Abstract
Banana production has been severely hindered by the long-term practice of monoculture agriculture. Fusarium wilt, caused by the Fusarium oxysporum f. sp. cubense (FOC), is one of the most destructive diseases that can afflict banana plants. It is both necessary and urgent to find an efficient method for protecting banana production worldwide. In this study, 57 antagonistic bacterial strains were isolated from the rhizospheres of healthy banana plants grown in a heavily wilt-diseased field; of the 57 strains, six strains with the best survival abilities were chosen for further study. Compared with the control and the other strains in the greenhouse experiment, W19 strain was found to observably decrease the incidence of Fusarium wilt and promote the growth of banana plants when combined with the organic fertilizer (OF). This strain was identified as Bacillus amyloliquefaciens based on its morphological, physiological, and biochemical properties, as well as 16S rRNA analysis. Two kinds of antifungal lipopeptides (iturin and bacillomycin D) produced by W19 strain were detected and identified using HPLC–ESI-MS. Another lipopeptide, called surfactin, was also produced by the thick biological film forming W19 strain. In addition to lipopeptides, 18 volatile antifungal compounds with significant antagonistic effect against F. oxysporum were detected and identified using gas chromatography–mass spectrometer (GC–MS). The work described herein not only highlights how the bioorganic fertilizer with B. amyloliquefaciens can be used to control Fusarium wilt of banana but also examines some of the potential mechanisms involved in the biocontrol of Fusarium wilt.
Similar content being viewed by others
References
Alabouvette C, Lemanceau P, Steinberg C (1993) Recent advances in the biological control of Fusarium wilts. Pestic Sci 37:365–373
Alef K, Nannipleri P (eds) (1995) Methods in applied soil microbiology and biochemistry. Academic, San Diego
Arguelles-Arias A, Brans A, Joris B, Fickers P (2009) Bacillus amyloliquefaciens GA1 as a source of potent antibiotics and other secondary metabolites for biocontrol of plant pathogens. Microb Cell Fact 8:1–12
Armstrong GM, Armstrong JK (1981) Formae speciales and races of Fusarium oxysporum causing wilt disease. In: Nelson PE, Toussoun TA, Cook RJ (eds) Fusarium: disease, biology, and taxonomy. Pennsylvania State University Press, University Park, pp 391–399
Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134:307–319
Besson F, Delcambe L (1978) Identification of antibiotics of iturin group various strains of Bacillus subtilis. J Antibiot 31:284–288
Borrero C, Trillas MI, Ordovas J, Tello JC, Aviles M (2004) Predictive factors for the suppression of Fusarium wilt of tomato in plant growth media. Phytopathology 94:1094–1101
Borrero C, Ordovas J, Trillas MI, Aviles M (2006) Tomato Fusarium wilt suppressiveness. The relationship between the organic plant growth media and their microbial communities as characterized by Biology. Soil Biol Biochem 38:1631–1637
Boulter JI, Trevors JT, Boland GJ (2002) Microbial studies of compost: bacterial identification, and their potential for turfgrass pathogen suppression. World J Microb Biot 18:661–671
Brooks DS, Gonzalez CF, Appel DN, Filer TH (1994) Evaluation of endophytic bacteria as potential biological control agents for oak wilt. Biol Control 4:373–381
Bruce A, Wheatley RE, Humphris SN, Hackett CA, Florence M (2000) Production of volatile organic compounds by Trichoderma spp. in media containing different amino acids and their effect on selected wood decay fungi. Holzforschung 54:481–486
Cao Y, Zhang ZH, Ling N, Yuan YJ, Zheng XY, Shen B, Shen QR (2011) Bacillus subtilis SQR 9 can control Fusarium wilt in cucumber by colonizing plant roots. Biol Fertil Soils 47:495–506
Cavaglieri L, Orlando J, Rodriguez MI (2005) Biocontrol of Bacillus subtilis against Fusarium verticillioides in vitro and at the maize root level. Res Microbiol 156:748–754
Cesco S, Mimmo T, Tonon G, Tomasi N, Pinton R, Terzano R, Neumann G, Weisskopf L, Renella G, Landi L, Nannipieri P (2012) Plant-borne flavonoids released into the rhizosphere: impact on soil bio-activities related to plant nutrition. A review. Biol Fertil Soils 48:123–149
Chaurasia B, Pandey A, Palni LMS, Trivedi P, Kumar B, Colvin N (2005) Diffusible and volatile compounds produced by an antagonistic Bacillus subtilis strain cause structural deformations in pathogenic fungi in vitro. Microbiol Res 160:75–81
Chen XH, Koumoutsi A, Scholz R, Eisenreich A, Gottschalk G, Borriss R (2007) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotechnol 25:1007–1014
Chen H, Xiao X, Wang J, Wu L, Zheng Z, Yu Z (2008) Antagonistic effects of volatiles generated by Bacillus subtilis on spore germination and hyphal growth of the plant pathogen, Botrytis cinerea. Biotechnol Lett 30:919–923
Duffy BK, Weller DM (1996) Biological control of take-all of wheat in the Pacific Northwest of the USA using hypovirulent Gaeumannomyces graminis var. tritici, fluorescent Pseudomonads. J Phytopathol 144:11–12
Dufour S, Deleu M, Nott K, Wathelet B, Thonart P, Paquo M (2005) Hemolytic activity of new linear surfactin analogs in relation to their physico-chemical properties. Biochim Biophys Acta 1726:87–95
El-Hassan SA, Gowen SR (2006) Formulation and delivery of the bacterial antagonist Bacillus subtilis for management of lentil vascular wilt caused by Fusarium oxysporum f. sp. lentis. Phytopathology 154:148–155
Fiddaman DJ, Rossall S (1994) Effect of substrate on the production of antifungal volatiles from Bacillus subtilis. Appl Bacteriol 76:396–405
Fuchs JG, Moenne-Loccoz Y, Defago G (1999) Ability of nonpathogenic Fusarium oxysporum Fo47 to protect tomato against Fusarium wilt. Biol Control 14:105–110
Getha K, Vikineswary S, Wong WH, Seki T, Ward A, Goodfellow M (2005) Evaluation of Streptomyces sp. strain g10 for suppression of Fusarium wilt, rhizosphere colonization in pot-grown banana plantlet. J Ind Microbiol Biotechnol 32:24–32
Gong M, Wang JD, Zhang J, Yang H, Lu XF, Pei Y, Cheng JQ (2006) Study of the antifungal ability of Bacillus subtilis strain PY-1 in vitro and identification of its antifungal substance (iturin A). Acta Biochim Biophys Sin 38:233–240
Hamon MA, Lazazzera BA (2001) The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol Microbiol 42:1199–1209
Hervás A, Linda B, Datnoff LE, Jiménez-Díaz RM (1998) Effect of commercial and indigenous microorganisms on Fusarium wilt development in chickpea. Biol Control 13:166–176
Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST (1994) Bergry’s manual of determinative bacteriology, 9th edn. Williams & Wilkins, Baltimore
Insam H, Seewald MSA (2010) Volatile organic compounds (VOCs) in soils. Biol Fertil Soils 46:199–214
Ji XL, Lu GB, Gai YP, Zheng CC, Mu ZM (2008) Biological control against bacterial wilt and colonization of mulberry by an endophytic Bacillus subtilis strain. FEMS Microbiol Ecol 65:565–573
Jourdan E, Henry G, Duby F, Dommes J, Barthelemy JP, Thonart P, Ongena M (2009) Insights into the defense-related events occurring in plant cells following perception of surfactin-type lipopeptides from Bacillus subtilis. Mol Plant Microbe In 22:456–468
Kinsinger R, Shirk M, Fall R (2003) Rapid surface motility in Bacillus subtilis is dependent on extracellular surfactin and potassium ion. J Bacteriol 185:5627–5631
Komada H (1975) Development of a selective medium for quantitative isolation of Fusarium oxysporum from natural soil. Rev Plant Protect Res 8:114–125
Leclère V, Béchet M, Adam A, Guez JS, 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 Microb 71:4577–4584
Leclère V, Marti R, Béchet M, Fickers Jacques P (2006) The lipopeptides mycosubtilin and surfactin enhance spreading of Bacillus subtilis strains by their surface-active properties. Arch Microbiol 186:6475–6483
Lin YH, Chang JY, Liu ET, Chao CP, Huang JW, Fang P, Chang LD (2009) Development of a molecular marker for specific detection of Fusarium oxysporum f. sp. cubense race 4. Eur J Plant Pathol 123:353–365
Ling N, Xue C, Huang QW, Yang XM, Xu YC, Shen QR (2010) Development of a mode of application of bioorganic fertilizer for improving the biocontrol efficacy to Fusarium wilt. BioControl 55:673–683
McKee N, Robinson PM (1988) Production of volatile inhibitors of germination and hyphal extension by Geotrichum candidum. Trans Br Mycol Soc 91:157–190
Minerdi D, Bossi S, Gullino ML, Garibaldi A (2009) Volatile organic compounds: a potential direct long-distance mechanism for antagonistic action of Fusarium oxysporum strain MSA 35. Environ Microbiol 11:844–854
Minuto A, Spadaro D, Garibaldi A, Gullino LM (2006) Control of soilborne pathogens of tomato using a commercial formulation of Streptomyces griseoviridis and solarization. Crop Prot 25:468–475
Molina MA, Ramos JL, Espinosa-Urgel M (2003) Plant-associated biofilms. Rev Environ Sci Biotechnol 2:99–108
Moyne AL, Shelby R, Cleveland TE, Tuzun S (2001) Bacillomycin D: an iturin with antifungal activity against Aspergillus flavus. J Appl Microbiol 90:622–629
Nemec S, Datnofft LE, Strandberg J (1996) Efficacy of biocontrol agents in planting mixes to colonize plant roots and control root diseases of vegetables and citrus. Crop Prot 15:735–742
O’Donnell K, Kistler HC, Cigelnik E, Ploetz RC (1998) Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear, mitochondrial gene genealogies. P Natl Acad Sci 95:2044–2049
Ongena M, Jacques P (2007) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125
O’Toole GA, Pratt LA, Watnick PI, Newman DK, Weaver VB, Kolter R (1999) Genetic approaches to study of biofilms. Methods Enzymol 310:91–109
Patel A, Deshattiwar M, Chaudhari B, Chincholkar S (2009) Production, purification and chemical characterization of the catecholate siderophore from potent probiotic strains of Bacillus spp. Bioresour Technol 100:368–373
Pereira P, Nesci A, Etcheverry MG (2009) Efficacy of bacterial seed treatments for the control of Fusarium verticillioides in maize. BioControl 54:103–111
Ren XL, Zhang N, Cao MH, Wu K, Shen QR, Huang QW (2012) Biological control of tobacco black shank and colonization of tobacco roots by a Paenibacillus polymyxa strain C5. Biol Fertil Soils. doi:10.1007/s00374-011-0651-4
Romano A, Vitullo D, Pietro AD, Lima G, Lanzotti V (2011) Antifungal lipopeptides from Bacillus amyloliquefaciens strain BO7. J Nat Prod 74:145–151
Romero D, Pérez-García A, Rivera ME, Cazorla FM, de Vicente A (2004) Isolation and evaluation of antagonistic bacteria towards the cucurbit powdery mildew fungus Podosphaera fusca. Appl Microbiol Biotechnol 64:263–269
Saravanan T, Muthusamy M, Marimuthu T (2003) Development of integrated approach to manage the fusarial wilt of banana. Crop Prot 22:1117–1123
Sartori M, Nesci A, Etcheverry M (2012) Production of Fusarium verticillioides biocontrol agents, Bacillus amyloliquefaciens and Microbacterium oleovorans, using different growth media: evaluation of biomass and viability after freeze-drying. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 29:287–292
Smyth TJP, Perfumo A, McClean S, Marchant R, Banat IM (2010) Isolation and analysis of lipopeptides and high molecular weight biosurfactants. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 3689–3704
Snyder W, Hanson H (1940) The species concept in Fusarium. Am J Bot 27:64–67
Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56:845–857
Strobel GA, Dirkse E, Sears J, Markworth C (2001) Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiology 147:2943–2950
Sun JB, Peng M, Wang YG, Zhao PJ, Xia QY (2010) Isolation and characterization of antagonistic bacteria against Fusarium wilt and induction of defense related enzymes in banana. Afr J Microbiol Res 5:509–515
Trevors JT (1996) Sterilization and inhibition of microbial activity in soil. J Microbiol Meth 26:53–59
Turner JT, Backman PA (1991) Factors relating to peanut yield increases after seed treatment with Bacillus subtilis. Plant Dis 75:347–353
Vitullo D, Pietro AD, Romano A, Lanzotti V, Lima G (2011) Role of new bacterial surfactins in the antifungal interaction between Bacillus amyloliquefaciens and Fusarium oxysporum. Plant Pathol. doi:10.1111/j.1365-3059.2011.02561.x
Wan M, Li G, Zhang J, Jiang D, Huang HC (2008) Effect of volatile substances of Streptomyces platensis F-1 on control of plant fungal diseases. Biol Control 46:552–559
Wang GL, Wang L, Chen HH, Shen B, Li SP, Jiang JD (2011) Lysobacter ruishenii sp. nov., a chlorothalonil-degrading bacterium isolated from a long-term chlorothalonil-contaminated soil in China. Int J Syst Evol Micr 61:674–679
Wheatley RE, Hackett C, Bruce A, Kundzewicz A (1997) Effect of substrate composition on production and inhibitory activity against wood decay fungi of volatile organic compounds from Trichoderma spp. Int Biodeter Biodegr 39:199–205
Wu HS, Yang XM, Fan JQ, Miao WG, Ling N, Shen QR (2008) Suppression of Fusarium wilt of watermelon by a bio-organic fertilizer containing combinations of antagonistic microorganisms. BioControl 54:287–295
Yuan J, Li B, Zhang N, Waseem R, Shen Q, Huang Q (2012) Production of bacillomycin- and macrolactin-type antibiotics by Bacillus amyloliquefaciens NJN-6 for suppressing soil borne plant pathogens. J Agric Food Chem 60:2976–2981
Zhang SS, Raza W, Yang XM, Hu J, Huang QW, Xu YC, Liu XH, Ran W, Shen QR (2008) Control of Fusarium wilt disease of cucumber plants with the application of a bioorganic fertilizer. Biol Fertil Soils 44:1073–1080
Zhang N, Wu K, He X, Li SQ, Zhang ZH, Shen B, Yang XM, Zhang RF, Huang QW, Shen QR (2011) A new bioorganic fertilizer can effectively control banana wilt by strong colonization with Bacillus subtilis N11. Plant Soil 344:87–97
Zhao QY, Dong CX, Yang XM, Mei XL, Ran W, Shen QR, Xu YC (2011) Biocontrol of Fusarium wilt disease for Cucumis melo melon using bio-organic fertilizer. Appl Soil Ecol 47:67–75
Acknowledgments
This work was supported by the National Natural Science Foundation of China (41101231), the Youth Foundation of Nanjing Agricultural University (KJ2011007), the Specialized Research Fund for the Doctoral Program of Higher Education (20110097120001), and the China Postdoctoral Science Foundation (2011M501248).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Rong Li and Yunze Ruan contributed equally to this article.
Rights and permissions
About this article
Cite this article
Wang, B., Yuan, J., Zhang, J. et al. Effects of novel bioorganic fertilizer produced by Bacillus amyloliquefaciens W19 on antagonism of Fusarium wilt of banana. Biol Fertil Soils 49, 435–446 (2013). https://doi.org/10.1007/s00374-012-0739-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-012-0739-5