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Biocontrol Potential of Novel Borrelidin-Producing Streptomyces rochei 3IZ-6 Isolated from Soil

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Abstract

A complex of soil actinomycetes in the upper horizon of Grumusol (Vertisol) on the western coast of Lake Kinneret in the vicinity of Tiberias (Lower Galilee, Israel) was studied. A high-throughput screening of the antibiotic activity of 26 isolates of the genus Streptomyces using on a dual reporter system revealed the strain 3IZ-6, which had the ability to inhibit protein synthesis. This strain was assigned to Streptomyces rochei according to the polyphase taxonomy approach. The active substance of S. rochei 3IZ-6 was isolated and purified using solid-phase extraction and high-performance liquid chromatography. Toeprint analysis and mass spectrophotometric data allowed us to identify this active compound as borrelidin, a known inhibitor of protein biosynthesis. When co-cultivated on solid media, strain 3IZ-6 is able to suppress the growth of phytopathogenic microorganisms Fusarium solani, F. sambucinum, and Botrytis cinerea, as well as the quarantine object Curtobacterium flaccumfaciens. The cultural liquid of 3IZ-6 had a pronounced phytotoxic effect on the seeds of common wheat (Triticum aestivum L.). Strain Streptomyces rochei 3IZ-6 can find application in biotechnology as a producer of borrelidin, a valuable natural compound with a wide spectrum of antibiotic activity, which can be used as a biocontrol agent for crop protection from phytopathogens and weeds.

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REFERENCES

  1. G. F. Gauze, T. P. Preobrazhenskaya, M. A. Sveshnikova, L. P. Terekhova, and T. S. Maksimova, Determinant of Actinomycetes: Streptomyces, Streptoverticillium, Chainia Genera (Nauka, Moscow, 1983) [in Russian].

    Google Scholar 

  2. D. G. Zvyagintsev and G. M. Zenova, Ecology of Actinomycetes (GEOS, Moscow, 2001) [in Russian].

    Google Scholar 

  3. I. A. Kozhevnikova and V. I. Shveikina, “Modeling level variations in Lake Kineret,” Water Resour. 41 (6), 627–633 (2014).

    Article  Google Scholar 

  4. Y. Oziransky, A. G. Kalmakova, and I. L. Margolina, “Integrated scarce water resource management for a sustainable water supply in arid regions (the experience of the state of Israel),” Arid Ecosyst. 4 (4), 270–276 (2014)

    Article  Google Scholar 

  5. I. Stancheva, Atlas of Crop Diseases (Pensoft, Sofia–Moscow, 2005) [in Russian].

    Google Scholar 

  6. M. B. Shapiro, “Soils of Israel,” Eurasian Soil Sci. 39 (11), 1170–1175 (2006)

    Article  Google Scholar 

  7. V. A. Alferova, T. P. Maviza, M. V. Biryukov, Y. V. Zakalyukina, D. A. Lukianov, D. A. Skvortsov, and I. A. Osterman, “Biological evaluation and spectral characterization of a novel tetracenomycin X congener,” Biochimie 192, 63–71 (2022). https://doi.org/10.1016/j.biochi.2021.09.014

    Article  Google Scholar 

  8. R. M. Atlas, Handbook of Microbiological Media (CRC Press, 2004).

    Book  Google Scholar 

  9. A. A. Baranova, A. A. Chistov, A. P. Tyurin, I. A. Prokhorenko, V. A. Korshun, M. V. Biryukov, and Y. V. Zakalyukina, “Chemical ecology of streptomyces albidoflavus strain a10 associated with carpenter ant camponotus vagus,” Microorganisms 8 (12), 1948 (2020).

    Article  Google Scholar 

  10. A. A. Belimov and K.-J. Dietz, “Effect of associative bacteria on element composition of barley seedlings grown in solution culture at toxic cadmium concentrations,” Microbiol. Res. 155 (2), 113–121 (2000). https://doi.org/10.1016/S0944-5013(00)80046-4

    Article  Google Scholar 

  11. J. Berger, L. M. Jampolsky, and M. W. Goldberg, “Borrelidin, a new antibiotic with antiborrelia activity and penicillin enhancement properties,” Arch. Biochem. 22 (3), 476–478 (1949).

    Google Scholar 

  12. Bergey’s Manual of Systematic Bacteriology, Vol. 5: The Actinobacteria, Part A, Ed. by. M. Goodfellow et al. (Springer, New York, 2012).

  13. Z. Cao, G. Khodakaramian, K. Arakawa, and H. Kinashi, “Isolation of borrelidin as a phytotoxic compound from a potato pathogenic Streptomyces strain,” Biosci., Biotechnol., Biochem. 76 (2), 353–357 (2012). https://doi.org/10.1271/bbb.110799

    Article  Google Scholar 

  14. Y.-Y. Chen, P.-C. Chen, and T.-T. Tsay, “The biocontrol efficacy and antibiotic activity of Streptomyces plicatus on the oomycete Phytophthora capsica,” Biol. Control 98, 34–42 (2016). https://doi.org/10.1016/j.biocontrol.2016.02.011

    Article  Google Scholar 

  15. Y.-M. Gao, Y. M. Gao, X. J. Wang, J. Zhang, M. Li, C. X. Liu, J. An, and W. S. Xiang, “Borrelidin, a potent antifungal agent: insight into the antifungal mechanism against Phytophthora sojae,” J. Agric. Food Chem. 60 (39), 9874–9881 (2012). https://doi.org/10.1021/jf302857x

    Article  Google Scholar 

  16. D. Habibi, N. Ogloff, R. B. Jalili, A. Yost, A. P. Weng, A. Ghahar, and C. J. Ong, “Borrelidin, a small molecule nitrile-containing macrolide inhibitor of threonyl-tRNA synthetase, is a potent inducer of apoptosis in acute lymphoblastic leukemia,” Invest. New Drugs 30 (4), 1361–1370 (2012). https://doi.org/10.1007/s10637-011-9700-y

    Article  Google Scholar 

  17. A. Hamed, A. S. Abdel-Razek, M. Frese, D. Wibberg, A. F. El-Haddad, T. M. Ibrahim, J. Kalinowski, et al., “N-Acetylborrelidin B: a new bioactive metabolite from Streptomyces mutabilis sp. MII,” Z. Naturforsch., C: J. Biosci. 73 (1–2), 49–57 (2018). https://doi.org/10.1515/znc-2017-0140

    Article  Google Scholar 

  18. N. Hazan, M. Stein, A. Agnon, S. Marco, D. Nadel, J. F. Negendank, and D. Neev, “The late Quaternary limnological history of Lake Kinneret (Sea of Galilee), Israel,” Quat. Res. 63 (1), 60–77 (2005). https://doi.org/10.1016/j.yqres.2004.09.004

    Article  Google Scholar 

  19. M. Li, J. Zhang, C. Liu, B. Fang, X. Wang, and W. Xiang, “Identification of borrelidin binding site on threonyl-tRNA synthetase,” Biochem. Biophys. Res. Commun. 451 (4), 485–490 (2014). https://doi.org/10.1016/j.bbrc.2014.07.100

    Article  Google Scholar 

  20. M. Lumb, PE. Macey, J. Spyvee, J. M. Whitmarsh, and R. D. Wright, “Isolation of vivomycin and borrelidin, two antibiotics with anti-viral activity, from a species of Streptomyces (C2989),” Nature 206 (4981), 263–265 (1965). https://doi.org/10.1038/206263a0

    Article  Google Scholar 

  21. C. Olano, S. J. Moss, A. F. Braña, R. M. Sheridan, V. Math, A. J. Weston, and J. A. Salas, “Biosynthesis of the angiogenesis inhibitor borrelidin by Streptomyces parvulus Tü4055: insights into nitrile formation†,” Mol. Microbiol. 52 (6), 1745–1756 (2004). https://doi.org/10.1111/j.1365-2958.2004.04090.x

    Article  Google Scholar 

  22. C. Orelle, S. Carlson, B. Kaushal, M. M. Almutairi, H. Liu, A. Ochabowicz, and A. S. Mankin, “Tools for characterizing bacterial protein synthesis inhibitors,” Antimicrob. Agents Chemother. 57 (12), 5994–6004 (2013). http://aac.asm.org/content/57/12/5994.

    Article  Google Scholar 

  23. I. A. Osterman, E. S. Komarova, D. I. Shiryaev, I. A. Korniltsev, I. M. Khven, D. A. Lukyanov, and O. A. Dontsova, “Sorting out antibiotics’ mechanisms of action: a double fluorescent protein reporter for high-throughput screening of ribosome and DNA biosynthesis inhibitors,” Antimicrob. Agents Chemother. 60 (12), 7481–7489 (2016). https://doi.org/10.1128/AAC.02117-16

    Article  Google Scholar 

  24. K. Otoguro, H. Ui, A. Ishiyama, M. Kobayashi, H. Togashi, Y. Takahashi, R. Masuma, et al., “In vitro and in vivo antimalarial activities of a non-glycosidic 18-membered macrolide antibiotic, borrelidin, against drug-resistant strains of plasmodia,” J. Antibiot. 56 (8), 727–729 (2003). https://doi.org/10.7164/antibiotics.56.727

    Article  Google Scholar 

  25. R. V. Rai and J. A. Bai, Natural Products from Actinomycetes: Diversity, Ecology and Drug Discovery (Mysore, 2022). https://doi.org/10.1007/978-981-16-6132-7

  26. D. I. Shiriaev, A. A. Sofronova, E. A. Berdnikovich, D. A. Lukianov, E. S. Komarova, V. I. Marina, and O. A. Dontsova, “Nybomycin inhibits both fluoroquinolone-sensitive and fluoroquinolone-resistant Escherichia coli DNA gyrase,” Antimicrob. Agents Chemother. 65 (5), e00777-20 (2021). https://doi.org/10.1128/AAC.00777-20

    Article  Google Scholar 

  27. E. B. Shirling and D. Gottlieb, “Methods for characterization of Streptomyces species,” Int. J. Syst. Bacteriol. 16 (3), 313–340 (1966).

    Article  Google Scholar 

  28. A. Singer, The Soils of Israel (Springer, Berlin, Heidelberg, 2007).https://doi.org/10.1007/978-3-540-71734-8

  29. J. Sun, J. Shao, C. Sun, Y. Song, Q. Li, L. Lu, and J. Ju, “Borrelidins F–I, cytotoxic and cell migration inhibiting agents from mangrove-derived Streptomyces rochei SCSIO ZJ89,” Bioorg. Med. Chem. 26 (8), 1488–1494 (2018). https://doi.org/10.1016/j.bmc.2018.01.010

    Article  Google Scholar 

  30. I. A. Volynkina, Y. V. Zakalyukina, V. A. Alferova, A. R. Belik, D. K. Yagoda, A. A. Nikandrova, Y. A. Buyuklyan, et al., “Mechanism-based approach to new antibiotic producers screening among Actinomycetes in the course of the citizen science project,” Antibiotics 9 (11), 1198 (2022). https://doi.org/10.20944/preprints202208.0132.v1

    Article  Google Scholar 

  31. M. Yu, Y. Li, S. P. Banakar, L. Liu, C. Shao, Z. Li, and C. Wang, “New metabolites from the co-culture of marine-derived actinomycete Streptomyces rochei MB037 and fungus Rhinocladiella similis 35,” Front. Microbiol. 10, 915 (2019). https://doi.org/10.3389/fmicb.2019.00915

    Article  Google Scholar 

  32. Y. V. Zakalyukina, I. A. Osterman, J. Wolf, M. Neumann-Schaal, I. Nouioui, and M. V. Biryukov, “Amycolatopsis camponoti sp. nov., new tetracenomycin-producing actinomycete isolated from carpenter ant Camponotus vagus,” Antonie van Leeuwenhoek 115 (4), 533–544 (2022). https://doi.org/10.1007/s10482-022-01716-w

    Article  Google Scholar 

  33. Y. V. Zakalyukina, A. R. Zaytsev, and M. V. Biryukov, “Study of cellulose-destroying activity of Actinobacteria associated with ants,” Moscow Univ. Biol. Sci. Bull. (Engl. Transl.) 76 (1), 20–27 (2021). https://doi.org/10.3103/S009639252101006510.3103/S0096392521010065

  34. European Soil Data Centre. https://esdac.jrc.ec.europa.eu/images/Eudasm/Asia/images/maps/download/ IL3002_SO.jpg

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ACKNOWLEDGMENTS

I.G. Shirokikh, A.A. Shirokikh, Ya.I. Nazarova, and N.A. Bokov are grateful to the Rudnitsky Federal Agricultural Research Center for support within the framework of state assignment of no. FNWE-2022-0005.

Yu.V. Zakalyukina thanks the Ministry of Science and Higher Education of the Russian Federation for support within the framework of state assignment no. 075-15-2021-1396.

The study of spore surface ultrastructure of S. rochei 3IZ-6 was carried out in the Laboratory of Electron Microscopy of the Faculty of Biology of the Lomonosov Moscow State University.

Funding

This study was supported by the Russian Science Foundation (project no. 22-24-00278).

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Correspondence to Yu. V. Zakalyukina.

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Translated by D. Konyushkov

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Shirokikh, I.G., Osterman, I.A., Lukianov, D.A. et al. Biocontrol Potential of Novel Borrelidin-Producing Streptomyces rochei 3IZ-6 Isolated from Soil. Eurasian Soil Sc. 56, 619–627 (2023). https://doi.org/10.1134/S1064229323600161

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