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A Synergistic Effect of Chitosan and Lactic Acid Bacteria on the Control of Cruciferous Vegetable Diseases

  • Received : 2020.01.01
  • Accepted : 2020.03.09
  • Published : 2020.04.01

Abstract

Two lactic acid bacteria (LAB) designated J02 and J13 were recovered from fermented vegetables based on their ability to suppress soft rot disease caused by Pectobacterium carotovorum subsp. carotovorum (Pcc) on radish. J02 and J13 were identified as Lactobacillus pentosus and Leuconostoc fallax, respectively. The ability of J02 and J13 to suppress plant diseases is highly dependent on chitosan. LAB alone has no effect and chitosan alone has only a moderate effect on disease reduction. However, J02 or J13 broth cultures plus chitosan display a strong inhibitory effect against plant pathogens and significantly reduces disease severity. LAB strains after being cultured in fish surimi (agricultural waste) and glycerol or sucrose-containing medium and mixed with chitosan, reduce three cruciferous vegetable diseases, including cabbage black spot caused by Alternaria brassicicola, black rot caused by Xanthomonas campestris pv. campestris, and soft rot caused by Pcc. Experimental trials reveal that multiple applications are more effective than a single application. In-vitro assays also reveal the J02/chitosan mixture is antagonistic against Colletotrichum higginsianum, Sclerotium rolfsii, and Fusarium oxysporum f. sp. rapae, indicating a broad-spectrum activity of LAB/chitosan. Overall, our results indicate that a synergistic combination of LAB and chitosan offers a promising approach to biocontrol.

Keywords

References

  1. Abd-El-Kareem, F., El-Mougy, N. S., El-Gamal, N. G. and Fotouh, Y. O. 2006. Use of chitin and chitosan against tomato root rot disease under greenhouse conditions. Res. J. Agric. Biol. Sci. 2:147-152.
  2. Alakomi, H.-L., Skytta, E., Saarela, M., Mattila-Sandholm, T., Latva-Kala, K. and Helander, I. M. 2000. Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane. Appl. Environ. Microbiol. 66:2001-2005. https://doi.org/10.1128/AEM.66.5.2001-2005.2000
  3. Arena, M. P., Silvain, A., Normanno, G., Grieco, F., Drider, D., Spano, G. and Fiocco, D. 2016. Use of Lactobacillus plantarum strains as a bio-control strategy against food-borne pathogenic microorganisms. Front. Microbiol. 7:464.
  4. Axel, C., Brosnan, B., Zannini, E., Furey, A., Coffey, A. and Arendt, E. K. 2016. Antifungal sourdough lactic acid bacteria as biopreservation tool in quinoa and rice bread. Int. J. Food Microbiol. 239:86-94. https://doi.org/10.1016/j.ijfoodmicro.2016.05.006
  5. Begin, A. and Van Calsteren, M. R. 1999. Antimicrobial films produced by chitosan. Int. J. Macromol. 26:63-67. https://doi.org/10.1016/S0141-8130(99)00064-1
  6. Cabo, M. L., Braber, A. F. and Koenraad, P. M. F. J. 2002. Apparent antifungal activity of several lactic acid bacteria against Penicillium discolor is due to acetic acid in the medium. J. Food Prot. 65:1309-1316. https://doi.org/10.4315/0362-028X-65.8.1309
  7. Castellano, P., Perez Ibarreche, M., Blanco Massani, M., Fontana, C. and Vignolo, G. M. 2017. Strategies for pathogen biocontrol using lactic acid bacteria and their metabolites: a focus on meat ecosystems and industrial environments. Microorganisms 5:E38. https://doi.org/10.3390/microorganisms5030038
  8. Chirkov, S. N. 2002. The antiviral activity of chitosan (review). Appl. Biochem. Microbiol. 38:1-8. https://doi.org/10.1023/A:1013206517442
  9. Colombo, M., Castilho, N. P. A., Todorov, S. D. and Nero, L. A. 2018. Beneficial properties of lactic acid bacteria naturally present in dairy production. BMC Microbiol. 18:219. https://doi.org/10.1186/s12866-018-1356-8
  10. Conn, K. L., Tewari, J. P. and Awasthi, R. P. 1990. A disease assessment key for Alternaria blackspot in rapeseed and mustard. Can. Plant Dis. Surv. 70:19-22.
  11. Crowley, S., Mahony, J. and van Sinderen, D. 2013. Current perspectives on antifungal lactic acid bacteria as natural biopreservatives. Trends Food Sci. Technol. 33:93-109. https://doi.org/10.1016/j.tifs.2013.07.004
  12. Daranas, N., Rosello, G., Cabrefiga, J., Donati, I., Frances, J., Badosa, E., Spinelli, F., Montesinos, E. and Bonaterra, A. 2019. Biological control of bacterial plant diseases with Lactobacillus plantarum strains selected for their broad-spectrum activity. Ann. Appl. Biol. 174:92-105. https://doi.org/10.1111/aab.12476
  13. De Man, J. C., Rogosa, M. and Sharpe, M. E. 1960. A medium for the cultivation of Lactobacilli. J. Appl. Bacteriol. 23:130-135. https://doi.org/10.1111/j.1365-2672.1960.tb00188.x
  14. El Hadrami, A., Adam, L. R., El Hadrami, I. and Daayf, F. 2010. Chitosan in plant protection. Mar. Drugs 8:968-987. https://doi.org/10.3390/md8040968
  15. Gajbhiye, M. H. and Kapadnis, B. P. 2016. Antifungal-activityproducing lactic acid bacteria as biocontrol agents in plants. Biocontrol Sci. Technol. 26:1451-1470. https://doi.org/10.1080/09583157.2016.1213793
  16. Hadwiger, L. A. 2013. Multiple effects of chitosan on plant systems:solid science or hype. Plant Sci. 208:42-49. https://doi.org/10.1016/j.plantsci.2013.03.007
  17. Hassan, N., Nakasuji, S., Elsharkawy, M. M., Naznin, H. A., Kubota, M., Ketta, H. and Shimizu, M. 2017. Biocontrol potential of an endophytic Streptomyces sp. strain MBCN152-1 against Alternaria brassicicola on cabbage plug seedlings. Microbes Environ. 32:133-141. https://doi.org/10.1264/jsme2.ME17014
  18. Hassan, O. and Chang, T. 2017. Chitosan for eco-friendly control of plant disease. Asian J. Plant Pathol. 11:53-70. https://doi.org/10.3923/ajppaj.2017.53.70
  19. Huang, J.-S., Peng, Y. H., Chung, K.-R. and Huang, J.-W. 2018. Suppressive efficacy of volatile organic compounds produced by Bacillus mycoides on damping-off pathogens of cabbage seedlings. J. Agric. Sci. 156:795-809. https://doi.org/10.1017/S0021859618000746
  20. Konappa, N. M., Malini, 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
  21. Laitila, A., Alakomi, H.-L., Raaska, L., Mattila-Sandholm, T. and Haikara, A. 2002. Antifungal activities of two Lactobacillus plantarum strains against Fusarium moulds in vitro and in malting of barley. J. Appl. Microbiol. 93:566-576. https://doi.org/10.1046/j.1365-2672.2002.01731.x
  22. Lin, W., Hu, X., Zhang, W., Rogers, W. J. and Cai, W. 2005. Hydrogen peroxide mediates defence responses induced by chitosans of different molecular weights in rice. J. Plant Physiol. 162:937-944. https://doi.org/10.1016/j.jplph.2004.10.003
  23. Litterick, A. M., Harrier, L., Wallace, P., Watson, C. A. and Wood, M. 2004. The role of uncomposted materials, composts, manures, and compost extracts in reducing pest and disease incidence and severity in sustainable temperate agricultural and horticultural crop production: a review. Crit. Rev. Plant Sci. 23:453-479. https://doi.org/10.1080/07352680490886815
  24. Lopez-Moya, F., Suarez-Fernandez, M. and Lopez-Llorca, L. V. 2019. Molecular mechanisms of chitosan interactions with fungi and plants. Int. J. Mol. Sci. 20:332. https://doi.org/10.3390/ijms20020332
  25. Malerba, M. and Cerana, R. 2016. Chitosan effects on plant systems. Int. J. Mol. Sci. 17:996. https://doi.org/10.3390/ijms17070996
  26. Mokoena, M. P. 2017. Lactic acid bacteria and their bacteriocins:classification, biosynthesis and applications against uropathogens:a mini-review. Molecules 22:1255. https://doi.org/10.3390/molecules22081255
  27. Morin-Crini, N., Lichtfouse, E., Torri, G. and Crini, G. 2019. Applications of chitosan in food, pharmaceuticals, medicine, cosmetics, agriculture, textiles, pulp and paper, biotechnology, and environmental chemistry. Environ. Chem. Lett. 17:1667-1692. https://doi.org/10.1007/s10311-019-00904-x
  28. Rabea, E. I., Badawy, M. E.-T., Stevens, C. V., Smagghe, G. and Steurbaut, W. 2003. Chitosan as antimicrobial agent: applications and mode of action. Biomacromolecules 4:1457-1465. https://doi.org/10.1021/bm034130m
  29. Sawaguchi, A., Ono, S., Oomura, M., Inami, K., Kumeta, Y., Honda, K., Sameshima-Saito, R., Sakamoto, K., Ando, A. and Saito, A. 2015. Chitosan degradation and associated changes in bacterial community structures in two contrasting soils. Soil Sci. Plant Nutr. 61:471-480. https://doi.org/10.1080/00380768.2014.1003965
  30. 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. Biocon. Sci. Technol. 24:763-779. https://doi.org/10.1080/09583157.2014.894495
  31. Toplaghaltsyan, A., Bazukyan, I. and Trchounian, A. 2017. The effects of different carbon sources on the antifungal activity by lactic acid bacteria. Curr. Microbiol. 74:168-174. https://doi.org/10.1007/s00284-016-1168-8
  32. Tsuda, K., Tsuji, G., Higashiyama, M., Ogiyama, H., Umemura, K., Mitomi, M., Kubo,Y. and Kosaka, Y. 2016. Biological control of bacterial soft rot in Chinese cabbage by Lactobacillus plantarum strain BY under field conditions. Biol. Control 100:63-69. https://doi.org/10.1016/j.biocontrol.2016.05.010
  33. Verlee, A., Mincke, S. and Stevens, C. V. 2017. Recent developments in antibacterial and antifungal chitosan and its derivatives. Carbohydr. Polym. 164:268-283. https://doi.org/10.1016/j.carbpol.2017.02.001
  34. 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
  35. Xing, K., Zhu, X., Peng, X. and Qin, S. 2015. Chitosan antimicrobial and eliciting properties for pest control in agriculture:a review. Agron. Sustain. Dev. 35:569-588. https://doi.org/10.1007/s13593-014-0252-3