Abstract
Trichoderma aggressivum, a mycopathogen causing green mould disease, is a major problem in Agaricus bisporus cultivation due to crop loss, and resistance to chemical fungicides. There is an urgent need for novel biological ways to control mycopathogens without affecting the growth of A. bisporus. Bacteria from the mushroom-casing environment were identified and tested for antagonistic effect on T. aggressivum. Bacillus velezensis produced a large zone of inhibition and its supernatant inhibited the growth of T. aggressivum [−37%], and slightly stimulated A. bisporus growth [+2%]. Label free quantitative-proteomic (LFQ) analysis of changes in the abundance of T. aggressivum proteins following exposure to B. velezensis supernatant indicated increased abundance of proteins associated with catabolic processing of amino acids (40-fold), amino oxidase proteins (14-fold), oxidoreductase proteins (13-fold, 4-fold) and hydrolases (3-fold). Proteins that decreased in relative abundance were antioxidants (29-fold), NTF2 domain containing protein (17-fold), 60S ribosomal protein L-13 (14-fold), glucoamylase proteins (13-fold), proteasome subunit proteins (11-fold) and other ribosomal proteins (9-fold). LFQ analysis revealed that exposing A. bisporus to B. velezensis supernatant led to a decrease in: prohibitin (13-fold, 6-fold), proteasomal proteins (11-fold), cytosolic adaptor domain containing protein (5-fold), aldehyde dehydrogenase (4-fold), ribosomal proteins (4-fold), DLH domain-containing protein (4-fold) and PKS_ER domain containing protein (3-fold). The results indicate that A. bisporus was not under stress upon contact with B. velezensis. Whereas a detrimental effect of B. velezensis on T. aggressivum is shown by inhibition of growth and damage-preventing proteins and increased abundance of proteins associated with stress.
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Abbreviations
- FDR:
-
False Discovery Rates
- GO:
-
gene ontology
- SSDA:
-
statistically significant differentially abundant
- DEP:
-
differentially expressed proteins
- LFQ:
-
Label free quantitative-proteomic
- ME:
-
malt extract
- CYM:
-
complete yeast media
- SN:
-
supernatant
- MPN:
-
Most probable number
- SE:
-
Standard error
References
Akinrinlola, R. J., Yuen, G. Y., Drijber, R. A., & Adesemoye, A. O. (2018). Evaluation of Bacillus strains for plant growth promotion and predictability of efficacy by in vitro physiological traits. International Journal of Microbiology, 2018, 1–11. https://doi.org/10.1155/2018/5686874.
Alexander, S. (2015). Horticulture in Ireland. Teagasc Research, 10(3), 18–19 https://www.teagasc.ie/media/website/publications/2015/TResearch-Autumn-15.pdf.
Anon, (2009). Directive 2009/128/EC of the European Parliament and of the Council of 21 October 2009, establishing a framework for Community action to achieve the sustainable use of pesticides. https://eur-lex.europa.eu/legal-content/EN/TXT/HTML/?uri=CELEX:02009L0128-20091125&from=EN
Bacon, C.W., Palencia, E.R., Hinton, D.M. (2015). Abiotic and biotic plant stress-tolerant and beneficial secondary metabolites produced by Endophytic Bacillus species, In: Arora, N.K. (Ed.), Plant microbes Symbiosis: Applied facets. Springer India, New Delhi, (pp. 163–177). https://doi.org/10.1007/978-81-322-2068-8_8.
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B, 57(1), 289–300.
Cawoy, H., Bettiol, W., Fickers, P., Onge, M. (2011). Bacillus-based biological control of plant diseases, in: Stoytcheva, M. (Ed.), Pesticides in the modern world - pesticides use and management. InTech.
Cho, W. C. S. (2007). Proteomics technologies and challenges. Genomics, Proteomics & Bioinformatics, 5, 77–85. https://doi.org/10.1016/S1672-0229(07)60018-7.
Fira, D., Dimkić, I., Berić, T., Lozo, J., & Stanković, S. (2018). Biological control of plant pathogens by Bacillus species. Journal of Biotechnology, 285, 44–55.
Fletcher, J.T., Yarham, D.J. (1976). The incidence of benomyl tolerance in Verticillium fungicola, Mycogone perniciosa and Hypomyces rosellus in mushroom crops. Annals of Applied Biology. 84, 343–353.
Gea, F. J., Navarro, M. J., & Tello, J. C. (2005). Reduced sensitivity of the mushroom pathogen Verticillium fungicola to prochloraz-manganese in vitro. Mycological Research, 109, 741–745.
Grewal, S. I. S., & Rainey, P. B. (1991). Phenotypic variation of Pseudomonas putida and P. tolizasii affects the chemotactic response to Agaricus bisporus mycelial exudate. Journal of General Microbiology., 137, 2761–2768.
Grogan, H. M. (2006). Fungicide control of mushroom cobweb disease caused by Cladobotryum strains with different benzimidazole resistance profiles. Pest Management Science, 62(2), 153–161. https://doi.org/10.1002/ps.1133.
Grogan, H.M. (2008). Challenges facing mushroom disease control in the 21st century. Mushroom biology and mushroom products. Proceedings of the Sixth International Conference on Mushroom Biology and Mushroom Products, Bonn, Germany: WSMBMP, (pp. 120–127).
Grogan, H. M., & Gaze, R. H. (2000). Fungicide resistance among Cladobotryum spp.: Causal agent of cobweb disease of the edible mushroom Agaricus bisporus. Mycology Research, 104, 357–364.
Harman, G. E., Obregón, M. A., Samuels, G., & Lorito, M. (2010). Changing models of biocontrol in the developing and developed world. Plant Disease, 94(8), 928–939.
Khan, N., Martínez-Hidalgo, P., Ice, T. A., Maymon, M., Humm, E. A., Nejat, N., Sanders, E. R., Kaplan, D., & Hirsch, A. M. (2018). Antifungal activity of Bacillus species against Fusarium and analysis of the potential mechanisms used in biocontrol. Frontiers in Microbiology, 9, 23–63. https://doi.org/10.3389/fmicb.2018.02363.
Kosanović, D., Potočnik, I., Duduk, B., Vukojević, J., Stajić, M., Rekanović, E., & Milijašević-Marčić, S. (2013). Trichoderma species on Agaricus bisporus farms in Serbia and their biocontrol. The Annals of Applied Biology, 163, 218–230.
Kosanović, D., Potočnik, I., Vukojević, J., Stajić, M., Rekanović, E., Stepanović, M., & Milijašević-Marčić, S. (2015). Fungicide sensitivity of Trichoderma spp. from Agaricus bisporus farms in Serbia. Journal of Environmental Science and Health, Part B, 50(8), 607–613. https://doi.org/10.1080/03601234.2015.1028849.
Kosanović, D., Sheehan, G., Grogan, H., & Kavanagh, K. (2019). Characterisation of the interaction of Pseudomonas putida and Pseudomonas tolaasii with Trichoderma aggressivum. European Journal of Plant Pathology, 156, 111–121. https://doi.org/10.1007/s10658-019-01867-z.
Klindworth, A., Pruesse, E., Schweer, T., Peplies, J., Quast, C., Horn, M., & Glöckner, F. O. (2013). Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Research, 41(1), e1. https://doi.org/10.1093/nar/gks808.
Kim, P., & Chung, K. C. (2004). Production of an antifungal protein for control of Colletotrichum lagenarium by Bacillus amyloliquefaciens MET0908. FEMS Microbiology Letters, 234, 177–183.
Leelasuphakul, W., Sivanunsakul, P., & Phongpaichit, S. (2006). Purification, characterization and synergistic activity of β-1,3-glucanase and antibiotic extract from an antagonistic Bacillus subtilis NSRS 89-24 against rice blast and sheath blight pathogens. Enzyme and Microbial Technology, 38, 990–997.
Leelasuphakul, W., Hemmanee, P., & Chuenchitt, S. (2008). Growth inhibitory properties of Bacillus subtilis strains and their metabolites against the green mold pathogen (Penicillium digitatum Sacc.) of citrus fruit. Postharvest Biology and Technology, 48, 113–121.
Lorito, M., Woo, S. L., Harman, G. E., & Monte, E. (2010). Translational research on Trichoderma: From ‘omics to the field. Annual Review of Phytopathology, 48, 395–417. https://doi.org/10.1146/annurev-phyto-073009-114314.
MacCanna, C., & Flanagan, J. B. (1972). Casing types and techniques. Mushroom Science, 3, 727–731.
Maher, A., Staunton, K., & Kavanagh, K. (2018). Analysis of the effect of temperature on protein abundance in Demodex-associated Bacillus oleronius. Pathogens and Disease, 76. https://doi.org/10.1093/femspd/fty032.
Marrone, P. G. (2002). An effective biofungicide with novel modes of action. Pesticide Outlook, 13, 193–194.
Mc Namara, L., Carolan, J. C., Griffin, C. T., Fitzpatrick, D., & Kavanagh, K. (2017). Analysis of the effect of entomopathogenic fungal culture filtrate on the immune response of the greater wax moth. Galleria mellonella. Journal of Insect Physiology, 100, 82–92.
Nagy, A., Manczinger, L., Tombácz, D., Hatvani, L., Gyõrfi, J., Antal, Z., Sajben, E., Vágvõllgyi, C., & Kredics, L. (2012). Biological control of oyster mushroom green mould disease by antagonistic Bacillus species. Biological Control of Fungal and Bacterial Plant Pathogens. IOBC-WPRS Bulletin, 78, 289–293.
Perez-Riverol, Y., Csordas, A., Bai, J., Bernal-Llinares, M., Hewapathirana, S., Kundu, D.J., Inuganti, A., Griss, J., Mayer, G., Eisenacher, M., Pérez, E., Uszkoreit, J., Pfeuffer, J., Sachsenberg, T., Yilmaz, S., Tiwary, S., Cox, J., Audain, E., Walzer, M., Jarnuczak, A.F., Ternent, T., Brazma, A., Vizcaíno, J.A. (2019). The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Research, 47(1): 442–450 (PubMed ID: 30395289).
Pandin, C., Védie, R., Rousseau, T., Le Coq, D., Aymerich, S., & Briandet, R. (2018). Dynamics of compost microbiota during the cultivation of Agaricus bisporus in the presence of Bacillus velezensis QST713 as biocontrol agent against Trichoderma aggressivum. Biological Control, 127, 39–54. https://doi.org/10.1016/j.biocontrol.2018.08.022.
Potočnik, I., Stepanović, M., Rekanović, E., Todorović, B., & Milijašević-Marčić, S. (2015). Disease control by chemical and biological fungicides in cultivated mushrooms: Button mushroom, oyster mushroom and shiitake. Journal of Pesticides and Phytomedicine, 30(4), 201–208. https://doi.org/10.2298/PIF1504201P.
Potočnik, I., Rekanović, E., Todorović, B., Luković, J., Paunović, D., Stanojević, O., & Milijašević-Marčić, S. (2019). The effects of casing soil treatment with Bacillus subtilis Ch-13 biofungicide on green mould control and mushroom yield. Journal of Pesticides and Phytomedicine, 34(1), 53–60. https://doi.org/10.2298/PIF1901053P.
Qiu, Z., Wu, X., Zhang, J., & Huang, C. (2017). High temperature enhances the ability of Trichoderma asperellum to infect Pleurotus ostreatus mycelia. PLoS One, 12(10), e0187055. https://doi.org/10.1371/journal.pone.0187055.
Radhakrishnan, R., Hashem, A., & Abd Allah, E. F. (2017). Bacillus: A biological tool for crop improvement through bio-molecular changes in adverse environments. Frontiers in Physiology, 8, 667. https://doi.org/10.3389/fphys.2017.00667 eCollection 2017.
Romaine, C. P., Royse, D. J., & Schlagnhaufer, C. (2005). Superpathogenic Trichoderma resistant to Topsin M found in Pennsylvania and Delaware. Mushroom News, 53, 6–9.
Royse, D.J., Baars, J., Tan, Q. (2017). Current overview of mushroom production in the world. In: Zied DC, Pardo-Giménez a (eds), edible and medicinal mushrooms, 1st edn. Technology and applications, (pp. 2–13).
Sansinenea, E. (2019). Bacillus Spp.: As plant growth-promoting Bacteria. In book: Secondary metabolites of plant growth-promoting, [ebook] Puebla, Pue, Mexico: Springer nature Singapore Pte ltd. https://doi.org/10.1007/978-981-13-5862-3_11.
Savoie, J.-M., Foulongne-Oriol, M., Barroso, G., & Callac, P. (2013). 1 genetics and genomics of cultivated mushrooms, application to breeding of agarics. In F. Kempken (Ed.), Agricultural applications, the Mycota (pp. 3–33). Heidelberg: Springer, Berlin. https://doi.org/10.1007/978-3-642-36821-9_1.
Stanlet, J., Preetha, G. (2016). Pesticide toxicity to non-target organisms exposure, Toxicity and Risk Assessment Methodologies. Springer Nature, 531p. https://link.springer.com/content/pdf/10.1007/978-94-017-7752-0.pdf
Tautorus, T. E., & Townsley, P. M. (1983). Biological control of olive green mold in Agaricus bisporus cultivation. Applied and Environmental Microbiology, 45(2), 511–515.
Védie, R., & Rousseau, T. (2008). Serenade biofungicide: une innovation mjeure dans les champignonnières françaises pour lutter contre Trichoderma aggressivum, agent de la moisissure verte du compost. La Lettre du CTC, 21, 1–2.
Wang, G., Cao, X., Ma, X., Guo, M., Liu, C., Yan, L., & Bian, Y. (2016). Diversity and effect of Trichoderma spp. associated with green mold disease on Lentinula edodes in China. Microbiologyopen, 5(4), 709–718. https://doi.org/10.1002/mbo3.364.
Weindling, R. (1932). Trichoderma lignorum as a parasite of other soil fungi. Phytopathology, 22, 837–845.
Živković, S., Stojanović, S., Ivanović, Z., Gavrilović, V., Popović, T., & Balaz, J. (2010). Screening of antagonistic activity of microorganisms against Colletotrichum acutatum and Colletotrichum gloeosporioides. Archives of Biological Sciences, 62(3), 611–623.
Acknowledgments
DK is a Postdoctoral Fellow supported by Irish Research Council, GOIPD/2018/115. Q-Exactive mass spectrometer was funded under the SFI Research Infrastructure Call 2012; Grant Number: 12/RI/2346. Dr. Thi Thuy Do, Maynooth University Antimicrobial Resistance and Microbiome Research Group, for helping with DNA extraction, sequencing, and identification.
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Kosanovic, D., Dyas, M., Grogan, H. et al. Differential proteomic response of Agaricus bisporus and Trichoderma aggressivum f. europaeum to Bacillus velezensis supernatant. Eur J Plant Pathol 160, 397–409 (2021). https://doi.org/10.1007/s10658-021-02252-5
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DOI: https://doi.org/10.1007/s10658-021-02252-5