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Bataeva Yu.V., Grigoryan L.N., Bataeva A.D. Biological effectiveness of soil actinobacteria for growing Cucumis sativus L. in greenhouses. Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2025, Vol. 60, № 3, p. 516-529.
(how to cite this article)

doi: 10.15389/agrobiology.2025.3.516eng

UDC: 635.63:632:579.64

Acknowledgements:
Carried out within the framework of the industry research program of Rospotrebnadzor.

 

BIOLOGICAL EFFECTIVENESS OF SOIL ACTINOBACTERIA FOR GROWING Cucumis sativus L. IN GREENHOUSES

Yu.V. Bataeva1 ✉, L.N. Grigoryan2, A.D. Bataeva1

1Timiryazev Russian State Agrarian University—Moscow Agrarian Academy, 49, ul. Timiryazevskaya, Moscow, 127434 Russia, e-mail aveatab@mail.ru (✉ corresponding author), adbataeva2006@yandex.ru;
2Tatishchev Astrakhan State University, 20A, ul. Tatishcheva, Astrakhan, 414056 Russia, e-mail lilyagrigoryan90@gmail.com

ORCID:
Bataeva Yu.V. orcid.org/0000-0003-1064-3731
Bataeva A.D. orcid.org/0009-0009-9547-8253
Grigoryan L.N. orcid.org/0000-0002-1132-2043

Final revision received July 31, 2024
Accepted October 28, 2024

Chemical pesticides are used to control viral and fungal plant diseases and insect pests, but due to multiple treatments, the resistance of pathogens to them increases. Biopesticides serve as an alternative to chemical pesticides. The use of actinobacteria strains is promising for the development of new biologicals with antiviral, fungicidal and insecticidal effects. In this work, the effectiveness of actinobacterium Nocardiopsis umidischolae RCAM04882, N. umidischolae RCAM04883, Streptomyces carpaticus RCAM04697 in growing cucumber plants in greenhouses under the arid climate of the south of the Russian Federation were shown for the first time. Our goals was to investigate the effect of three strains of soil actinobacteria on cucumber (Cucumis sativus L.) cv. Forvard yield and the incidence of fungal and viral diseases and attacks of insect pests in a greenhouse (Astrakhan Province, 2019).. The plants were inoculated with 3-day cultures of the actinobacteria and suspensions of their dry biomass diluted in sterile distilled water to 1 mg/1 ml. N. umidischolae RCAM04882, N. umidischolae RCAM04883, Streptomyces carpaticus RCAM04697 strains (109 CFU/ml) were isolated from saline soils in the Astrakhan region in 2013. Tests were carried out under natural infectious loads. Root watering was applied 1 day after planting 2-3 true leaves’ seedling, 8 days after the first treatment during plant active growth, 8 days after the second treatment at budding and flowering. Then the plants were sprayed 14 days after the third treatment at ovary formation and milk ripeness, 14 days after the fourth treatment during active fruiting, and 14 days after the fifth treatment at harvesting. The treatments were as follows: 1 — positive control (treatment with the reference biological preparation Phytosporin-M (PS), paste) (NVP BashInkom LLC, Russia); 2 — negative control (treatment with tap water); 3 — treatment with suspension of N. umidischolae RCAM04882; 4 — treatment with suspension of N. umidischolae RCAM04883; 5 — treatment with suspension of S. carpaticus RCAM04697; 6 — treatment with suspension from dry biomass of strain N. umidischolae RCAM04882; 7 — treatment with suspension from dry biomass of strain N. umidischolae RCAM04883; 8 — treatment with suspension of dry S. carpaticus RCAM04697 biomass. The precursors of cucumber plants were tomatoes (Solanum lycopersicum) of the Grand variety. The soil was disinfected with copper sulfate before planting seedlings. The watering was carried out by drip method with a rate of 4.5-5 l per plant with tap water heated to 26 °С. Harvesting began on June 1, with the last harvest date being August 31. The insecticidal activity of actinobacteria strains against the melon aphid Aphis gossypii and the spider mite Tetranychus urticae was recorded on days 3 after the third and fourth treatments. The viral infections was detected by serological method at the stage of ovary formation (3 days after the third treatment) and fruit ripening (3 days after the fourth treatment). For immunochemical detection of viruses, Flashkits immunostrips (ImmunoStrip Test Kit, USA) were used. Antiviral activity was calculated as a percentage of the number of plants without symptoms. The identification of phytopathogenic fungi was carried out by hybridization-fluorescence detection of PCR products in real time using the AriaDNA microchip nucleic acid amplifier (LUMEX LLC, Russia). The yield was determined by summing the mass of ripe fruits in each variant. The maximum insecticidal (85.3 %) and acaricidal (69.2 %) activity was recorded during suspension treatment of a 3-day culture of S. carpaticus RCAM04697. The highest antiviral activity (100 %) was also found when treated with S. carpaticus RCAM04697 suspension — all plants were without symptoms of cucumber mosaic virus and tomato mosaic virus. For bacterization with all strains of actinobacteria, the symptoms of diseases caused by Fusarium oxysporum and Alternari a infecta were completely absent. In the variant with the treatment of cucumber plants with suspension of a 3-day culture S. carpaticus RCAM04697 showed the highest biological efficiency at a high yield (62.9 kg), which was 3.8 times higher compared to the negative control. The studied strains can be recommended for further testing in industrial field experiments when growing vegetables in an integrated plant protection system.

Keywords: actinobacteria, cucumbers, Nocardiopsis, Streptomyces, antiviral activity, fungicidal activity, insectoacaricidal activity.

 

REFERENCES

  1. Constant P., Chowdhury S.P., Pratscher J., Conrad R. Streptomycetes contributing to atmospheric molecular hydrogen soil uptake are widespread and encode a putative high-affinity (NiFe)-hydrogenase. Environmental Microbiology, 2010, 12(3): 821-829 CrossRef
  2. Smaoui S., Ennouri K., Chakchouk-Mtibaa A., Sellem I., Bouchaala K., Karray-Rebai I., Mellouli L., Ben Ayed R., Mathieu F. Modeling-based optimization approaches for the development of Anti-agrobacterium tumefaciens activity using Streptomyces sp. TN71. Microbial Pathogenesis, 2018, 119: 19-27 CrossRef
  3. Golińska P., Dahm H. Antagonistic properties of Streptomyces isolated from forest soils against fungal pathogens of pine seedlings. Dendrobiology, 2013, 69: 87-97 CrossRef
  4. Biliavska L.A., Pidlypska V.A., Kozyritska V.Ye., Iutynska G.A. Biosynthetic activity of soil streptomycetes — antagonists of plan-parasitic nematodes and phytopathogens. The Fourth European Conference on Biology and Medical Sciences. Vienna, Austria, 2015: 10-16.
  5. Shirokikh I.G., Nazarova Ya.I., Bakulina A.V., Abubakirova R.I. Teoreticheskaya i prikladnaya ekologiya, 2021, 1: 172-180 CrossRef (in Russ.).
  6. Nikitina E.P., Buyantueva L.B., Abidueva E.Yu., Sun Ch.Kh. Vavilovskiy zhurnal genetiki i selektsii, 2023, 27(4): 411-420 CrossRef (in Russ.).
  7. Badji B., Mostefaoui A., Sabaou N., Lebrihi A., Mathieu F., Seguin E., Tillequin F. Isolation and partial characterization of antimicrobial compounds from a new strain Nonomuraea sp. NM94. Journal of Industrial Microbiology and Biotechnology, 2007, 34(6): 403-412 CrossRef
  8. Amin D.H., Abdallah N.A, Abolmaaty A., Tolba S., Wellington E.M.H. Microbiological and molecular insights on rare Actinobacteria harboring bioactive prospective. Bulletin of the National Research Centre, 2020, 44: 5 CrossRef
  9. Jacquiod S., Franqueville L., Cécillon S., M. Vogel T., Simonet P. Soil Bacterial Community Shifts after Chitin Enrichment: An Integrative Metagenomic Approach Soil. PLoS ONE, 2013, 8(11): e79699 CrossRef
  10. Shahid M., Singh B.N., Verma S., Choudhary P., Das S., Chakdar H., Murugan K., Goswami S.K., Saxena A.K. Bioactive antifungal metabolites produced by Streptomyces amritsarensis V31 help to control diverse phytopathogenic fungi. Brazilian Journal of Microbiology, 2021, 52(4): 1687-1699 CrossRef
  11. Shaaban M., El-Mahdy A.M. Biosynthesis of Ag, Se, and Zno nanoparticles with antimicrobial activities against resistant pathogens using waste isolate Streptomyces enissocaesilis. IET Nanobiotechnology, 2018, 12(6): 741-747 CrossRef
  12. Mitra D., Mondal R., Khoshru B., Senapati A., Radha T., Mahakur B., Uniyal N., Myo E.M., Boutaj H., Guerra Sierra B.E., Panneerselvam P., Ganeshamurthy A., Anđjelković S., Vasić T., Rani A., Dutta S., das Mohapatra P.K. Actinobacteria-enhanced plant growth, nutrient acquisition, and crop protection: advances in soil, plant, and microbial multifactorial interactions. Pedosphere, 2022, 32(1): 149-170 CrossRef
  13. Grigoryan L.N., Bataeva Yu.V. Teoreticheskaya i prikladnaya ekologiya, 2023, 2: 6-19 CrossRef (in Russ.).
  14. Rainey F.A., Ward-Rainey N., Kroppenstedt R.M., Stackebrandt E. The genus Nocardiopsis represents a phylogenetically coherent taxon and a distinct actinomycete lineage: proposal of Nocardiopsaceae fam. NOV. International Journal of Systematic Bacteriology, 1996, 46(4): CrossRef
  15. Bennura T., Ravikumara A., Zinjardea S., JavdekarbV. Nocardiopsis species: incidence, ecological roles and adaptations. Microbiological Research, 2015, 174: 33-47 CrossRef
  16. Vijayabharathi R., Kumari B.R., Sathya A., Srinivas V., Abhishek R., Sharma H.C., Gopalakrishnan S. Biological activity of entomopathogenic actinomycetes against lepidopteran insects (Noctuidae: Lepidoptera). Canadian Journal of Plant Science, 2014, 94(4): 759-769 CrossRef
  17. Jung S.J., Kim N.K., Lee D.H., Hong S.I., Lee J.K. Screening and evaluation of Streptomyces species as a potential biocontrol agent against a wood Decay fungus, Gloeophyllum trabeum. Mycobiology, 2018, 46(2): 138-146 CrossRef
  18. Daulagala P.W.H.K.P. Chitinolytic endophytic bacteria as biocontrolagents for phytopathogenic fungi and nematode pests: a review. Asian Journal of Research in Botany,2021, 5(3): 14-24.
  19. Avramenko C.B., Galinkin V.A. Prikladnaya biokhimiya i mikrobiologiya, 2010, 46(4): 443-447 (in Russ.).
  20. Efimenko T.A., Malanicheva I.A., Vasil’eva B.F., Glukhova A.A., Sumarukova I.G., Boikova Yu.V., Malkina N.D., Terekhova L.P., Efremenkova O.V. Antibiotic activity of bacterial endobionts of basidiomycete fruit bodies. Microbiology, 2016, 85: 752-758 CrossRef
  21. Brzezinska M.S., Jankiewicz U., Burkowska A., Walczak M. Chitinolytic microorganisms and their possible application in environmental protection. Current Microbiology, 2014, 68(1): 71-81 CrossRef
  22. Manucharova N.A., Kuteinikova Y.V., Ivanov P.V., Nikolaeva S.K., Trofimov V.T., Stepanov P.Yu, Tyapkina E.V., Lipatov D.N., Stepanov A.L. Molecular analysis of the hydrolytic component of petroleum-contaminated soils and of soils remediated with chitin. Microbiology, 2017, 86: 395-402 CrossRef
  23. Silva G.C., Kitano I.T., Ribeiro I.A.F., Lacava P.T. The potential use of actinomycetes as microbial inoculants and biopesticides in agriculture. Front. Soil Sci., 2022, 2: 833181 CrossRef
  24. Sergeeva O.V., Dolzhenko T.V. Izvestiya Sankt-Peterburgskogo gosudarstvennogo agrarnogo universiteta, 2018, 2(51): 89-94 (in Russ.).
  25. Devanshi S., Shah K., Arora S., Saxena S. Actinomycetes as an environmental scrubber. In: Crude oil — new technologies and recent approaches. IntechOpen, 2022 CrossRef
  26. Das A.C., Mukherjee D. Soil application of insecticides influences microorganisms and plant nutrients. Applied Soil Ecology, 2000, 14(1): 55-62 CrossRef
  27. Danilenko V.N. Patent № 2147320 RF. MPK C12R1/645, C12C-C12Q, C12P1/06, C12P19/62 Shtamm Streptomyces avermitilis NITsB 132 — produtsent avermektinov. Patentoobladateli: Avtonomnaya nekommercheskaya organizatsiya "Nauchno-issledovatel’skiy tsentr biotekhnologii antibiotikov i drugikh biologicheski aktivnikh veshchestv "BIOAN". № 99119946/13. Zayavl. 22.09.1999. Opubl. 10.04.2000 [Patent No. 2147320 of the Russian Federation. IPC C12R1/645, C12C-C12Q, C12P1/06, C12P19/62 Strain Streptomyces avermitilis NICB 132 — producer of avermectins. Patent Holders: Autonomous Non-Commercial Organization "Research Center for Biotechnology of Antibiotics and Other Biologically Active Substances "BIOAN". No. 99119946/13. Claimed 09/22/1999. Published 04/10/2000](in Russ.).
  28. Burg R.W., Miller B.M., Baker E.E., Birnbaum J., Currie S.A., Hartman R., Kong Y.L., Monaghan R.L., Olson G., Putter I., Tunac J.B., Wallick H., Stapley E.O., Oiwa R., Ōmura S. Avermectins, new family of potent anthelmintic agents: producing organism and fermentation. Antimicrobial Agents and Chemotherapy, 1979, 15(3): 361-367 CrossRef
  29. Boykova I.V. Vestnik zashchiti rasteniy, 2016, 3(89): 30-32 (in Russ.).
  30. Grigoryan L.N., Bataeva Yu.V., Shlyakhov V.A., Dzerzhinskaya I.S. Patent № 2695157 C1 (RF) MPK C12N 1/20, A01N 63/02, C12R 1/465 Shtamm Streptomyces carpaticus dlya zashchiti ot nasekomikh-vrediteley, gribnikh, virusnikh bolezney i stimulyatsii rosta tomatov. Patentoobladateli: L.N. Grigoryan, Yu.V. Bataeva, V.A. Shlyakhov. № 2018113688. Zayavl. 13.04.2018. Opubl. 22.07.2019. Byul. № 21, 2019 [Patent No. 2695157 C1 (RF) IPC C12N 1/20, A01N 63/02, C12R 1/465 Streptomyces carpaticus strain for protection against insect pests, fungal, viral diseases and stimulation of tomato growth. Patent holders: L.N. Grigoryan, Yu.V. Bataeva, V.A. Shlyakhov. No. 2018113688. Claimed 04/13/2018. Published 07/22/2019. Bull. No. 21, 2019](in Russ.).
  31. Bataeva Yu.V., Grigoryan L.N., Bogun A.G., Kislichkina A.A., Platonov M.E., Kurashov E.A., Krylova J.V., Fedorenko A.G., Andreeva M.P. Biological activity and composition of metabolites of potential agricultural application from Streptomyces carpaticus K-11 RCAM04697 (SCPM-O-B-9993). Microbiology, 2023, 92(3): 459-467 CrossRef
  32. Raveh A., Delekta P.C., Dobry C.J., Peng W., Schultz P.J., Blakely P.K., Tai A.W., Matainaho T., Irani D.N., Sherman D.H., Miller D.J. Discovery of potent broad spectrum antivirals derived from marine actinobacteria. PLoS One, 2013, 8(12): e82318 CrossRef
  33. Dospekhov B.A. Metodika polevogo opita [Methods of field trials]. Moscow, 1985 (in Russ.).
  34. MUK 4.2.3533-18. Immunologicheskie metodi laboratornoy diagnostiki parazitarnikh bolezney. Metodicheskie ukazaniya [MUK 4.2.3533-18. Immunological methods of laboratory diagnostics of parasitic diseases. Methodical instructions]. Moscow, 2018 (in Russ.).
  35. Putsa N.M., Razgulyaeva N.V., Kostenko N.Yu., SolozhentsevaL.F. Metodicheskie ukazaniya po izucheniyu ustoychivosti kormovikh kul’tur k vozbuditelyam gribnikh bolezney na polevikh iskusstvennikh infektsionnikh fonakh [Guidelines for studying the resistance of forage crops to pathogens of fungal diseases on artificial infectious field backgrounds]. Moscow, 1999 (in Russ.).
  36. Ovchinnikova A.M.Metodi uskorennoy otsenki selektsionnogo materiala gorokha na infektsionnikh i provokatsionnikh fonakh. Metodicheskie rekomendatsii [Methods of accelerated evaluation of pea breeding material on infectious and provocative backgrounds. Methodical recommendations]. Moscow, 1990 (in Russ.).
  37. Grigoryan L.N. Biologicheskoe obosnovanie ispol’zovaniya aktinomitsetov — produtsentov antimikrobnikh metabolitov. Kandidatskaya dissertatsiya [Biological justification for the use of actinomycetes - producers of antimicrobial metabolites. PhD Thesis]. Obolensk, 2021 (in Russ.).
  38. Bataeva Yu.V. Osobennosti mikrobnikh kompleksov aridnoy zoni v usloviyakh agro- i tekhnogeneza i ikh biotekhnologicheskaya znachimost’. Doktorskaya dissertatsiya [Features of microbial complexes of the arid zone under conditions of agro- and technogenesis and their biotechnological significance. DSc Thesis]. Obolensk, 2023 (in Russ.).
  39. Grigoryan L.N., Bataeva Yu.V., Fedotova A.V., Yakovleva L.V. Ekologicheskie sistemi i pribori, 2023, 3: 30-39 CrossRef (in Russ.).
  40. Diab M.K., Mead H.M., Khedr M.A., Nafie M.S., Abu-Elsaoud A.M., El-Shatoury S.A. Metabolite profiling and in-silico studies show multiple effects of insecticidal actinobacterium on Spodoptera littoralis. Scientific Reports, 2024, 14: 3057 CrossRef
  41. Aggarwal N., Thind S., Sharma S. Role of secondary metabolites of actinomycetes in crop protection. In: Plant growth promoting actinobacteria. G. Subramaniam, S. Arumugam, V. Rajendran (eds.). Springer, Singapore, 2016: 99-121 CrossRef
  42. Tim Cushnie T.P., Cushnie B., Lamb A.J. Alkaloids: an overview of their antibacterial, antibiotic-enhancing and antivirulence activities. International Journal of Antimicrobial Agents, 2014, 44(5): 377-386 CrossRef
  43. Chowański S., Adamski Z., Marciniak P., Rosiński G., Büyükgüzel E., Büyükgüzel K., Falabella P., Scrano L., Ventrella E., Lelario F., Bufo S.A. A review of bioinsecticidal activity of Solanaceae alkaloids. Toxins, 2016, 8(3): 60 CrossRef
  44. Benslama O. Bioinsecticidal activity of actinomycete secondary metabolites against the acetylcholinesterase of the legume’s insect pest Acyrthosiphon pisum: a computational study. Journal of Genetic Engineering and Biotechnology, 2022, 20(1): 158 CrossRef
  45. Bataeva Yu.V., Grigoryan L.N. Biotekhnologiya,2024, 40(2): 84-92 CrossRef (in Russ.).
  46. Grigoryan L.N., Bataeva Yu.V., Shlyakhov V.A., Andreeva E.D., Egorov M.A. Sovremennaya nauka: aktual’nie problemi teorii i praktiki. Seriya «Estestvennie i tekhnicheskie nauki», 2018, 12: 14-22 (in Russ.).
  47. Grigoryan L.N., Bataeva Yu.V., Shlyakhov V.A., Magzanova D.K., Baymukhambetova A.S. Yug Rossii: ekologiya, razvitie, 2020, 15(2): 103-112 CrossRef (in Russ.).
  48. Novikova I.I., Boykova I.V., Shenin Yu.D. Vestnik zashchiti rasteniy, 2006, 3: 13-21 (in Russ.).
  49. Novikova I.I. Patent № 2226214C1 RF. MPK C12N 1/20(2006.01), A01N 63/00(2006.01), C12R 1/465(2006.01) Shtamm aktinomitseta Streptomyces chrysomallus R-21 dlya polucheniya biopreparata polifunktsional’nogo deystviya. Patentoobladatel’: Vserossiyskiy nauchno-issledovatel’skiy institut zashchiti rasteniy. № 2002117842/13. Zayavl. 02.07.2002. Opubl. 27.12.2003 [Patent No. 2226214C1 of the Russian Federation. IPC C12N 1/20(2006.01), A01N 63/00(2006.01), C12R 1/465(2006.01) Strain of actinomycete Streptomyces chrysomallus P-21 for obtaining a biopreparation with multifunctional action. Patent holder: All-Russian Research Institute for Plant Protection. No. 2002117842/13. Claimed 07/02/2002. Published 12/27/2003] (in Russ.).
  50. Ebrahimi-Zarandi M., Saberi Riseh R., Tarkka M.T. Actinobacteria as effective biocontrol agents against plant pathogens, an overview on their role in eliciting plant defense. Microorganisms, 2022, 10(9): 1739 CrossRef
  51. Singh S., Gupta R., Gaur R., Srivastava A. Antagonistic actinomycetes mediated resistance in Solanum lycopersicon Mill. against Rhizoctonia solani Kühn. Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci., 2015, 87(3): 789-798 CrossRef
  52. Shirokikh I.G., Liskova I.V., Nazarova Ya.I., Gradoboeva T.P., Pislegina S.S., Bokov N.A., Abubakirova R.I. Teoreticheskaya i prikladnaya ekologiya, 2022, 2: 173-182 CrossRef (in Russ.).
  53. Pavlyusin V.A., Novikova I.I., Boikova I.V. Microbiological control in phytosanitary optimization technologies for agroecosystems: research and practice (review).  Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2020, 55(3): 421-438 CrossRef
  54. Novikova I.I., Popova E.V., Kolesnikov L.E. Kolesnikova Yu.R., Chekurova S.S. Multifunctional biopreparations and complexes based on microorganisms and chitosan increase diseases resistance, productivity and leaf photosynthetic pigment contents in spring soft wheat (Triticum aestivum L.). Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2023, 58(1):158-183 CrossRef
  55. Teregulova G.A., Manucharova N.A., Urazbakhtina N.A., Zhemchuzhina N.S., Stepanov A.L. Antimicrobial activity of specialized metabolites of soil chitinolytic streptomycetes. Moscow University Soil Science Bulletin, 2024, 79: 47-55 CrossRef

 

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