Antagonistic activity of microorganisms isolated from chernozem against plant pathogens
Abstract
T. V. Sklyar*, O. A. Drehval, N. V. Cherevach, V. L. Matyukha, V. V. Sudak, S. S. Yaroshenko, N. V. Kuragina, Y. V. Lykholat, N. O. Khromykh, O. O. Didur, K. V. Lavrentieva and О. А. Lykholat
The aim of the work was to establish the antagonistic activity spectrum of microorganisms of different taxonomic groups isolated from Calcic Chernozem, against plant pathogens. Antagonistic activity of the soil microorganisms against phytopathogens was checked by diffusion in agar, taking into account the diameter of the growth inhibition zones around the blocks. The strains of phytopathogenic bacteria X a n t h o m o n a s c a m p e s t ris 8003b, P e c t o b a c t e riu m c a r o t o v o r u m 8982, P s e u d o m o n a s s y rin g a e p v . atrofaciens 8254, Pseudomonas syringae pv. lachrymans 7595 and fungi Fusarium oxysporum 54201, Fusarium culmorum 50716, Cladosporium herbarum 16878, Alternaria alternata 16 and Aspergillus niger 25 were used as the test cultures. Soil isolates were screened to determine the spectrum and level of their antagonistic activity in relation to test cultures of phytopathogens. The most active micromycetes isolates were Trichoderma lignorum 14, which exhibited antagonism against four of the five fungal species and three of the four bacteria, and T ric h o d e r m a lo n gib r a c hia t u m 17, active against all the tested plant pathogens. Among the actinobacteria, the most active isolates belonged to the genus Streptomyces : Streptomyces sp . 31 inhibited the growth of all tested plant pathogens, and Streptomyces sp. 35 showed antagonism against all phytopathogenic fungi and three of the four bacterial species. The most active bacterial isolates identified as Bacillus megaterium 3 and Bacillus brevis 6 inhibited the growth of all phytopathogenic cultures tested. All active antagonist isolates had no phytotoxic effect on spring barley seedlings, on the contrary, T. longibrachiatum 17 significantly increased the number of germinated seeds, and Streptomyces sp. 35 had a positive effect on shoot growth. Selected soil cultures can be used for the creation of plant protection products against fungal and bacterial disease.
Keywords: Soil microorganisms; Calcic chernozem; Phytopathogens; Antagonism; Plant protection
References
Abro, M. A., Sun, X., Li, X., Jatoi, G. N., & Guo, L. D. (2019). Biocontrol potential of fungal endophytes against Fusarium oxysporum f. sp. cucumerinum causing wilt in cucumber. Plant Pathology Journal, 35(6), 598–608. Doi: https://doi.org/10.5423/PPJ.OA.05.2019.0129
Alimova, F. K. (2006). Promyshlennoe primenenie gribov roda Trichoderma. [Industrial application of fungi Trichoderma genus]. Kazanskij gosudarstvennyj universitet, Kazan. (in Russian).
Asad, S. A., Ali, N., Hameed, A., Khan, S. A., Ahmad, R., Bilal, M., Shahzad, M., & Tabassum, A. (2014). Biocontrol efficacy of different isolates of Trichoderma against soil borne pathogen Rhizoctonia solani. Polish Journal of Microbiology, 63(1), 95–103.
Basler, R. (2016). Diversity of Fusarium species isolated from UK forage maize and the population structure of F. graminearum from maize and wheat. PeerJ, 4, e2143. Doi: https://doi.org/10.7717/peerj.2143
Belyavskaya, L. A., Efimenko, T. A., Efremenkova, O. V., Kozy`riczkaya, V. E., Iutinskaya, G. A. (2016). Identifikacziya i antagonisticheskie svojstva pochvennogo streptomiczeta Streptomyces sp. 100. [Identification and antagonistic properties of the soil streptomycetes Streptomyces sp. 100]. Mikrobiolohichnyi Zhurnal, 78(2), 61–73. (in Russian).
Buchanan, R. E. & Gibbons, N. E. (1974). Bergey's Manual of Determinative Bacteriology. Williams and Wilkins, Baltimore.
Holt, J. G., Krieg, N. R., Sneath, P. H. A., Stanley, J. T. & William, S. T. (1994). Bergey’s Manual of Determinative Bacteriology. Williams and Wilikins, Baltimore.
Bodhankar, S., Glover, V., Hemanth, S., Reddy, G., Rasul, S., Yadav, S. k., Desai, S., Mallappa, M., Mandapaka, M., & Srinivasarao, C. (2017). Maize seed endophytic bacteria: Dominance of antagonistic, lytic enzyme-producing Bacillus spp. 3. Biotechnology, 7(4), 232. Doi: https://doi.org/10.1007/s13205-017-0860-0
Brygadyrenko, V. V. (2015). Community structure of litter invertebrates of forest belt ecosystems in the Ukrainian Steppe Zone. International Journal of Environmental Research, 9(4), 1183–1192. Doi: https://doi.org/10.22059/IJER.2015.1008
Chibrik, T. S., Lukina, N. V., Filimonova, E. I., Glazyrina, M. A., Rakov, E. A., Maleva, M. G. & Prasad, M. N. V. (2016). Biological recultivation of mine industry deserts: Facilitating the formation of phytocoenosis in the middle Ural region, Russia. In: Prasad, M. N. V. (Ed.). Bioremediation and Bioeconomy. Elsevier, 389–418. https://doi.org/10.1016/B978-0-12-802830-8.00016-2
Colombo, E. M., Kunova, A., Cortesi, P., Saracchi, M., & Pasquali, M. Critical assessment of Streptomycesspp. Able to control toxigenic fusaria in cereals: a literature and patent review.International Journal of Molecular Sciences, 20(24), pii: E6119. Doi: https://doi.org/10.3390/ijms20246119
Dighton, J. (2003). Fungi in ecology processes. Marcel Dekker, Inc., New York, Basel. Domsh, K. H., Gams, W., & Anderson, T.-H. (2007). Compendium of soil fungi. IHW-Verlag, Eching.
Egorov, N. S. (2004). Osnovy uchenija ob antibiotikah. [Fundamentals of the doctrine of antibiotics]. Moscow. Nauka (in Russian). Fan, Y. T., Chung K. R., & Huang, J. W. F. (2019). Fungichromin production by Streptomyces padanus PMS-702 for controlling cucumber downy mildew. Plant Pathology Journal, 35(4), 341–350. Doi: https://doi.org/10.5423/PPJ.OA.03.2019.0057
Ibrahim, S. R. M., Abdallah, H. M., Elkhayat, E. S., Al Musayeib, N. M., Asfour, H. Z., Zayed, M. F., & Mohamed, G. A. (2017). Fusaripeptide A: new antifungal and anti-malarial cyclodepsipeptide from the endophytic fungus Fusarium sp. Journal of Asian Natural Products Research, 27, 1–11. Doi: https://doi.org/10.1080/10286020.2017.1320989
Irkitova, A. N., Grebenshchikova, A. V., Matsyura, A. V. (2018). Antagonistic activity of Bacillus subtilis strains isolated from various sources. Ukrainian Journal of Ecology, 8(2), 354-364. Doi: https://doi.org/10.15421/2018_354
IUSS Working Group WRB (2015). World Reference Base for Soil Resources 2014, Update 2015. International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports No. 106. FAO, Rome
Iutynska, G. O., & Ponomarenko, S. P. (2010). Bioreguljacija mikrobno-rastitelnyh sistem [Bioregulation of microbial-plant systems]. Kiev. Nichlava (in Russian).
Kaushal, K. S., Rao, D. V., & Amla, B. (2013). In vitro antimicrobial activities of endophytic fungi isolates from medicinal tree – Melia azedarach L. Journal of Microbiology Research, 3(1), 19–24. Doi: https://doi.org/10.5923/j.microbiology.20130301.03
Khong, N. G., Randoux, B., Deravel, J., Tisserant, B., Tayeh, C., Coutte, F., Bourdon, N., Jacques, P., & Reignault, P. (2013). Induction of resistance in wheat by bacterial cyclic lipopeptides. Communications in Agricultural and Applied Biological Sciences, 78(3), 479–487.
Khromykh, N. O., Lykholat, Y. V., Kovalenko, I. M., Kabar, A. M., Didur, O. O., & Nedzvetska, M. I. (2018). Variability of the antioxidant properties of Berberis fruits depending on the plant species and conditions of habitat. Regulatory Mechanisms in Biosystems, 9(1), 56–61. Doi: https://doi.org/10.15421/021807
Klymenko, G., Kovalenko, I., Lykholat, Y., Khromykh, N., Didur, O. & Alekseeva, A. (2017). Intehralna otsinka stanu populiatsii ridkisnykh vydiv roslyn [The integral assessment of the rare plant populations]. Ukrainian Journal of Ecology, 7(2), 201–209. (In Ukrainian). Doi: https://doi.org/10.15421/2017_37
Lykholat Y. V., Khromykh, N. O., Lykholat, T. Y., Bobrova, O. M., Didur, O. O., Lykholat, O. A., Sudak, V. M., Legostaeva T. V., Gtytzaj, Z. V., Kabar, A. M., Savosko,V. M., Kovalenko, I. M., Davydov, V. R., Suvorova, K. M., Dudkina, K. A., Kolinko, O. M., Grygoryuk, I. P. (2019a). Introduction success of less common species from the genus Berberis L. Ukrainian Journal of Ecology, 2019, 9(4), 634–640. Doi: https://doi.org/10.15421/2019_801
Lykholat, Y. V., Khromykh, N. O., Lykholat, T. Y., Didur O. O., Lykholat, O. A., Legostaeva, T. V., Kabar, A. M., Sklyar, T. V., Savosko, V. M., Kovalenko, I. M., Davydov, V. R., Bielyk, Y. V., Volyanik, K. O., Onopa, A. V., Dudkina, K. A., Grygoryuk, I. P. (2019b). Industrial characteristics and consumer properties of Chaenomeles Lindl. fruits. Ukrainian Journal of Ecology, 9(3), 132– 137. Doi: https://doi.org/10.15421/2019_720
Lykholat, Y., Khromykh, N., Didur, O., Alexeyeva, A., Lykholat, T., & Davydov, V. (2018a). Modeling the invasiveness of Ulmus pumila in urban ecosystems under climate change. Regulatory Mechanisms in Biosystems, 9(2), 161–166. Doi: https://doi.org/10.15421/021824
Lykholat, Y. V., Khromykh, N. O., Pirko, Y. V., Alexeyeva, A. A., Pastukhova, N. L., & Blume, Y. B. (2018b). Epicuticular wax composition of leaves of Tilia L. trees as a marker of adaptation to the climatic conditions of the steppe Dnieper. Cytology and Genetics, 52 (5), 323–330. Doi: https://doi.org/10.3103/S0095452718050067
Meena, K. R., & Kanwar, S. S. (2015). Lipopeptides as the antifungal and antibacterial agents: Applications in food safety therapeutics. BioMed Research International, 2015, 473050. Doi: https://doi.org/10.1155/2015/473050 Nazarenko, M., Lykholat, Y., Grigoryuk, I., & Khromykh, N. (2018). Optimal doses and concentrations of mutagens for winter wheat breeding purposes. Part I. Grain productivity. Journal of Central European Agriculture, 19(1), 194–205. Doi: https://doi.org/10.5513/JCEA01/19.1.2037
Nazarenko, M., Khromykh, N., Matyukha, V., Lykholat, Y., Bezus, R., Alexeeva, A., Lykholat, T., Shupranova, L. (2019). Chemical plant protection agents change the yield structure and the grain quality of winter wheat (Triticum aestivum L.). Bulletin of Transilvania University of Brasov - series II – Forestry, Wood Industry, Agricultural, Food Engineering, 12 (61), 2, 97-106. https://doi.org/10.31926/but.fwiafe.2019.12.61.2.8
Oldenburg, E., Höppner, F., Ellner, F. & Weinert, J. (2017). Fusarium diseases of maize associated with mycotoxin contamination of agricultural products intended to be used for food and feed. Mycotoxin Research, 33(3), 167–182. Doi:https://doi.org/10.1007/s12550-017-0277-y Pakhomov, A. E., Kulbachko, Y. L., Didur, O. A., & Loza, I. (2009). Mining dump rehabilitation: the potential role of bigeminatelegged milipeds (Diplopoda) and artificial mixed-soil habitats. In: Apostol, I. et al. (Eds). Optimization of disaster forecasting and prevention measures in the context of human and social dynamics, vol. 52. IOS Press, Amsterdam-Berlin-Tokyo-Washington, DC, pp. 163–171. Doi: https://doi.org/10.3233/978-1-58603-948-6-163.
Patyka, V. P., & Pasichnyk, L. A. (2014). Fitopatohenni bakterii: fundamentalni i prykladni aspekty [Phytopathogenic bacteria: fundamental and applied aspects] Visnyk Umanskoho natsionalnoho universytetu sadivnytstva, 2, 8–11. (in Ukrainian). Pirko, Y. V., Demkovich A. E., Kalafat L. O., Lykholat, O. A., Blume Y. B. (2018). Studying the genetic structure of Quercus robur forest stands on anthropogenically transformed territories using introns of the β-tubulin gene. Biosystems Diversity, 26(4), 269–275. Doi: https://doi.org/10.15421/011841
Pokhylenko, A., Lykholat, O., Didur, O., Kulbachko, Y., & Lykholat, T. (2019). Morphological variability of Rossiulus kessleri (Diplopoda, Julida) from different biotopes within Steppe Zone of Ukraine. Ukrainian Journal of Ecology, 9(1), 176–182.
Pozniak, S. P. (2016). Сhornozemy Ukrainy: heohrafiia, heneza I suchasnyi stan [Chernozems of Ukraine: genesis and current condition]. Ukrainskyi heohrafichnyi zhurnal, 1, 9–13. (in Ukrainian). Doi: https://doi.org/10.15407/ugz2016.01.009
Prudnikova, E. Y., & Savin, I. Y. (2015). Satellite assessment of dehumification of arable soils in Saratov region. Eurasian Soil Science, 48, 533–539. Doi:https://doi.org/10.1134/S1064229315050075
Qi, D., Zou, L, Zhou, D., Chen, Y., Gao, Z., Fenq, R., Zhanq, M., Li, K., Xie, J., & Wanq, W. (2019). Taxonomy and broad-spectrum antifungal activity of Streptomycessp. SCA3-4 isolated from rhizosphere soil of Opuntia stricta. Frontiers in Microbiology, 10, 1390. eCollection 2019. Doi: https://doi.org/10.3389/fmicb.2019.01390
Ribeiro, A. I., Costa, E. S., Thomasi, S. S., Brandão, D. F. R., Vieira, P. C., Fernandes, J. B., Forim, M. R., Ferreira, A. G., Pascholati, S. F., Gusmão, L. F. P., & da Silva, M. F. D. G. F. (2018). Biological and chemical control of Sclerotinia sclerotiorum using Stachybotrys levispora and its secondary metabolite griseofulvin. Journal Agricultural and Food Chemistry, 66(29), 7627–7632. Doi: https://doi.org/10.1021/acs.jafc.7b04197
Rishad, K. S., Rebello, S., Shabanamol, P. S., & Jisha, M. S. (2017). Biocontrol potential of halotolerant bacterial chitinase from high yielding novel Bacillus pumilus MCB-7 autochthonous to mangrove ecosystem. Pesticide Biochemistry and Physiology, 137, 36–41. Doi: https://doi.org/10.1016/j.pestbp.2016.09.005
Sarrocco, S., Mauro, A., & Battilani, P. (2019). Use of competitive filamentous fungi as an alternative approach for mycotoxin risk reduction in staple cereals: state of art and future perspectives. Toxins (Basel), 11(12), pii E701. Doi: https://doi.org/10.3390/toxins11120701
Savosko, V., Lykholat, Y., Bielyk, Y., & Lykholat, T. (2019). Ecological and geological determination of the initial pedogenesis on devastated lands in the Kryvyi Rih Iron Mining & Metallurgical District (Ukraine). Journal of Geology, Geography and Geoecology, 2019, 28(4), 738–746. https://doi.org/10.15421/111969
Savosko, V., Lykholat, Y., Domshyna, K., & Lykholat, T. (2018). Ekolohichna ta heolohichna zumovlenist poshyrennia derev I chaharnykiv na devastovanykh zemliakh Kryvorizhzhia [Ecological and geological determination of trees and shrubs’ dispersal on the devastated lands at Kryvorizhia]. Journal of Geology, Geography and Geoecology, 27(1), 116–130. (in Ukrainian). Doi: https://doi.org/10.15421/111837
Shakeel, Q., Lyu, F. Zhang, J., Wu, M., li, G., Hsiang, T., & Yang, L. (2018). Biocontrol of Aspergillus flavus on peanut kernels using Streptomyces yanglinensis 3-10. Frontiers in Microbiology, 9, 1049. eCollection 2018. Doi: https://doi.org/10.3389/fmicb.2018.01049
Shi, W., Tan, Y., Wang S., Gardiner, D. M., De Saeger, S., Liao, Y., Wang, C., Fan, Y., Wang, Z. &Wu, A. (2016). Mycotoxigenic potentials of Fusarium species in various culture matrices revealed by mycotoxin profiling. Toxins (Basel), 9(1), pii: E6. Doi: https://doi.org/10.3390/toxins9010006
Tepper, E. Z., Shilnikova, V. K., & Pereverzeva G. I. (2004). Praktikum po mikrobiologii. [Workshop on Microbiology]. Moscow. Drofa (in Russian). Trenozhnikova, L. P., Balgimbaeva, A. S., Ultanbekova, G. D., & Galimbaeva, R. S. (2018). Antifungalnaya aktivnost protiv patogenov zernovykh kultur i izuchenie antibiotika shtamma Streptomyces sp. strain K-541, vydelennogo iz ekstremalnykh sistem Kazakhstana [Antifungal activity against patogens of cereals and characterization of antibiotics of isolated from extreme ecosystems in Kazakhstan]. Selskokhozyajstvennaya biologiya, 53(1), 96–102. (in Russian). Doi: https://doi.org/10.15389/agrobiology.2018.1.96rus
Van Bohemen, A. I, Zalouk-Vergnoux, A., Poirier, L., Phuong, N. N., Inguimbert, N., Ben Haj Salah, K., Ruiz, N., & Pouchus, Y. F. (2016). Development and validation of LC-MS methods for peptaibol quantification in fungal extracts according to their lengths. Journal of Chromatography B: Analytical Technologies in the Biomedical and Life Sciences, 1009–1010, 25–33. Doi: https://doi.org/10.1016/j.jchromb.2015.11.039 Yamammoto, S., Shiraishi, S., & Suzuki, S. (2015). Are cyclic lipopeptides produced by Bacillus amyloliquefaciens S-13-3 responsible for the plant defense response in strawberry against Colletotrichum gloesporioides? Letters in Applied Microbiology, 60(4), 379–386. Doi: https://doi.org/10.1111/lam.12382
Yang, H. X., Ai H. L., Feng, T., Wang, W. X., Wu, B., Zheng, Y. S., Sun, H., He, J., Li, Z. H., & Liu, J. K. (2018). Trichothecrotocins A-C, antiphytopathogenic agents from potato endophytic fungus Trichothecium crotocinigenum. Organic Letters, 20(24), 8069– 8072. Doi: https://doi.org/10.1021/acs.orglett.8b03735
Zhang, P., Yuan, X. L., Du, Y. M., Zhang, H. B., Shen, G. M., Zhang, Z. F., Liang, Y. J., Zhao, D. L., & Xu, K. (2019). Angularly prenylated indole alkaloids with antimicrobial and insecticidal activities from an endophytic fungus Fusarium sambucinum TE-6L. Agricultural and Food Chemistry, 67(43), 11994–12001. Doi: https://doi.org/10.1021/acs.jafc.9b05827