Advertisement

Environmental Science and Pollution Research

, Volume 22, Issue 22, pp 18137–18147 | Cite as

Antifungal efficiency of a lipopeptide biosurfactant derived from Bacillus subtilis SPB1 versus the phytopathogenic fungus, Fusarium solani

  • Ines MnifEmail author
  • Ines Hammami
  • Mohamed Ali Triki
  • Manel Cheffi Azabou
  • Semia Ellouze-Chaabouni
  • Dhouha Ghribi
Research Article

Abstract

Bacillus subtilis SPB1 lipopeptides were evaluated as a natural antifungal agent against Fusarium solani infestation. In vitro antifungal assay showed a minimal inhibitory concentration of about 3 mg/ml with a fungicidal mode of action. In fact, treatment of F. solani by SPB1 lipopeptides generated excessive lyses of the mycelium and caused polynucleation and destruction of the related spores together with a total inhibition of spore production. Furthermore, an inhibition of germination potency accompanied with a high spore blowing was observed. Moreover, in order to be applied in agricultural field, in vivo antifungal activity was proved against the dry rot potato tubers caused by F. solani. Preventive treatment appeared as the most promising as after 20 days of fungi inoculation, rot invasion was reduced by almost 78 %, in comparison to that of non-treated one. When treating infected tomato plants, disease symptoms were reduced by almost 100 % when applying the curative method. Results of this study are very promising as it enables the use of the crude lipopeptide preparation of B. subtilis SPB1 as a potent natural fungicide that could effectively control the infection of F. solani in tomato and potato tubers at a concentration similar to the commercial fungicide hymexazol and therefore prevent the damage of olive tree.

Keywords

F. solani SPB1 lipopeptide Antifungal activity Bio-control Potato tuber rot Tomato root rot 

Notes

Acknowledgments

This work has been supported by grants from the Tunisian Ministry of Higher Education, Scientific Research and Technology and the Tunisian Ministry of Agriculture.

References

  1. Al-Reza SM, Rahman A, Ahmed Y, Kang SC (2010) Inhibition of plant pathogens in vitro and in vivo with essential oil and organic extracts of Cestrum nocturnum L. Pestic Biochem Physiol 96:86–92CrossRefGoogle Scholar
  2. Cao Y, Xu Z, Ling N, Yuan Y, Yang X, Chen L, Shen B, Shen Q (2012) Isolation and identification of lipopeptides produced by B. subtilis SQR 9 for suppressing Fusarium wilt of cucumber. Sci Hortic 135:32–39CrossRefGoogle Scholar
  3. Cazorla FM, Romero D, Pérez-Garcia A, Lugtenberg BJJ, de Vicente A, Bloemberg G (2007) Isolation and characterization of antagonistic Bacillus subtilis strains from the avocado rhizoplane displaying biocontrol activity. J Appl Microbiol 103:1950–1959CrossRefGoogle Scholar
  4. Chitarra GS, Breeuwer P, Nout MJR, van Aelst AC, Rombouts FM, Abee T (2003) An antifungal compound produced by Bacillus subtilis YM 10–20 inhibits germination of Penicillium roqueforti conidiospores. J Appl Microbiol 94:159–166CrossRefGoogle Scholar
  5. Daami-Remadi M, Jabnoun-Khiareddine H, Ayed F, Hibar K, Znaidi IEA, El Mahjoub M (2006) In vitro and in vivo evaluation of individually compost fungi for potato Fusarium dry rot biocontrol. J Biol Sci 6(3):572–580CrossRefGoogle Scholar
  6. De Corato U, Viola E, Arcieri G, Valerio V, Cancellara FA, Zimbardi F (2014) Antifungal activity of liquid waste obtained from the detoxification of steam-exploded plant biomass against plant pathogenic fungi. Crop Prot 55:109–118CrossRefGoogle Scholar
  7. des Grades ZE, der Agrarwissenschaften D, Fakultät HL, Wilhelms RF (2012) Biological control of leaf pathogens of tomato plants by Bacillus subtilis (strain FZB24): antagonistic effects and induced plant resistance. Inaugural-Dissertation, Institute of Crop Science and Resource Conservation—Phytomedicine, vorgelegt am 06.06.2012Google Scholar
  8. Ebtsam MM, Abdel-Kawi KA, Khalil MNA (2009) Efficiency of Trichodermaviride and Bacillus subtilis as biocontrol agents against Fusarium solani on tomato plants. Egypt J Phytopathol 37:47–57Google Scholar
  9. El-Kassas HY, Khairy HM (2009) A trial for biological control of a pathogenic fungus (Fusarium solani) by some marine microorganisms. Am Eurasian J Agric Environ Sci 5:434–440CrossRefGoogle Scholar
  10. Ghribi D, Abdelkefi-Mesrati L, Mnif I, Kammoun R, Ayadi I, Saadaoui I, Maktouf S, Chaabouni-Ellouze S (2012) Investigation of antimicrobial activity and statistical optimization of Bacillus subtilis SPB1 biosurfactant production in solid-state fermentation. J Biomed Biotechnol. doi: 10.1155/2012/373682 Google Scholar
  11. Hammami I, Rhouma A, Jaouadi B, Rebai A, Nesme X (2009) Optimization and biochemical characterization of a bacteriocin from a newly isolated Bacillus subtilis strain 14B for biocontrol of Agrobacterium spp. strains. Lett Appl Microbiol 48:253–260CrossRefGoogle Scholar
  12. Hammami I, Triki MA, Rebai A (2011) Purification and characterization of the novel bacteriocin Back IH7 with antifungal and antibacterial properties. J Plant Pathol 93:443–454Google Scholar
  13. Hu LB, Shi ZQ, Zhang T, Yang ZM (2007) Fengycin antibiotics isolated from B-FS01 culture inhibit the growth of Fusarium moniliforme Sheldon ATCC38932. FEMS Microbiol Lett 272:91–98CrossRefGoogle Scholar
  14. Jing L, Yang Q, Zhao L-H, Zhang S-M, Wang Y-X, Zhao X-Y (2009) Purification and characterization of a novel antifungal protein from Bacillus subtilis strain B29. J Zhejiang Univ Sci B 10:264–272CrossRefGoogle Scholar
  15. Kim PI, Bai H, Chae H, Chung S, Kim Y, Park Y, Chi Y-T (2004) Purification and characterization of a lipopeptide produced by Bacillus thuringiensis CMB26. J Appl Microbiol 97:942–949CrossRefGoogle Scholar
  16. Kita N, Ohya T, Uekusa H, Nomura K, Manago M, Shoda M (2005) Biological control of damping-off of tomato seedlings and cucumber Phomopsis root rot by Bacillus subtilis RB14-C. Jpn Agric Res Q 39:109–114Google Scholar
  17. Leclère V, Béchet M, Adam A, Guez J-S, Wathelet B, Ongena M, Thonart P, Gancel F, Chollet-Imbert M, Jacques P (2005) Mycosubtilin overproduction by Bacillus subtilis BBG100 enhances the organism’s antagonistic and biocontrol activities. Appl Environ Microbiol 71:4577–4584CrossRefGoogle Scholar
  18. 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 Biol Technol 48:113–121CrossRefGoogle Scholar
  19. Li L, Ma MC, Huang R, Qu Q, Li GH, Zhou JW, Zhang KQ, Lu KP, Niu XM, Luo J (2012) Induction of chlamydospore formation in Fusarium by cyclic lipopeptide antibiotics from Bacillus subtilis C2. J Chem Ecol 38:966–974CrossRefGoogle Scholar
  20. Lin HF, Chen TH, Liu SD (2010) Bioactivity of antifungal substance iturin A produced by Bacillus subtilis strain BS-99-H against Pestalotiopsis eugeniae, a causal pathogen of wax apple fruit rot. Plant Pathol Bull 19:225–233Google Scholar
  21. Matar SM, El-Kazzaz SA, Wagih EE, Al-Diwany AI, Moustafa HE, Abo-Zaid GA, Abd-Elsalam HE, Hafez EE (2009) Antagonistic and inhibitory effect of Bacillus subtilis against certain plant pathogenic fungi, I. Biotechnology 8:53–61CrossRefGoogle Scholar
  22. Mnif I, Sahnoun R, Ellouze-Chaabouni S, Ghribi D (2013) Evaluation of B. subtilis SPB1 biosurfactants’ potency for diesel-contaminated soil washing: optimization of oil desorption using Taguchi design. Environ Sci Pollut Res. doi: 10.1007/s11356-013-1894-4 Google Scholar
  23. Montealegre JR, Errera R, Velásquez JC, Silva P, Besoaín X, Pérez LM (2005) Biocontrol of root and crown rot in tomatoes under greenhouse conditions using Trichoderma harzianum and Paenibacillus lentimorbus. Additional effect of solarization. Electron J Biotechnol 8:250–257CrossRefGoogle Scholar
  24. Muyolo NG, Lipps PE, Schmitthenner AF (1993) Reactions of dry bean, lima bean, and soybean cultivars to Rhizoctonia root and hypocotyl rot and web blight. Plant Dis 77:234–238CrossRefGoogle Scholar
  25. Nihorimbere V, Ongena M, Cawoy H, Brostaux Y, Kakana P, Jourdan E, Thonart P (2010) Beneficial effects of Bacillus subtilis on field-grown tomato in Burundi: reduction of local Fusarium disease and growth promotion. Afr J Microbiol Res 4:1135–1142Google Scholar
  26. Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125CrossRefGoogle Scholar
  27. Oxenham SK, Svoboda KP, Walters DR (2005) Antifungal activity of the essential oil of basil (Ocimum basilicum). J Phytopathol 153:174–180CrossRefGoogle Scholar
  28. Rebib H, Hedi A, Rousset M, Boudabous A, Limam F, Sadfi-Zouaoui N (2012) Biological control of Fusarium foot rot of wheat using fengycin-producing Bacillus subtilis isolated from salty soil. Afr J Biotechnol 11:8464–8475Google Scholar
  29. Risoen PA, Ronning P, Hegna IK, Kolsto AB (2004) Characterization of a broad range antimicrobial substance from Bacillus cereus. J Appl Microbiol 96:648–655CrossRefGoogle Scholar
  30. Ruangwong OU, Chang C-I, Lamine SA, Liang W-J (2012) Identification of antifungal compound produced by Bacillus subtilisLB5 with ability to control anthracnose disease caused by Colletotrichum gloeosporioides. Afr J Microbiol Res 6:3732–3738Google Scholar
  31. Senthilkumar M, Swarnalakshmi K, Govindasamy V, Lee YK, Annapurna K (2009) Biocontrol potential of soybean bacterial endophytes against charcoal rot fungus, Rhizoctonia bataticola. Curr Microbiol 58:288–293CrossRefGoogle Scholar
  32. Soothill JS, Ward R, Girling AJ (1992) The IC50: an exactly defined measure of antibiotic sensitivity. J Antimicrob Chemother 29:137–139CrossRefGoogle Scholar
  33. Soylu EM, Kurt S, Soylu S (2010) In vitro and in vivo antifungal activities of the essential oils of various plants against tomato grey mould disease agent Botrytis cinerea. Int J Food Microbiol 143:183–189CrossRefGoogle Scholar
  34. Tawara S, Ikeda F, Maki K, Morishita Y, Otomo K, Teratani N, Goto T, Tomishima M, Ohki H, Yamada A, Kawabata K, Takasugi H, Sakane K, Tanaka H, Matsumoto F, Kuwahara S (2000) In vitro activities of a new lipopeptide antifungal agent, FK463, against a variety of clinically important fungi. Antimicrob Agents Chemother 44:57–62CrossRefGoogle Scholar
  35. Triki MA, Hammami I, KridHadj-Taieb S, Daami-Remadi M, Mseddi A, El Mahjoub M, Gdoura R, Khammasy N (2012) Biological control of atypical pink rot disease of potato in Tunisia. Glob Sci Books Pest Tech 6:60–64Google Scholar
  36. Wang J, Xia XM, Wang HY, Li PP, Wang KY (2013) Inhibitory effect of lactoferrin against gray mould on tomato plants caused by Botrytis cinerea and possible mechanisms of action. Int J Food Microbiol 161:151–157CrossRefGoogle Scholar
  37. Yangui T, Sayadi S, Dhouib A (2013) Sensitivity of Pectobacteriu mcarotovorum to hydroxytyrosol-rich extracts and their effect on the development of soft rot in potato tubers during storage. Crop Prot 53:52–57CrossRefGoogle Scholar
  38. Yun-feng Y, Qi-qin L, Gang F, Gao-qing Y, Jian-hua M, Wei L (2012) Identification of antifungal substance (Iturin A2) produced by Bacillus subtilis B47 and its effect on southern corn leaf blight. J Integ Agric 11:90–99CrossRefGoogle Scholar
  39. Zhang Y-L, Li S, Jiang D-H, Kong L-C, Zhang P-H, Xu J-D (2013) Antifungal activities of metabolites produced by a termite associated Streptomyces canus BYB02. J Agric Food Chem 61:1521–1524CrossRefGoogle Scholar
  40. Zu W, Yu H, Liang L, Fu Y, Efferth T, Liu X, Wu N (2010) Activities of ten essential oils towards Propionibacterium acnes and PC-3, A-549 and MCF-7 cancer cells. Molecules 15:3200–3210CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Ines Mnif
    • 1
    • 2
    Email author
  • Ines Hammami
    • 3
  • Mohamed Ali Triki
    • 4
  • Manel Cheffi Azabou
    • 4
  • Semia Ellouze-Chaabouni
    • 1
  • Dhouha Ghribi
    • 1
    • 2
  1. 1.Unit “Enzymes and Bioconversion”, National School of Engineers of SfaxUniversity of SfaxSfaxTunisia
  2. 2.Higher Institute of Biotechnology of SfaxUniversity of SfaxSfaxTunisia
  3. 3.Higher School of Agriculture of KefKefTunisia
  4. 4.Laboratory “Amélioration et Protection des Ressources Génétiques de l’Olivier”, Sfax BP1087Institut of Olivier, IRESA - University of SfaxSfaxTunisia

Personalised recommendations