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Biological Control of Root-Knot Nematodes by Organic Acid-Producing Lactobacillus brevis WiKim0069 Isolated from Kimchi

  • Seo, Hye Jeong (Department of Agricultural Chemistry, Institute of Environmentally Friendly Agriculture, College of Agriculture and Life Science, Chonnam National University) ;
  • Park, Ae Ran (Department of Agricultural Chemistry, Institute of Environmentally Friendly Agriculture, College of Agriculture and Life Science, Chonnam National University) ;
  • Kim, Seulbi (Department of Agricultural Chemistry, Institute of Environmentally Friendly Agriculture, College of Agriculture and Life Science, Chonnam National University) ;
  • Yeon, Jehyeong (Department of Agricultural Chemistry, Institute of Environmentally Friendly Agriculture, College of Agriculture and Life Science, Chonnam National University) ;
  • Yu, Nan Hee (Department of Agricultural Chemistry, Institute of Environmentally Friendly Agriculture, College of Agriculture and Life Science, Chonnam National University) ;
  • Ha, Sanghyun (R&D Division, World Institute of Kimchi) ;
  • Chang, Ji Yoon (R&D Division, World Institute of Kimchi) ;
  • Park, Hae Woong (R&D Division, World Institute of Kimchi) ;
  • Kim, Jin-Cheol (Department of Agricultural Chemistry, Institute of Environmentally Friendly Agriculture, College of Agriculture and Life Science, Chonnam National University)
  • 투고 : 2019.08.27
  • 심사 : 2019.10.31
  • 발행 : 2019.12.01

초록

Root-knot nematodes (RKNs) are among the most destructive plant-parasites worldwide, and RKN control has been attempted mainly using chemical nematicides. However, these chemical nematicides have negative effects on humans and the environment, thus necessitating the search for eco-friendly alternative RKN control methods. Here, we screened nematicidal lactic acid bacteria (LAB) isolated from kimchi and evaluated their efficacy as biocontrol agents against RKNs. Of 237 bacterial strains, Lactobacillus brevis WiKim0069 showed the strongest nematicidal activity against the second-stage juveniles (J2) of Meloidogyne incognita, M. arenaria, and M. hapla and inhibited the egg hatch of M. incognita. The culture filtrate of WiKim0069 had a pH of 4.2 and contained acetic acid (11,190 ㎍/ml), lactic acid (7,790 ㎍/ml), malic acid (470 ㎍/ml), and succinic acid (660 ㎍/ml). An artificial mixture of the four organic acids produced by WiKim0069 also induced 98% M. incognita J2 mortality at a concentration of 1.25%, indicating that its nematicidal activity was derived mainly from the four organic acids. Application of WiKim0069 culture filtrate suppressed the formation of galls and egg masses on tomato roots by M. incognita in a dose-dependent manner in a pot experiment. The fermentation broth of WiKim0069 also reduced gall formation on melon under field conditions, with a higher efficacy (62.8%) than that of fosthiazate (32.8%). This study is the first report to identify the effectiveness of kimchi LAB against RKNs and to demonstrate that the organic acids produced by LAB can be used for the RKN management.

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참고문헌

  1. Abbott, W. S. 1925. A method of computing the effectiveness of and insecticide. J. Econ. Entomol. 18:265-267. https://doi.org/10.1093/jee/18.2.265a
  2. Abdel-Aziz, S. M., Moustafa, Y. A. and Hamed, H. A. 2014. Lactic acid bacteria in the green biocontrol against some phytopathogenic fungi: treatment of tomato seeds. J. Basic Appl. Sci. Res. 4:1-9.
  3. Akhtar, M. and Malik, A. 2000. Roles of organic soil amendments and soil organisms in the biological control of plantparasitic nematodes: a review. Bioresour. Technol. 74:35-47. https://doi.org/10.1016/S0960-8524(99)00154-6
  4. Aktar, M. W., Sengupta, D. and Chowdhury, A. 2009. Impact of pesticides use in agriculture: their benefits and hazards. Interdiscip. Toxicol. 2:1-12. https://doi.org/10.2478/v10102-009-0001-7
  5. Ashoub, A. H. and Amara, M. T. 2010. Biocontrol activity of some bacterial genera against root-knot nematode, Meloidogyne incognita. J. Am. Sci. 6:321-328.
  6. Bansal, R. K. and Bajaj, A. 2003. Effect of volatile fatty acids on embryogenesis and hatching of Meloidogyne incognita eggs. Nematol. Mediterr. 31:135-140.
  7. Barefoot, S. F. and Klaenhammer, T. R. 1983. Detection and activity of lactacin B, a bacteriocin produced by Lactobacillus acidophilus. Appl. Environ. Microbiol. 45:1808-1815. https://doi.org/10.1128/aem.45.6.1808-1815.1983
  8. Barker, K. R. 1985. Nematode extractions and bioassays. In: An advanced treatise on Meloidogyne, Vol. II. Methodology, eds. by K. R. Barker, C. C. Carter, J. N. Sasser, pp. 19-35. North Carolina State University Graphics, Raleigh, NC, USA.
  9. Blok, V. C., Jones, J. T., Phillips, M. S. and Trudgill, D. L. 2008. Parasitism genes and host range disparities in biotrophic nematodes: the conundrum of polyphagy versus specialisation. BioEssays 30:249-259. https://doi.org/10.1002/bies.20717
  10. Cayrol, J.-C., Djian, C. and Pijarowski, L. 1989. Study of the nematocidal properties of the culture filtrate of the nematophagous fungus Paecilomyces lilacinus. Rev. Nematol. 12:331-336.
  11. Choi, A.-R., Patra, J. K., Kim, W. J. and Kang, S.-S. 2018. Antagonistic activities and probiotic potential of lactic acid bacteria derived from a plant-based fermented food. Front. Microbiol. 9:1963. https://doi.org/10.3389/fmicb.2018.01963
  12. da Cunha, M. V. and Foster, M. A. 1992. Sugar-glycerol cofermentations in lactobacilli: the fate of lactate. J. Bacteriol. 174:1013-1019. https://doi.org/10.1128/jb.174.3.1013-1019.1992
  13. Driehuis, F., Elferink, S. J. and Spoelstra, S. F. 1999. Anaerobic lactic acid degradation during ensilage of whole crop maize inoculated with Lactobacillus buchneri inhibits yeast growth and improves aerobic stability. J. Appl. Microbiol. 87:583-594. https://doi.org/10.1046/j.1365-2672.1999.00856.x
  14. El-Mabrok, A. S. W., Hassan, Z., Mokhtar, A. M., Hussain, K. M. A. and Kahar, F. K. S. B. A. 2012. Screening of lactic acid bacteria as biocontrol against (Collectotrichum capsici) on chilli Bangi. Res. J. Appl. Sci. 7:446-473.
  15. Elling, A. A. 2013. Major emerging problems with minor Meloidogyne species. Phytopathology 103:1092-1102. https://doi.org/10.1094/PHYTO-01-13-0019-RVW
  16. Favre-Bonvin, J., Ponchet, M., Djian, C., Arpin, N. and Pijarowski, L. 1991. Acetic acid: a selective nematicidal metabolite from culture filtrates of Paecilomyces lilacinus (Thom) Samson and Trichoderma longibrachiatum Rifai. Nematologica 37:101-112. https://doi.org/10.1163/187529291X00105
  17. Ghazvini, R. D., Kouhsari, E., Zibafar, E., Hashemi, S. J., Amini, A. and Niknejad, F. 2016. Antifungal activity and aflatoxin degradation of Bifidobacterium bifidum and Lactobacillus fermentum against toxigenic Aspergillus parasiticus. Open Microbiol. J. 10:197-201. https://doi.org/10.2174/1874285801610010197
  18. Gilliland, S. E. 1990. Health and nutritional benefits from lactic acid bacteria. FEMS Microbiol. Rev. 7:175-188. https://doi.org/10.1111/j.1574-6968.1990.tb04887.x
  19. Guarner, F., Khan, A. G., Garisch, J., Eliakim, R., Gangl, A., Thomson, A., Krabshuis, J., Lemair, T., Kaufmann, P., de Paula, J. A., Fedorak, R., Shanahan, F., Sanders, M. E., Szajewska, H., Ramakrishna, B. S., Karakan, T., Kim, N. and World Gastroenterology Organization. 2012. World Gastroenterology Organisation global guidelines: probiotics and prebiotics October 2011. J. Clin. Gastroenterol. 46:468-481. https://doi.org/10.1097/MCG.0b013e3182549092
  20. Hamed, H. A., Moustafa, Y. A. and Abdel-Aziz, S. M. 2011. In vivo efficacy of lactic acid bacteria in biological control against Fusarium oxysporum for protection of tomato plant. Life Sci. J. 8:462-468.
  21. Holbrook, C. C., Knauft, D. A. and Dickson, D. W. 1983. A technique for screening peanut for resistance to Meloidogyne arenaria. Plant Dis. 67:957-958. https://doi.org/10.1094/PD-67-957
  22. Hwang, S. M., Park, M. S., Kim, J.-C., Jang, K. S., Choi, Y. H. and Choi, G. J. 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. Hortic. Sci. Technol. 32:217-226. https://doi.org/10.7235/hort.2014.13129
  23. Jang, J. Y., Choi, Y. H., Shin, T. S., Kim, T. H., Shin, K.-S., Park, H. W., Kim, Y. H., Kim, H., Choi, G. J., Jang, K. S., Cha, B., Kim, I. S., Myung, E. J. and Kim, J.-C. 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
  24. Jang, S.-E., Hyun, Y.-J., Oh, Y.-J., Choi, K. B., Kim, T., Yeo, I. H., Han, M. J. and Kim, D.-H. 2011. Adhesion activity of Lactobacillus plantarum PM 008 isolated from kimchi on the intestine of mice. J. Bacteriol. Virol. 41:83-90. https://doi.org/10.4167/jbv.2011.41.2.83
  25. Jenkins, W. R. 1964. A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Dis. Rep. 48:692.
  26. Jones, J. T., Haegeman, A., Danchin, E. G. J., Gaur, H. S., Helder, J., Jones, M. G. K., Kikuchi, T., Manzanilla-Lopez, R., Palomares-Rius, J. E., Wesemael, W. M. L. and Perry, R. N. 2013. Top 10 plant-parasitic nematodes in molecular plant pathology. Mol. Plant Pathol. 14:946-961. https://doi.org/10.1111/mpp.12057
  27. Jung, J. Y., Lee, S. H., Kim, J. M., Park, M. S., Bae, J.-W., Hahn, Y., Madsen, E. L. and Jeon, C. O. 2011. Metagenomic analysis of kimchi, a traditional Korean fermented food. Appl. Environ. Microbiol. 77:2264-2274. https://doi.org/10.1128/AEM.02157-10
  28. Kandler, O., Schillinger, U. and Weiss, N. 1983. Lactobacillus bifermentans sp. nov., nom. rev., an organism forming $CO_2$ and $H_2$ from lactic acid. Syst. Appl. Microbiol. 4:408-412. https://doi.org/10.1016/s0723-2020(83)80025-3
  29. Khanafari, A., Soudi, H. and Miraboulfathi, M. 2007. Biocontrol of Aspergillus flavus and aflatoxin B1 production in corn. Iran. J. Environ. Health Sci. Eng. 4:163-168.
  30. Kim, D.-G., Lee, Y.-K. and Park, B.-Y. 2001. Root-knot nematode species distributing in greenhouses and their simple identification scheme. Res. Plant Dis. 7:49-55 (in Korean).
  31. Kim, T. Y., Jang, J. Y., Jeon, S. J., Lee, H. W., Bae, C.-H., Yeo, J. H., Lee, H. B., Kim, I. S., Park, H. W. and Kim, J.-C. 2016. Nematicidal activity of kojic acid produced by Aspergillus oryzae against Meloidogyne incognita. J. Microbiol. Biotechnol 26:1383-1391. https://doi.org/10.4014/jmb.1603.03040
  32. Konappa, N. M., Maria, M., Uzma, F., Krishnamurthy, S., Nayaka, S. C., Niranjana, S. R. and Chowdappa, S. 2016. Lactic acid bacteria mediated induction of defense enzymes to enhance the resistance in tomato against Ralstonia solanacearum causing bacterial wilt. Sci. Hortic. 207:183-192. https://doi.org/10.1016/j.scienta.2016.05.029
  33. Kormin, S., Rusul, G., Radu, S. and Ling, F. H. 2001. Bacteriocin-producing lactic acid bacteria isolated from traditional fermented food. Malays. J. Med. Sci. 8:63-68.
  34. Lee, Y. S., Naning, K. W., Nguyen, X. H., Kim, S. B., Moon, J. H. and Kim, K. Y. 2014. Ovicidal activity of lactic acid produced by Lysobacter capsici YS1215 on eggs of root-knot nematode, Meloidogyne incognita. J. Microbiol. Biotechnol. 24:1510-1515. https://doi.org/10.4014/jmb.1405.05014
  35. Lim, J.-H., Yoon, S.-M., Tan, P.-L., Yang, S., Kim, S.-H. and Park, H.-J. 2018. Probiotic properties of Lactobacillus Plantarum LRCC5193, a plant-origin lactic acid bacterium isolated from kimchi and its use in chocolates. J. Food Sci. 83:2802-2811. https://doi.org/10.1111/1750-3841.14364
  36. Limanska, N., Korotaeva, N., Biscola, V., Ivanytsia, T., Merlich, A., Franco, B. D. G. M. and Haertle, T. 2015. Study of the potential application of lactic acid bacteria in the control of infection caused by Agrobacterium tumefaciens. J. Plant Pathol. Microbiol. 6:292.
  37. Lindgren, S. E., Axelsson, L. T. and McFeeters, R. F. 1990. Anaerobic L-lactate degradation by Lactobacillus plantarum. FEMS Microbiol. Lett. 66:209-213.
  38. Lindgren, S. E. and Dobrogosz, W. J. 1990. Antagonistic activities of lactic acid bacteria in food and feed fermentations. FEMS Microbiol. Rev. 7:149-163. https://doi.org/10.1111/j.1574-6968.1990.tb04885.x
  39. McBride, R. G., Mikkelsen, R. L. and Barker, K. R. 2000. The role of low molecular weight organic acids from decomposing rye in inhibiting root-knot nematode populations in soil. Appl. Soil Ecol. 15:243-251. https://doi.org/10.1016/S0929-1393(00)00062-7
  40. Meyer, S. L. F., Massoud, S. I., Chitwood, D. J. and Roberts, D. P. 2000. Evaluation of Trichoderma virens and Burkholderia cepacia for antagonistic activity against root-knot nematode, Meloidogyne incognita. Nematology 2:871-879. https://doi.org/10.1163/156854100750112815
  41. Moens, M., Perry, R. N. and Starr, J. L. 2009. Meloidogyne species: a diverse group of novel and important plant parasites. In: Root-knot nematodes, eds. by R. N. Perry, J. L. Starr and M. Moens, pp. 1-17. CAB International, London, UK.
  42. Molinari, S. 2009. Antioxidant enzymes in (a)virulent populations of root-knot nematodes. Nematology 11:689-697. https://doi.org/10.1163/156854108X399317
  43. Molinari, S., Fanelli, E. and Leonetti, P. 2014. Expression of tomato salicylic acid (SA)-responsive pathogenesis-related genes in Mi-1-mediated and SA-induced resistance to rootknot nematodes. Mol. Plant Pathol. 15:255-264. https://doi.org/10.1111/mpp.12085
  44. Naseby, D. C., Pascual, J. A. and Lynch, J. M. 2000. Effect of biocontrol strains of Trichoderma on plant growth, Pythium ultimum populations, soil microbial communities and soil enzyme activities. J. Appl. Microbiol. 88:161-169. https://doi.org/10.1046/j.1365-2672.2000.00939.x
  45. Ntalli, N., Ratajczak, M., Oplos, C., Menkissoglu-Spiroudi, U. and Adamski, Z. 2016. Acetic acid, 2-undecanone, and (e)-2-decenal ultrastructural malformations on Meloidogyne incognita. J. Nematol. 48:248-260. https://doi.org/10.21307/jofnem-2017-033
  46. Park, J., Seo, Y. and Kim, Y. H. 2014. Biological control of Meloidogyne hapla using an antagonistic bacterium. Plant Pathol. J. 30:288-298. https://doi.org/10.5423/PPJ.OA.02.2014.0013
  47. Prusky, D., Kobiler, I., Akerman, M. and Miyara, I. 2006. Effect of acidic solutions and acidic prochloraz on the control of postharvest decay caused by Alternaria alternata in mango and persimmon fruit. Postharvest Biol. Technol. 42:134-141. https://doi.org/10.1016/j.postharvbio.2006.06.001
  48. Ralmi, N. H. A. A., Khandaker, M. M. and Mat, N. 2016. Occurrence and control of root knot nematode in crops: a review. Aust. J. Crop Sci. 10:1649-1654. https://doi.org/10.21475/ajcs.2016.10.12.p7444
  49. Schneider, P. and Orelli, O. 1947. Entomologisches praktikum [Entomological internship]. Verlag. H. R. Sauerlander Co., Aarau, Switzerland. 237 pp.
  50. Seo, Y. and Kim, Y. H. 2014. Control of Meloidogyne incognita using mixtures of organic acids. Plant Pathol. J. 30:450-455. https://doi.org/10.5423/PPJ.NT.07.2014.0062
  51. Shrestha, A., Kim, B. S. and Park, D. H. 2014. Biological control of bacterial spot disease and plant growth-promoting effects of lactic acid bacteria on pepper. Biocontrol Sci. Technol. 24:763-779. https://doi.org/10.1080/09583157.2014.894495
  52. Sitton, J. W. and Patterson, M. E. 1992. Effect of high-carbon dioxide and low-oxygen controlled atmospheres on postharvest decays of apples. Plant Dis. 76:992-995. https://doi.org/10.1094/PD-76-0992
  53. Stiles, M. E. and Holzapfel, W. H. 1997. Lactic acid bacteria of foods and their current taxonomy. Int. J. Food Microbiol. 36:1-29. https://doi.org/10.1016/S0168-1605(96)01233-0
  54. 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
  55. Terefe, M., Tefera, T. and Sakhuja, P. K. 2009. Effect of a formulation of Bacillus firmus on root-knot nematode Meloidogyne incognita infestation and the growth of tomato plants in the greenhouse and nursery. J. Invertebr. Pathol. 100:94-99. https://doi.org/10.1016/j.jip.2008.11.004
  56. Trias, R., Baneras, L., Montesinos, E. and Badosa, E. 2008. Lactic acid bacteria from fresh fruit and vegetables as biocontrol agents of phytopathogenic bacteria and fungi. Int. Microbiol. 11:231-236.
  57. Trudgill, D. L. and Blok, V. C. 2001. Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Annu. Rev. Phytopathol 39:53-77. https://doi.org/10.1146/annurev.phyto.39.1.53
  58. Viglierchio, D. R. and Schmitt, R. V. 1983. On the methodology of nematode extraction from field samples: Baermann funnel modifications. J. Nematol. 15:438-444.
  59. Visser, R. and Holzapfel, W. H. 1992. Lactic acid bacteria in the control of plant pathogens. In: The Lactic Acid Bacteria. Vol. 1, ed. by B. J. B. Wood, pp. 193-210. Springer, Boston, MA, USA.
  60. Wodzki, R. and Nowaczyk, J. 2001. Membrane transport of organics. III. Permeation of some carboxylic acids through bipolar polymer membrane. J. Appl. Polym. Sci. 80:2705-2717. https://doi.org/10.1002/app.1385
  61. Yadav, U. 2017. Recent trends in nematode management practices: the Indian context. Int. Res. J. Eng. Technol. 4:482-489.
  62. Yeon, J., Park, A. R., Kim, Y. J., Seo, H. J., Yu, N. H., Ha, S., Park, H. W. and Kim, J.-C. 2019. Control of root-knot nematodes by a mixture of maleic acid and copper sulfate. Appl. Soil Ecol. 141:61-68. https://doi.org/10.1016/j.apsoil.2019.05.010
  63. Zuckerman, B. M., Matheny, M. and Acosta, N. 1994. Control of plant-parasitic nematodes by a nematicidal strain of Aspergillus niger. J. Chem. Ecol. 20:33-43. https://doi.org/10.1007/BF02065989