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Novel approaches for application of biosurfactant produced by Pseudomonas aeruginosa for biocontrol of Colletotrichum capsici responsible for anthracnose disease in chilli

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Abstract

Anthracnose disease caused by fungal pathogen Colletotrichum capsici is considered to be one of the most destructive diseases in chilli cultivation as it infects and leads to complete destruction of the crop by infecting the mature fruit in the field and/or during the storage period. The management of the disease is difficult due to the absence of any resistant cultivar and effective fungicide. The current study was initiated to evaluate the antifungal efficacy of the biosurfactant produced by strain Pseudomonas aeruginosa JS29 for biological control of anthracnose disease. The results revealed significant disease reduction using biosurfactant in plant assay which were challenge-inoculated with the fungal spore. In vitro experiments clearly showed that the biosurfactant can effectively inhibit the growth of both spore and mycelia of the pathogen. Moreover, the biosurfactant can also effectively inhibit the fungal growth in detached-fruit assay in different storage conditions. The study confirmed that the biosurfactant has tremendous potential to become a viable, cost-effective and environment-friendly alternative for managing anthracnose disease in field and in post-harvest storage condition.

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References

  • Abildgren, M. P., Lund, F., Thrane, U., & Elmholt, S. (1987). Czapek-dox agar containing iprodione and dicloran as a selective medium for the isolation of Fusarium species. Letters in Applied Microbiology, 5, 83–86.

    Google Scholar 

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215(3), 403–410.

    CAS  PubMed  Google Scholar 

  • Anand, T., Chandrasekaran, A., Raguchander, T., Prakasam, T., & Samiyappan, R. (2007). Chemical and biological treatments for enhancing resistance in chili against Collectotrichum capsici and Leveillula taurica. Archives of Phytopathology and Plant Protection, 1, 1–19.

    Google Scholar 

  • Baider, A., & Cohen, Y. (2003). Synergistic interaction between BABA and Mancozeb in controlling Phytophthora infestans in potato and tomato and Pseudoperonospora cubensis in cucumber. Phytoparasitica, 31, 399–409.

    CAS  Google Scholar 

  • Boonyapipat, P. (2013). Study of three fungicides to control anthracnose (Colletotrichum capsici) in chilli (Capsicum frutescens): Case study from Songkhla province, Thailand. Acta Horticulturae (ISHS), 973, 103–108.

    Google Scholar 

  • Borah, S. N., Goswami, D., Lahkar, J., Sarma, H. K., Khan, M. R., & Deka, S. (2015). Rhamnolipid produced by Pseudomonas aeruginosa SS14 causes complete suppression of wilt by Fusarium oxysporum f. Sp. pisi in Pisum sativum. BioControl, 60(3), 375–385.

    CAS  Google Scholar 

  • Bosland, P. W., & Votava, E. J. (2003). Peppers: Vegetable and spice capsicums. In: Crop production science in horticulture. Wallingford: CAB International.

    Google Scholar 

  • Cannon, P. F., Damm, U., Johnston, P. R., & Weir, B. S. (2012). Colletotrichum – Current status and future directions. Studies in Mycology, 73, 181–213.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chanchaichaovivat, A., Ruenwongsa, P., & Panijpan, B. (2007). Screening and identification of yeast strains from fruits and vegetables: Potential for biological control of postharvest chili anthracnose (Colletotrichum capsici). Biological Control, 42, 326–335.

    Google Scholar 

  • Das, P., Mukherjee, S., & Sen, R. (2008). Antimicrobial potential of a lipopeptide biosurfactant derived from a marine Bacillus circulans. Journal of Applied Microbiology, 104, 1675–1684.

    CAS  PubMed  Google Scholar 

  • Dasgupta, B. (1981). Sporulation and relative virulence among isolates of Colletotrichum capsici causing anthracnose of betel vine. Indian Phytopathology, 34, 196–199.

    Google Scholar 

  • De Jonghe, K., De Dobbelaere, I., Sarrazyn, R., & Hofte, M. (2005). Control of brown root rot caused by Phytophthora cryptogea in the hydroponic forcing of witloof chicory (Cichorium intybus var. foliosum) by means of a nonionic surfactant. Crop Protection, 24(9), 771–778.

    CAS  Google Scholar 

  • Dugan, F.M. (2006). The identification of fungi. Saint Paul: American Phytopathological Society Press.

  • Gan, P., Ikeda, K., Irieda, H., Narusaka, M., O’Connell, R. J., Narusaka, Y., et al. (2013). Comparative genomic and transcriptomic analyses reveal the hemibiotrophic stage shift of Colletotrichum fungi. New Phytologist, 197, 1236–1249.

    CAS  PubMed  Google Scholar 

  • Gilman, J. (1957). A manual of soil fungi. Revised 2nd edn., Calcutta, Bombay: Oxford and IBH publishing company (Indian reprint). 436 pp.

  • Goswami, D., Handique, P. J., & Deka, S. (2014a). Rhamnolipid biosurfactant against Fusarium sacchari-the causal organism of pokkah boeng disease of sugarcane. Journal of Basic Microbiology, 54, 548–557.

    CAS  PubMed  Google Scholar 

  • Goswami, D., Borah, S. N., Lahkar, J., Handique, P. J., & Deka, S. (2015b). Antifungal properties of rhamnolipid produced by Pseudomonas aeruginosa DS9 against Colletotrichum falcatum. Journal of Basic Microbiology, 55, 1265–1274.

    CAS  PubMed  Google Scholar 

  • Higgins, D., Thompson, J., Gibson, T., Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.

    PubMed  PubMed Central  Google Scholar 

  • Hultberg, M., Bergstrand, K.J., Khalil, S., &Alsanius, B. (2008). Characterization of biosurfactant-producing strains of fluorescent pseudomonads in a soilless cultivation system. Antonie Van Leeuwenhoek, 94, 329–334.

  • Hultberg, M., Alsberg, T., Khalil, S., & Alsanius, B. (2010). Suppression of disease in tomato infected by Pythium ultimum with a biosurfactant produced by Pseudomonas koreensis. BioControl, 55, 435–444.

    CAS  Google Scholar 

  • Intanoo, W., & Chamswarng, C. (2007). Effect of antagonistic bacterial formulations for control of anthracnose on chilli fruits. In Proceeding of the 8th National Plant Protection Conference (pp. 309–322). Phisanulok: Naresuan University.

    Google Scholar 

  • Keith, L. M., Velasquez, M. E., & Zee, F. T. (2006). Identification and characterization of Pestalotiopsis spp. causing scab disease of guava, Psidium guajava in Hawaii. Plant Disease, 90, 16–23.

    CAS  PubMed  Google Scholar 

  • Kim, S. K., Kim, Y. C., Lee, S., Kim, J. C., Yun, M. Y., & Kim, I. N. (2011). Insecticidal activity of Rhamnolipid isolated from Pseudomonas sp. EP-3 against green peach aphid (Myzus persicae). Journal of Agriculture and Food Chemistry, 59(3), 934–938.

    CAS  Google Scholar 

  • Lahkar, J., Borah, S. N., Deka, S., & Ahmed, G. (2015). Biosurfactant of Pseudomonas aeruginosa JS29 against Alternaria solani: The causal organism of early blight of tomato. BioControl, 60(3), 401–411.

    CAS  Google Scholar 

  • Liljeroth, E., Bengtsson, T., Wiik, L., & Andreasson, E. (2010). Induced resistance in potato to Phytphthora infestans - effects of BABA in greenhouse and field tests with different potato varieties. European Journal of Plant Pathology, 127, 171–183.

    CAS  Google Scholar 

  • Manandhar, J. B., Hartman, G. L., & Wang, T. C. (1995). Anthracnose development on pepper fruits inoculated with Colletotrichum gloeosporioides. Plant Disease, 79, 380–383.

    Google Scholar 

  • Mansour, S. A., Belal, M. H., Abou-Arab, A. A. K., Ashour, H. M., & Gad, M. F. (2008). Evaluation of some pollutant levels in conventionallyand organically farmed potato tubers and their risks to human health. Food and Chemical Toxicology, 47, 615–624.

    PubMed  Google Scholar 

  • Mata-Sandoval, J. C., Karns, J., & Torrents, A. (2001). Effect of nutritional and environmental conditions on the production and composition of rhamnolipids by P. aeruginosa UG2. Microbiological Research, 155(4), 249–256.

    CAS  PubMed  Google Scholar 

  • McKinney, H. H. (1923). Influence of soil temperature and moisture on infection of wheat seedlings by Helmintosporium sativum. Journal of Agriculture Research, 26, 195–219.

    Google Scholar 

  • Nagamani, A., Kunwar, I. K., & Manoharachary, C. (2006). Handbook of soil fungi (1st ed.). New Delhi: I.K International Pvt. Ltd. (436 pp).

    Google Scholar 

  • Nantawanit, N., Chanchaichaovivat, A., Panijpan, B., & Ruenwongsa, P. (2010). Induction of defense response against Colletotrichum capsici in chili fruit by the yeast Pichia guilliermondii strain R13. Biological Control, 52, 145–152.

    CAS  Google Scholar 

  • Nielsen, C. J., Ferrin, D. M., & Stanghellini, M. E. (2006). Efficacy of biosurfactants in the management of Phytophthora capsici on pepper in recirculating hydroponic systems. Canadian Journal of Plant Pathology, 28, 450–460.

    CAS  Google Scholar 

  • Nihorimbere, V., Ongena, M., Smargiassi, M., & Thonart, P. (2011). Beneficial effect of the rhizosphere microbial community for plant growth and health. Biotechnologie, Agronomie, Société et Environnement, 15(2), 327–337.

    Google Scholar 

  • Nitschke, M., & Costa, S. G. V. A. O. (2007). Biosurfactants in food industry. Trends in Food Science and Technology, 18, 252–259.

    CAS  Google Scholar 

  • Nunes, C. A. (2012). Biological control of postharvest diseases of fruit. European Journal of Plant Pathology, 133, 181–196.

    Google Scholar 

  • Oanh, L. T. K., Korpraditskul, V., Rattanakreetakul, C., & Wasee, S. (2006). Influence of biotic and chemical plant inducers on resistance of chili to anthracnose. Kasetsart Journal (Natural Science), 40, 39–48.

    Google Scholar 

  • Oberbremer, A., Muhller-Hurtig, R., & Wagner, F. (1990). Effect of addition of microbial surfactant on hydrocarbon degradation in soil population in stirred reactor. Applied Microbiology and Biotechnology, 32, 485–489.

    CAS  PubMed  Google Scholar 

  • Ojiambo, P. S., & Scherm, H. (2006). Biological control and application-oriented factors influencing plant disease suppression by biological control: A meta-analytical review. Phytopathology, 96, 1168–1174.

    CAS  PubMed  Google Scholar 

  • Oro, L., Feliziani, E., Ciani, M., Romanazzi, G., & Comitini, F. (2014). Biocontrol of postharvest brown rot of sweet cherries by Saccharomyces cerevisiae Disva 599, Metschnikowia pulcherrima Disva 267 and Wickerhamomyces anomalus Disva 2 strains. Postharvest Biology and Technology, 96, 68–64.

    Google Scholar 

  • Perfumo, A., Banat, I. M., Canganella, F., & Marchant, R. (2006). Rhamnolipid production by a novel thermos-tolerant hydrocarbon-degrading Pseudomonas aeruginosa AP02-1. Journal of Applied Microbiology, 75, 132–138.

    Google Scholar 

  • Poremba, K., Gunkel, W., Lang, S., Wagner, F. (1991). Marine biosurfactants III toxicity testing with marine microorganisms and comparison with synthetic surfactants. Z. Naturforsch., 46c, 210-216.

    CAS  Google Scholar 

  • Prusky, D., Koblier, I., Aridi, R., Beno-Moalem, D., Yakoby, N., & Keen, N. T. (2000). Resistance mechanisms of subtropical fruits to Colletotrichum gloeosporioides. In J. A. Bailey & M. J. Jeger (Eds.), Colletotrichum: Biology, Pathology and control (pp. 232–244). Wallingford: CAB International.

    Google Scholar 

  • Ramamoorthy, V., & Samiyappan, R. (2001). Induction of defense-related genes in Pseudomonas fluorescens treated chilli plants in response to infection by Colletotrichum capsici. Journal of Mycology and Plant Pathology, 31, 146–155.

    CAS  Google Scholar 

  • Saikia, R. R., Deka, S., Deka, M., & Sarma, H. (2012). Optimization of environmental factors for improved production of rhamnolipid biosurfactant by Pseudomonas aeruginosa RS29 on glycerol. Journal of Basic Microbiology, 52, 446–457.

    CAS  PubMed  Google Scholar 

  • Sambanthamoorthy, K., Feng, X., Patel, R., Patel, S., & Paranavitana, C. (2014). Antimicrobial and antibiofilm potential of biosurfactants isolated from lactobacilli against multi-drug-resistant pathogens. BMC Microbiology, 14(197), 1–9.

    Google Scholar 

  • Sanchez, L., Courteaux, B., Hubert, J., Kauffmann, S., Renault, J. H., Clément, C., et al. (2012). Rhamnolipids elicit defense responses and induce disease resistance against biotrophic, hemibiotrophic, and necrotrophic pathogens that require different signaling pathways in Arabidopsis and highlight a central role for salicylic acid. Plant Physiology, 160, 1630–1641.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Santos, E. C., Jacques, R. J. S., Bento, F. M., Peralba, M. C. R., Selbach, P. A., Sá, E. L. S., et al. (2008). Anthracene biodegradation and surface activity by an iron-stimulated Pseudomonas sp. Bio/Technology, 99(7), 2644–2649.

    CAS  Google Scholar 

  • Sen, R., & Swaminathan, T. (2005). Characterization of concentration and purification parameters and operating conditions for the small-scale recovery of surfactin. Process Biochemistry, 40, 2953–2958.

    CAS  Google Scholar 

  • Sha, R., Jiang, L., Meng, Q., Zhang, G., & Song, Z. (2011). Producing cell-free culture broth of rhamnolipids as a cost-effective fungicide against plant pathogens. Journal of Basic Microbiology, 52, 458–466.

  • Sharma, P. N., Kaur, M., Sharma, O. P., Sharma, P., & Pathania, A. (2005). Morphological, pathological and molecular variability in Colletotrichum capsici, the cause of fruit rot of chillies in the subtropical region of north-western Indian. Journal of Phytopathology, 153, 232–237.

    Google Scholar 

  • Singh, A., Hamme, J. D. V., & Ward, O. P. (2007). Surfactants in microbiology and biotechnology: Part 2. Application aspects. Biotechnology Advances, 25(1), 99–121.

    CAS  PubMed  Google Scholar 

  • Singh, A. K., Rautela, R., & Cameotra, S. S. (2014). Substrate dependent in vitro antifungal activity of Bacillus sp. strain AR2. Microbial Cell Factory, 13(67), 1–11.

    CAS  Google Scholar 

  • Sotirova, A., Spasova, D., Vasileva-Tonkova, E., & Galabova, D. (2009). Effect of rhamnolipid-biosurfactant on cell-surface of Pseudomonas aeruginosa. Microbiological Research, 164, 297–303.

    CAS  PubMed  Google Scholar 

  • Sotirova, A., Avramova, T., Stoitsova, S., Lazarkevich, I., Lubenets, V., Karpenko, E., et al. (2012). The importance of rhamnolipid-biosurfactant-induced changes in bacterial membrane lipids of Bacillus subtilis for the antimicrobial activity of thiosulfonates. Current Microbiology, 65, 534–541.

    CAS  PubMed  Google Scholar 

  • Srinivas, C., Niranjana, S.R., Kumar, P., Chandra L., Nayaka, S., Shetty, H.S. (2006). Effect of fungicides and bioagents against Collectotrichum capsici on seed quality of chilli. Indian Phytopathology, 59, 62–67.

  • Stanghellini, M. E., & Miller, R. M. (1997). Biosurfactants: Their identity and potential efficacy in the biological control of zoosporic plant pathogens. Plant Disease, 81, 4–12.

    CAS  PubMed  Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10), 2731–2739.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Than, P. P., Jeewon, R., Hyde, K. D., Pongsupasamit, S., Mongkolporn, O., & Taylor, P. W. J. (2008). Characterization and pathogenicity of Colletotrichum species associated with anthracnose on chilli (Capsicum spp.) in Thailand. Plant Pathology, 57, 562–572.

    Google Scholar 

  • U.S. EPA (U.S. Environmental Protection Agency) (2004). Abandoned uranium mines on the Navajo Nation, Arizona. EPA Region 9.

  • Varnier, A. L., Sanchez, L., Vatsa, P., Boudesocque, L., Garcia-Brugger, A., Rabenoelina, F., et al. (2009). Bacterial rhamnolipids are novel MAMPs conferring resistance to Botrytis cinerea in grapevine. Plant, Cell and Environment, 32, 178–193.

    CAS  PubMed  Google Scholar 

  • Vatsa, P., Sanchez, L., Clement, C., Baillieul, F., & Dorey, S. (2010). Rhamnolipid biosurfactants as new players in animal and plant defense against microbes. International Journal of Molecular Sciences, 11(12), 5095–5108.

    CAS  PubMed  PubMed Central  Google Scholar 

  • White, T. J., Bruns, T., Lee, S., & Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & Y. J. White (Eds.), PCR protocols: A guide to methods and application (pp. 315–322). San Diego: Academic Press.

    Google Scholar 

  • Yan, F., Xu, S., Guo, J., Chen, Q., Meng, Q., & Zheng, X. (2014). Biocontrol of post-harvest Alternaria alternata decay of cherry tomatoes with rhamnolipids and possible mechanisms of action. Journal of the Science of Food and Agriculture, 95(7), 1469–1474.

    PubMed  Google Scholar 

  • Yoshida, S., Koitabashi, M., Nakamura, J., Fukuoka, T., Sakai, H., Abe, M., Kitamoto, D., & Kitamoto, H. (2015). Effects of biosurfactants mannosylerythritol lipids on the hydrophobicity of solid surfaces and infection behaviors of plant pathogenic fungi. Journal of Applied Microbiology, 119(1), 215–224.

    CAS  PubMed  Google Scholar 

  • Zaragoza, A., Aranda, F. J., Espuny, M. J., Teruel, J. A., Marqués, A., Manresa, Á., & Antonio, O. (2009). Mechanism of membrane permeabilization by a bacterial trehalose lipid biosurfactant produced by Rhodococcus sp. Langmuir, 25, 7892–7898.

    CAS  PubMed  Google Scholar 

  • Zeraik, A. E., & Nitschke, M. (2010). Biosurfactants as agents to reduce adhesion of pathogenic bacteria to polystyrene surfaces: Effect of temperature and hydrophobicity. Current Microbiology, 61(6), 554–559.

    CAS  PubMed  Google Scholar 

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Acknowledgements

The first author is thankful to the Department of Biotechnology (DBT), Government of India for providing assistance as a Senior Research Fellow (SRF) to carry out the research work under the project BT/186/NE/TBP/2011 sponsored by the Department of Biotechnology, Govt. of India to the corresponding author. Authors would like to acknowledge Dr. Hemen Deka, Jintu Rabha, Assistant Professor, Gauhati University and Siddhartha Narayan Borah, Senior Research Fellow, Life Science Division, Institute of Advanced Study in Science and Technology, Assam, India for their contribution in statistical analysis, phylogenetic analysis and scanning electron microscopy, respectively.

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Lahkar, J., Goswami, D., Deka, S. et al. Novel approaches for application of biosurfactant produced by Pseudomonas aeruginosa for biocontrol of Colletotrichum capsici responsible for anthracnose disease in chilli. Eur J Plant Pathol 150, 57–71 (2018). https://doi.org/10.1007/s10658-017-1252-3

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