
  36. Wishart DS, Knox C, Guo AC, Eisner R, Young N, Gautam, B, et al. 2009. HMDB: a knowledgebase for the human metabolome. Nucleic Acids Res. 2009 Jan; 37 (Database issue): D603-10. 
  37. Ayaz M, Ali Q, Farzand A, Khan AR, Ling H, Gao X. 2021. Nematicidal volatiles from Bacillus atrophaeus GBSC56 promote growth and stimulate induced systemic resistance in tomato against Meloidogyne incognita. Int. J. Mol. Sci. 22: 5049. 
  38. Tomar P, Thakur N, Yadav AN. 2022. Endosymbiotic microbes from entomopathogenic nematode (EPNs) and their applications as biocontrol agents for agro-environmental sustainability. Egypt. J. Biol. Pest Control 32: 80. 
  39. Wang Y, Gaugler R. 1998. Host and penetration site location by entomopathogenic nematodes against Japanese beetle larvae. J. Invertebr. Pathol. 72: 313-318. 
  40. Damascena AP, Ferreira JCA, Costa MGS, de Araujo Junior LM, Wilcken SRS. 2019. Hatching and mortality of Meloidogyne enterolobii under the interference of entomopathogenic nematodes in vitro. J. Nematol. 51: e2019-58. 
  41. Li J, Li Y, Wei X, Cui Y, Gu X, Li X, et al. 2023. Direct antagonistic effect of entomopathogenic nematodes and their symbiotic bacteria on root-knot nematodes migration toward tomato roots. Plant Soil 484: 441-455. 
  42. Challinor VL, Bode HB. 2015. Bioactive natural products from novel microbial sources. Ann. N. Y. Acad. 1354: 82-97. 
  43. Shi H, Zeng H, Yang X, Zhao J, Chen M, Qiu D. 2012. An insecticidal protein from Xenorhabdus ehlersii triggers prophenoloxidase activation and hemocyte decrease in Galleria mellonella. Curr. Microbiol. 64: 604-610. 
  44. Lewis EE, Grewal PS. 2005. Interactions with plant-parasitic nematodes, pp. 349-362. In Grewal PS, Ehlers RU, Shapiro-Ilan DI (eds.), CAB International: Oxon, UK. 
  45. Trinh THT, Wang SL, Nguyen VB, Phan TQ, Doan MD, Tran TPH, et al. 2022. Novel nematocidal compounds from shrimp shell wastes valorized by Bacillus velezensis RB.EK7 against black pepper nematodes. Agronomy 12: 2300. 
  46. Shapiro-Ilan DI, Nyczepir AP, Lewis EE. 2006. Entomopathogenic nematodes and bacteria applications for control of the pecan root-knot nematode, Meloidogyne partityla, in the greenhouse. J. Nematol. 38: 449-454.