Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2018, Vol. 53, ¹ 1, p. 29-37.
(how to cite this article)

doi: 10.15389/agrobiology.2018.1.29eng

UDC 632.937.15:579.64

 

BIOLOGICALLY ACTIVE METABOLITES OF Bacillus subtilis AND THEIR
ROLE IN THE CONTROL OF PHYTOPATHOGENIC MICROORGANISMS
(review)

Ò.Ì. Sidorova, À.Ì. Asaturova, A.I. Homyak

All-Russian Research Institute of Biological Plant Protection, Federal Agency for Scientific Organizations, 39, Krasnodar, 350039 Russia, e-mail 0166505@mail.ru (✉ corresponding author), biocontrol-vniibzr@yandex.ru, HomyakAI87@mail.ru

ORCID:
Sidorova Ò.Ì. orcid.org/0000-0003-4281-5278
Asaturova À.Ì. orcid.org/0000-0002-0060-1995
Homyak A.I. orcid.org/0000-0001-9360-2323

Received January 30, 2017

 

The use of nonpathogenic soil bacteria living in association with the roots of higher plants enhances the adaptive potential of the hosts, stimulates their growth and serves as a promising alternative to chemical pesticides (V.K. Chebotar’ et al., 2015). The bacterium Bacillus subtilis is recognized as a powerful biocontrol tool because of suppression of a wide range of phytopathogens due to the ability to produce a variety of secondary metabolites of different chemical nature, e.g. cyclic lipopeptides, polypeptides, proteins and nonpeptidic compounds (T. Stein, 2005). Information on the structure of bioactive metabolites of bacterial antagonists of phytopathogens, as well as mechanisms of their biological activity promotes targeted selection of strains for the development of microbiological products. B. subtilis is widely distributed due to the ability to form biofilms (A.L. McLoon et al., 2011). The chemical composition of compounds produced by the bacteria is determined by genetic characteristics and physical and chemical conditions of the environment. The cyclic lipopeptide surfactin exhibits antimicrobial (antibacterial, antiviral, antifungal) activity, causing lysis of the cell, and also contributes to a decrease in the production of mycotoxins by microorganisms (M. Mohammadipour et al., 2009). The structure of another peptide metabolite, rizocticin, promotes penetration into the microbial cell and inhibition of protein synthesis (K. Kino et al., 2009). B. subtilis can produce various hydrolytic enzymes which lyse the phytopathogenic fungus cell wall (C.P. Quardros et al., 2011). Among the metabolites synthesized by bacteria, lantibiotics play important role, their structure allows the synthesis of peptidoglycan which contributes to the formation of pores in cytoplasmic membrane (J. Parisot et al., 2008). A large family of polyketones exhibits antimicrobial activity due to the ability to collect multifunctional polypeptides into large pesticide complexes. The phospholipid antibiotic bacilizycin, which is produced immediately after the growth ceases and before the formation of thermostable spores, exhibits fungicidal activity against some fungi (A. Hamdache et al., 2011). Some strains of B. subtilis synthesize polyene antibiotics with conjugated double bonds, for example, hexaenes which inhibit growth of phytopathogenic fungi (E.B. Kudryashova et al., 2005). Several soil microorganisms, including strains of B. subtilis, can synthesize gibberellins and gibberellin-like substances that stimulate plant growth (R. Aloni et al., 2006). Proteins, lipopeptides, polysaccharides and other compounds associated with the B. subtilis cell wall can trigger the protective mechanism of the plant, that is, act as elicitors (M. Ongena et al., 2007). Thus, research aimed at studying biologically active metabolites of B. subtilis, which possess the properties of biopesticides or inducers of plant resistance to diseases, opens new prospects for the development of environmentally friendly technologies for protection against phytopathogens.

Keywords: biological control, Bacillus subtilis, metabolites, antimicrobial activity, biopreparation, phytopathogens, system resistance.

 

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REFERENCES

  1. Chebotar’ V.K., Shcherbakov A.V., Shcherbakova E.N., Maslennikova S.N., Zaplatkin A.N., Mal’fanova N.V. Biodiversity of endophytic bacteria as a promising biotechnological resource. Agricultural Biology, 2015, 50(5): 648-654 CrossRef
  2. Olfa K.-F., Saoussen B.K., Mouna D., Amel K., Hayfa J.-K., Majda D.-R., Slim T. Improvement of antifungal metabolites production by Bacillus subtilis V 26 for biocontrol of tomato postharvest disease. Biol. Control, 2016, 95: 73-82 CrossRef
  3. Mnif I., Ghribi D. Review lipopeptides biosurfactants: mean classes and new insights for industrial, biomedical and environmental applications. Biopolymers, 2015, 104(3): 129-147 CrossRef
  4. Lirong Y., Quana X., Xuea B., Goodwinb P.H., Lua S., Wanga J., Dua W., Wua C. Isolation and identification of Bacillus subtilis strain YB-05 and its antifungal substances showing antagonism against Gaeumannomyces graminis var. tritici. Biol. Control, 2015, 85: 52-58 CrossRef
  5. Ines M., Dhouha G. Lipopeptide surfactants: production, recovery and pore forming capacity. Peptides, 2015, 71: 100-112 CrossRef
  6. Boronin A.M. Sorosovskii obrazovatel'nyi zhurnal, 1998, 10: 25-31 (in Russ.).
  7. Ongena M., Jacques P., Touré Y., Destain J., Jabrane A., Thonart P. Involvement of fengycin-type lipopeptides in the multifaceted biocontrol potential of Bacillus subtilis. Appl. Microbiol. Biot., 2005, 69: 29-38 CrossRef
  8. Timmusk S. Grantcharova N., Wagner E.G. Paenibacillus polymyxa invades plant roots and forms biofilms. Appl. Environ. Microb., 2005, 71: 7292-7300 CrossRef
  9. Sidorova T.M., Sidorov I.A. MaterialyVMezhdunarodnoinauchno-prakticheskoikonferentsii «Agrotekhnicheskiimetodzashchityrasteniiotvrednykhorganizmov» [Proc. V Int. Conf. on agrotechnologies for crop protection against pests]. Krasnodar, 2011: 335-337 (in Russ.).
  10. Asaturova A.M., Sidorova T.M., Sidorov I.A., Dubyaga V.M., Tomashevich N.S., Zharnikova M.D., Zhevnova N.A., Khomyak A.I. Materialy Mezhdunarodnoi nauchno-prakticheskoi konferentsii «Biologicheskaya zashchita rastenii — osnova stabilizatsii agroekosistem» [Proc. Int. Conf. «BioMethods in plant protection for sustainable agroecocoenoses. Iss. 7].Krasnodar, 2012, vypusk 7: 167-169 (in Russ.).
  11. Ongena M., Duby F., Jourdan E., Beandry T., Jadin V., Dommes J., Thonart P. Bacillus subtilis M4 decreases plant susceptibility towards fungal pathogens by increasing host resistance associated with differential gene expression. Appl. Microbiol. Biot., 2005, 67: 692-698 CrossRef
  12. Khomyak A. I., Asaturova A. M., Sidorova T. M. Materialy II nauchno-prakticheskoi konferentsii studentov, aspirantov i molodykh uchenykh «Sovremennye aspekty proizvodstva i pererabotki sel'skokhozyaistvennoi produktsii» [Proc. II Conf. of students, graduate students and young scientists «Food stuffs — modern aspects of production and processing]. Krasnodar, 2016: 216-224 (in Russ.).
  13. Stein T. Bacillus subtilis antibiotics: structures, syntheses and specific functions. Micro Review. Mol. Microbiol., 2005, 56(4): 845-857 CrossRef
  14. Wang T., Liang Y., Wu M., Chen Z., Lin J., Yang L. Natural products from Bacillus subtilis with antimicrobial properties. Chinese J. Chem. Eng., 2015, 23(4): 744-754 CrossRef
  15. Jacques P. Surfactin and other lipopeptides from Bacillus spp. In: Biosurfactants. Microbiology monographs. G. Soberón-Chávez (ed.). Springer, Berlin, Heidelberg, 2011, V. 20 CrossRef
  16. Nagorska K., Bikowski M., Obuchowski M. Multicellular behavior and production of a wide variety of toxic substances support usage of Bacillus subtilis as a powerful biocontrol agent. Acta Biochim. Pol., 2007, 54(3): 495-508.
  17. Lopez D., Fischbach M.A., Chu F., Losick R., Kolter R. Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis. PNAS USA, 2009, 106: 280-285 CrossRef
  18. Fickers P., Guez L.-S., Damblon C., Leclérel V., Béchet M., Jacques P., Joris B. High-level biosynthesis of the anteiso-C17 isoform of the antibiotic mycosubtilin in Bacillus subtilis and characterization of its candidacidal activity. Appl. Environ. Microb., 2009, 12: 4636-4640 CrossRef
  19. Farace G., Fernandez O., Jacquens L., Coutte F., Krier F., Jacques Ph., Clément Ch., Barka E.A., Jacquard C., Dorey S. Cyclic lipopeptides from Bacillus subtilis activate distinct patterns of defense responses in grapevine. Mol. Plant Pathol., 2015, 16(2): 177-187 CrossRef
  20. Kino K., Kotanaka Y., Arai T., Yagasaki M. A novel L-amino acid ligase from Bacillus subtilis NBRC3134, a microorganism producing peptide — antibiotic rhizocticin. Biosci. Biotech. Bioch., 2009, 73(4): 901-907 CrossRef
  21. Sharma A. Rhamnolipid producing PGPR and their role in damping off disease suppression. In: Plant bacteria interactions strategies and techniques to promote plant growth. I. Ahmad, J. Pichtel, S. Haya (eds.). Wiley VCH Publications, Weinheim, 2008.
  22. Jourdan E., Henry G., Duby F., Dommes J., Barthélemy J.P., Thonart P., Ongena M. Insights into the defense-related events occurring in plant cells following perception of surfactin-type lipopeptide from Bacillus subtilis. Mol. Plant Microbe In., 2009, 22: 456-468 CrossRef
  23. Korenblum E., de Araujo L.V., Guimarâes C.R., de Sourza L.M., Sassaki G., Abreu F., Nitschke M., Lins U., Guimarâes-Freire D.M., Barreto-Bergter E., Seldin L. Purification and characterization of a surfactin-like molecule produced by Bacillus sp. H2O-1 and its antagonistic effect against sulfate reducing bacteria. BMC Microbiol., 2012, 12(252): 1-13 CrossRef
  24. McLoon A.L., Guttenplan S.B., Kearns D.B., Kolter R., Losick R. Tracing the domestication of a biofilmforming bacterium. J. Bacteriol., 2011, 193: 2027-2034 CrossRef
  25. Chu F., Kearns D.B., McLoon A., Chai Y., Kolter R., Losick R. A novel regulatory protein governing biofilm formation in Bacillus subtilis. Mol. Microbiol., 2008, 68(5): 1117-1127 CrossRef
  26. Chen Y., Yan F., Chai Y., Liu H., Kolter R., Losick R., Guo J. Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environ. Microbiol., 2013, 15(3): 848-864 CrossRef
  27. Earl A.M., Losick R., Kolter R. Ecology and genomics of Bacillus subtilis. Trends Microbiol., 2008, 16: 269-275 CrossRef
  28. Branda S.S., Chu F., Kearns D.B., Losick R., Kolter R. A major protein component of the Bacillus subtilis biofilm matrix. Mol. Microbiol., 2005, 59: 1229-1238 CrossRef
  29. Epstein A.K., Pokroy B., Seminara A., Aizenberg J. Bacterial biofilm shows persisten resistance to liquid wetting and gas penetration. PNAS USA, 2011, 108: 995-1000 CrossRef
  30. Kovács A.T., van Gestel J., Kuipers O.P. The protective layer of biofilm: a repellent function for a new class of amphiphitic proteins. Mol. Microbiol, 2012, 85(1): 8-11 CrossRef
  31. Abdel-Mawgoud A.M., Aboulwafa M.M., Hassouna N.A.-H. Characterization of surfactin produced by Bacillus subtilis isolates BS5. Appl. Biochem. Biotech., 2008, 150(3): 289-303 CrossRef
  32. Leclére V., Béchet M., Adam A., Guez J.-S., Wathelet B., Ongena M., Thonart P., Gancel F., Chollet-Imbert M., Jacques P. Mycosubtilin overproduction by Bacillus subtilis BBG100 enhances the organism’s antagonistic and biocontrol activities mycosubtilin. Appl. Environ. Microb., 2005, 71(8): 4577-4584 CrossRef
  33. Fernandes P.A.V., Arruda I.R., Santos A.F.B., Araujo A.A., Major A.M.S., Ximenes E.A. Antimicrobial activity of surfactants produces by Bacillus subtilis R14 against multidrug-resistant bacteria. Braz. J. Microbiol., 2007, 38: 704-709 CrossRef
  34. Shoeb E., Akhlag F., Badar U., Akhter J., Imtiaz S. Classification and industrial applications of biosurfactants. Academic Research International, 2013, 4(3): 243-252.
  35. Debois D., Fernandez O., Franzil L., Jourdan E., de Brogniez A., Willems L., Clément C., Dorey S., De Pauw E., Ongena M. Plant polysaccharides initiate underground crosstalk with bacilli by inducing synthesis of the immunogenic lipopeptide surfactin. FEMS Microbiol. Rev., 2015, 10: 1758-2229 CrossRef
  36. Cawoy H., Mariutto M., Henry G., Fisher C., Vasilyeva N., Thonart P., Dommes J., Ongena M. Plant defense stimulation by natural isolates of Bacillus depends on efficient surfactin production. Mol. Plant Microbe In., 2014, 27: 87-100 CrossRef
  37. Mohammadipour M., Mousivand M., Jouzani G.S., Abbasalizadeh S. Molecular and biochemical characterization of Iranian surfactin-producing Bacillus subtilis isolates and evaluation of their biocontrol potential against Aspergillus flavus and Colletotrichum gloeosporioides. Can. J. Microbiol., 2009, 55: 395-404 CrossRef
  38. Li J., Yang Q., Zhao L., Zhang S., Wang Y., Zhao X. Purification and characterization of a novel antifungal protein from Bacillus subtilis strain B29. J. Zhejiang Univ.-Sc. B, 2009, 10(4): 264-272 CrossRef
  39. López D., Vlamakis H., Losick R., Kolter R. Cannibalism enhances biofilm development in Bacillus subtilis. Mol. Microbiol., 2009, 74: 609-618 CrossRef
  40. Zhong J., Zhang X., Ren Y., Yang J., Tan H., Zhou J. Optimization of Bacillus subtilis cell growth effecting jiean-peptide production in fed batch fermentation using central composite design. Electron. J. Biotechn., 2014, 17: 132-136 CrossRef
  41. Zhang X., Zhou J., Fu W., Li Z., Zhong J., Yang J., Xiao L., Tan H. Response surface methodology used for statistical optimization of jiean-peptide production by Bacillus subtilis. Electron. J. Biotechn., 2010, 15: 0717-3458 CrossRef
  42. Meena K.R., Kanwar S.S. Lipopeptides as the antifungal and antibacterial agents: applications in food safety and therapeutics. BioMed Res. Int., 2014, 2015: 9 CrossRef
  43. Willey J.M., van der Donk W.A. Lantibiotics: peptides of diverse structure and function. Annu. Rev. Microbiol., 2007, 61: 477-501 CrossRef
  44. Hu L.B., Shi Z.Q., Zhang T., Yang Z.M. Fengycin antibiotics isolated from B-FS 01 culture inhibit the growth of Fusarium moniliforme Sheldon ATCC38932. FEMS Microbiol. Lett., 2007, 272: 91-98 CrossRef
  45. Sachdev D.P., Cameota S.S. Biosurfactants in agriculture. Appl. Microbiol. Biot., 2013, 97: 1005-1016 https://doi.org/10.1007/s00253-012-4641-8).
  46. Choudhary D.K., Johri B.N. Interactions of Bacillus spp. and plants — with special reference to induced systemic resistance (ISR). Microbiol. Res., 2008, 164: 493-513 CrossRef
  47. Degering C., Eggert T., Puls M., Bongaerts J., Evers S., Maurer K.-H., Jaeger K. Optimization of protease secretion in Bacillus subtilis and Bacillus licheniformis by screening of homologous and heterologous signal peptides. Appl. Environ. Microb., 2010, 76: 6370-6376 CrossRef
  48. Borisova S.A., Circello B.T., Zhang J.K., van der Donk W.A., Metcalf W.W. Biosynthesis of rhizocticins, antifungal phosphonate oligopeptides produced by Bacillus subtilis ATCC6633. Chemistry Biology, 2010, 17: 28-37 CrossRef
  49. Parisot J., Carey S., Breukink E., Chan W.C., Narbad A. Molecular mechanism of target recognition by subtilin, a class I lanthionine antibiotic. Antimicrob. Agents Chemother., 2008, 52: 612-618 CrossRef
  50. Al-Bahry S.N., Al-Wahaibi Y.M., Elshafie A.E., Al-Bemani A.S., Joshi S.J., Al-Makhmari H.S., Al-Sulaimani H.S. Biosurfactant production by Bacillus subtilis B20 using date molasses and its possible application in enhanced oil recovery. Int. Biodeter. Biodegr., 2013, 81: 141-146 CrossRef
  51. Fickers P. Antibiotic compounds from so Bacillus: why are they amazing? American Journal of Biochemistry and Biotechnology, 2012, 8(1): 38-43 CrossRef
  52. Chebotar’ V.K., Makarova N.M., Shaposhnikov A.I., Kravchenko L.V. Antifungal and phytostimulating characteristics of Bacillus subtilis Ch-13 rhizospheric strain, producer biopreparations. Appl. Biochem. Microbiol., 2009, 45(4): 419-423 CrossRef
  53. van Loon L.C. Plant responses to plant growth promoting rhizobacteria. Eur. J. Plant Pathol., 2007, 119: 243-254 CrossRef
  54. Quardros C.P., Teixeira Duarte M.C., Pastore G.M. Biological activities of a mixture of biosurfactant from Bacillus subtilis and alkaline lipase from Fusarium oxysporum. Braz. J. Microbiol., 2011, 42: 354-361 CrossRef
  55. Kino K., Kotanaka Y., Arai T., Yagasaki M. A novel L-amino acid ligase from Bacillus subtilis NBRC3134, a microorganism producing peptide-antibiotic rhizocticin. Biosci. Biotech. Bioch., 2009, 73(4): 901-907 CrossRef
  56. Deleu M., Paquot M., Nylander T. Fengycin interaction with lipid monolayers at the air-aqueous interface — implications for the effect of fengycin on biological membranes. J. Colloid Interf. Sci., 2005, 283: 358-365 CrossRef
  57. Linares J.F., Gustafsson I., Baquero F., Martinez J.L. Antibiotics as intermicrobial signaling agents instead of weapons. PNAS USA, 2006, 103: 19484-19489 CrossRef
  58. Hamdache A., Lamarti A., Aleu J., Collado I.G. Non-peptide metabolites from the genus Bacillus. J. Nat. Prod., 2011, 74(4): 893-899 CrossRef
  59. Alaa R.K., alden Sanaa B. Antimicrobial effect of phospholipid produced from Bacillus subtilis. World Journal of Experimental Biosciences, 2014, 2(2): 59-63.
  60. Kudryashova E.B., Vinokurova N.G., Ariskina E.V. Bacillus subtilis and phenotypically similar strains producing hexaene antibiotics. Appl. Biochem. Microbiol., 2005, 41(5): 486-489 CrossRef
  61. Aloni R., Aloni E., Langhans M., Ullrich C.I. Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Annals of Botany, 2006, 97: 883-893 CrossRef
  62. Yarullina L.G., Kasimova R.I., Ibragimov R.I., Akhatova A.R., Umarov I.A., Maksimov I.V. Qualitative and quantitative changes of potato tuber proteome under the influence of signal molecules and infection with Phytophthora infestans. Appl. Biochem. Microbiol., 2016, 52(1): 71-78 CrossRef
  63. Vandeputte O., Öden S., Mol A., Vereecke D., Goethals K., El Jaziri M., Prinsen E. Biosynthesis of auxin by the Gram-positive phytopathogen Rhodococcus faseians is controlled by compounds specific to infected plant tissues. Appl. Environ. Microb., 2005, 71(3): 1169-1177 CrossRef
  64. Gordillo A., Maldonado M.C. Purification of peptides from Bacillus strains with biological activity. Chromatography and Its Applications, 2012, 11: 201-225.
  65. Dyakov Yu.T., Ozeretskovskaya O.L. Vertical pathosystem: Resistance genes and their products. Immune response. In: Comprehensive and molecular phytopathology. Yu.T. Dyakov, V.G. Dzhavakhiya, T. Korpela (eds.). Elsevier, Amsterdam, 2007: 181-215 CrossRef
  66. Ongena M., Jourdan E., Adam A., Paquot M., Brans A., Joris B., Arpigny J.L., Thonart P. Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ. Microbiol., 2007, 9: 1084-1090 CrossRef
  67. Jordan E., Henry G., Duby F., Dommes J., Barthélemy J.P., Thonart P., Ongena M. Insights into defense-related events occurring in plant cells following perception of surfactin-type lipopeptide from Bacillus subtilis. Mol. Plant Microbe In., 2009, 22: 456-468 CrossRef

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