Skip to main content

Advertisement

SpringerLink
Log in

Efficacy of Bacillus amyloliquefaciens as biocontrol agent to fight fungal diseases of maize under tropical climates: from lab to field assays in south Kivu

  • Chemistry, Activity and Impact of Plant Biocontrol products
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

In the province of South Kivu (Democratic Republic of Congo), warm and humid climatic conditions favor the development and spreading of phytopathogens. The resulting diseases cause important losses in production both in crop and after harvest. In this study, we wanted to evaluate the potential of Bacillus amyloliquefaciens as biocontrol agent to fight some newly isolated endemic fungal pathogens infesting maize. The strain S499 has been selected based on its high in vitro antagonistic activity correlating with a huge potential to secrete fungitoxic lipopeptides upon feeding on maize root exudates. Biocontrol activity of S499 was further tested on infected plantlets in growth chamber and on plants grown under field conditions over an entire cropping period. We observed a strong protective effect of this strain evaluated at two different locations with specific agro-ecological conditions. Interestingly, disease protection was associated with higher yields and our data strongly suggest that, in addition to directly inhibit pathogens, the strain may also act as biofertilizer through the solubilization of phosphorus and/or by producing plant growth hormones in the rhizosphere. This work supports the hope of exploiting such technologically advantageous bacilli for the sake of sustainable local production of this important crop in central Africa.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Arguelles-Arias A, Ongena M, Halimi B, Lara Y, 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 Factories 8:1–12. doi:10.1186/1475-2859-8-63

    Article  CAS  Google Scholar 

  • Borriss R (2011) Use of plant-associated Bacillus strains as biofertilizers and biocontrol agents. In: Maheshwari DK (ed) Bacteria in agrobiology: plant growth responses. Springer, Heidelberg, pp 41–76

    Chapter  Google Scholar 

  • Budiharjo A, Chowdhury SP, Dietel K, Beator B, Dolgova O, Fan B, Borriss R (2014) Transposon mutagenesis of the plant-associated Bacillus amyloliquefaciens sp. plantarum FZB42 revealed that the nfrA and RBAM17410 genes are involved in plant-microbe-interactions. PLoS One 9:1–13. doi:10.1371/journal.pone.0098267

    Article  CAS  Google Scholar 

  • Cavaglieri L, Orlando J, Rodríguez MI, Chulze S, Etcheverry M (2005) Biocontrol of Bacillus subtilis against Fusarium verticillioides in vitro and at the maize root level. Res Microbiol 156:748–754. doi:10.1016/j.resmic.2005.03.001

    Article  CAS  Google Scholar 

  • Cawoy H, Debois D, Franzil L, De Pauw E, Thonart P, Ongena M (2015) Lipopeptides as main ingredients for inhibition of fungal phytopathogens by Bacillus subtilis/ amyloliquefaciens. Microb Biotechnol 8:281–295. doi:10.1111/1751-7915.12238

    Article  CAS  Google Scholar 

  • Cawoy H, Mariutto M, Henry G, Fisher C, Vasilyeva N, Thonart P, Dommes J, Ongena M (2014) Plant defense stimulation by natural isolates of Bacillus depends on efficient surfactin production. Mol Plant-Microbe Interact 27:87–100. doi:10.1094/MPMI-09-13-0262

    Article  CAS  Google Scholar 

  • Chen XH, Koumoutsi A, Scholz R, Schneider K, Vater J, Süssmuth R, Borriss R (2009) Genome analysis of Bacillus amyloliquefaciens FZB42 reveals its potential for biocontrol of plant pathogens. J Biotechnol 140:27–37. doi:10.1016/j.jbiotec.2008.10.011

    Article  CAS  Google Scholar 

  • 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 94:159–166. doi:10.1046/j.1365-2672.2003.01819.x

    Article  CAS  Google Scholar 

  • Chowdhury SP, Hartmann A, Gao X, Borriss R (2015) Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42 - a review. Front Microbiol 6:1–12. doi:10.3389/fmicb.2015.00780

    Article  Google Scholar 

  • Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959. doi:10.1128/AEM.71.9.4951-4959.2005

    Article  CAS  Google Scholar 

  • Debois D, Fernandez O, Franzil L, Jourdan E, de Brogniez A, Willems L, Ongena M (2015) Plant polysaccharides initiate underground crosstalk with bacilli by inducing synthesis of the immunogenic lipopeptide surfactin. Environ Microbiol Rep 7:570–582. doi:10.1111/1758-2229.12286

    Article  CAS  Google Scholar 

  • Debois D, Jourdan E, Smargiasso N, Thonart P, De Pauw E, Ongena M (2014) Spatiotemporal monitoring of the antibiome secreted by Bacillus biofilms on plant roots using MALDI mass spectrometry imaging. Anal Chem 86:4431–4438. doi:10.1021/ac500290s

    Article  CAS  Google Scholar 

  • Debois D, Ongena M, Cawoy H, De Pauw E (2013) MALDI-FTICR MS imaging as a powerful tool to identify Paenibacillus antibiotics involved in the inhibition of plant pathogens. J Am Soc Mass Spectrom 24:1202–1213. doi:10.1007/s13361-013-0620-2

    Article  CAS  Google Scholar 

  • Dunlap CA, Kim SJ, Kwon SW, Rooney AP (2016) Bacillus velezensis is not a later heterotypic synonym of Bacillus amyloliquefaciens; Bacillus velezensis, Bacillus amyloliquefaciens subsp. plantarum and Bacillus oryzicola are later heterotypic synonyms of Bacillus velezensis based on phylogenomics. Int J Syst Evol Microbiol 66:1212–1217. doi:10.1099/ijsem.0.000858

    Article  CAS  Google Scholar 

  • Fravel DR (2005) Commercialization and implementation of biocontrol. Annu Rev Phytopathol 43:337–359. doi:10.1146/annurev.phyto.43.032904.092924

    Article  CAS  Google Scholar 

  • García-Gutiérrez L, Zeriouh H, Romero D, Cubero J, de Vicente A, Pérez-García A (2013) The antagonistic strain Bacillus subtilis UMAF6639 also confers protection to melon plants against cucurbit powdery mildew by activation of jasmonate- and salicylic acid-dependent defence responses. Microb Biotechnol 6:264–274. doi:10.1111/1751-7915.12028

    Article  CAS  Google Scholar 

  • Gond SK, Bergen MS, Torres MS, White JF (2015) Endophytic Bacillus spp. produce antifungal lipopeptides and induce host defence gene expression in maize. Microbiol Res 172:79–87. doi:10.1016/j.micres.2014.11.004

    Article  CAS  Google Scholar 

  • Hanene R, Abdeljabbar H, Marc R, Abdellatif B, Ferid L, Najla SZ (2012) Biological control of Fusarium foot rot of wheat using fengycin-producing Bacillus subtilis isolated from salty soil. Afr J Biotechnol 11:8464–8475. doi:10.5897/AJB11.2887

    Article  CAS  Google Scholar 

  • Jourdan E, Henry G, Duby F, Dommes J, Barthélemy JP, Thonart P, Ongena M (2009) Insights into the defense-related events occurring in plant cells following perception of surfactin-type lipopeptide from Bacillus subtilis. Mol Plant-Microbe Interact 22:456–468. doi:10.1371/journal.pone.0106041

    Article  CAS  Google Scholar 

  • Kwon J, Kang S, Kim J, Park C (2001) Rhizopus soft rot on cherry tomato caused by Rhizopus stolonifer in Korea. J Microbiol 29:176–178. doi:10.4489/MYCO.2006.34.3.151

    Article  Google Scholar 

  • Leclère V, Béchet M, Adam A, Wathelet B, Ongena M, Thonart P, Jacques P (2005) Mycosubtilin overproduction by Bacillus subtilis BBG100 enhances the organisms antagonistic and biocontrol activities. Appl Environ Microbiol 71:4577–4584. doi:10.1128/AEM.71.8.4577

    Article  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556. doi:10.1146/annurev.micro.62.081307.162918

    Article  CAS  Google Scholar 

  • Manjula K, Podile AR (2005) Production of fungal cell wall degrading enzymes by a biocontrol strain of Bacillus subtilis AF 1. Indian J Exp Biol 43:892–896

    CAS  Google Scholar 

  • Mehta P, Walia A, Chauhan A, Kulshrestha S, Shirkot CK (2013) Phosphate solubilisation and plant growth promoting potential by stress tolerant Bacillus sp. isolated from rhizosphere of apple orchards in trans Himalayan region of Himachal Pradesh. Ann Appl Biol 163:430–443. doi:10.1111/aab.12077

    Article  CAS  Google Scholar 

  • Mercado-Blanco J, Bakker PAHM (2007) Interactions between plants and beneficial Pseudomonas spp: Exploiting bacterial traits for crop protection. A Van Leeuw J Microb 92:367. doi:10.1007/s10482-007-9167-1

    Article  Google Scholar 

  • Molinatto G, Puopolo G, Sonego P, Moretto M, Engelen K, Viti C, Ongena M, Pertot I (2016) Complete genome sequence of Bacillus amyloliquefaciens subsp. plantarum S499,a rhizobacterium that triggers plant defences and inhibits fungal phytopathogens. J Biotechnol 238:56–59. doi:10.1016/j.jbiotec.2016.09.013

    Article  CAS  Google Scholar 

  • 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. doi:10.1046/j.1365-2672.2001.01290.x

    Article  CAS  Google Scholar 

  • Nagorska K, Bikowski M, Obuchowskji M (2007) Multicellular behaviourand production of a wide variety of toxic substances support usage of Bacillus subtilis as a powerful biocontrol agent. Acta Biochim Pol 54:495–508

    CAS  Google Scholar 

  • Nihorimbere V, Cawoy H, Seyer A, Brunelle A, Thonart P, Ongena M (2012) Impact of rhizosphere factors on cyclic lipopeptide signature from the plant beneficial strain Bacillus amyloliquefaciens S499. FEMS Microbiol Ecol 79:176–191. doi:10.1111/j.1574-6941.2011.01208

    Article  CAS  Google Scholar 

  • 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 4:1135–1142

    Google Scholar 

  • Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125. doi:10.1016/j.tim.2007.12.009

    Article  CAS  Google Scholar 

  • Ongena M, Jourdan E, Adam A, Paquot M, Brans A, Joris B, Thonart P (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9:1084–1090. doi:10.1111/j.1462-2920.2006.01202.x

    Article  CAS  Google Scholar 

  • Pérez-García A, Romero D, de Vicente A (2011) Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture. Curr Opin Biotechnol 22:187–193. doi:10.1016/j.copbio.2010.12.003

    Article  CAS  Google Scholar 

  • Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375. doi:10.1146/annurev-phyto-082712-102340

    Article  CAS  Google Scholar 

  • Raaijmakers JM, de Bruijn I, Nybroe O, Ongena M (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev 34:1037–1062. doi:10.1111/j.1574-6976.2010.00221.x

    Article  CAS  Google Scholar 

  • Ravensberg WJ (2015) Commercialisation of microbes: present situation and future prospects. In: Lugtenberg B (ed) Principles of Plant-microbe interactions. Microbes for sustainable agriculture. Springer International Publishing Switzerland, Heidelberg, p 309–317

    Google Scholar 

  • Reid LM, Zhu X, Canada. Agriculture et agroalimentaire Canada. (2005) Criblage du maïs quant à sa résistance aux maladies courantes au Canada. Agriculture et agroalimentaire Canada

  • Rodríguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339. doi:10.1016/S0734-9750(99)00014-2

    Article  Google Scholar 

  • Romero D, De Vicente A, Olmos JL, Dávila JC, Pérez-García A (2007) Effect of lipopeptides of antagonistic strains of Bacillus subtilis on the morphology and ultrastructure of the cucurbit fungal pathogen Podosphaera fusca. J Appl Microbiol 103:969–976. doi:10.1111/j.1365-2672.2007.03323

    Article  CAS  Google Scholar 

  • Rückert C, Blom J, Chen X, Reva O, Borriss R (2011) Genome sequence of B. amyloliquefaciens type strain DSM7T reveals differences to plant-associated B. amyloliquefaciens FZB42. J Biotechnol 155:78–85. doi:10.1016/j.jbiotec.2011.01.006

    Article  CAS  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci U S A 100:4927–4932

    Article  CAS  Google Scholar 

  • Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56:845–857. doi:10.1111/j.1365-2958.2005.04587.x

    Article  CAS  Google Scholar 

  • Sweets LE, Wright S (2008) Integrated pest management. Corn diseases. Plant protection programs. College of Agriculture, Food and Natural Resources. University of Missouri, Columbia. 1–23

  • Tollens E (2003) L’état actuel de la sécurité alimentaire en R.D. Congo: Diagnostic et perspectives. Working Paper, n°77, Département d'Economie Agricole et de l'Environnement, Katholieke Universiteit Leuven, 6p

  • Touré Y, Ongena M, Jacques P, Guiro A, Thonart P (2004) Role of lipopeptides produced by Bacillus subtilis GA1 in the reduction of grey mould disease caused by Botrytis cinerea on apple. J Appl Microbiol 96:1151–1160. doi:10.1111/j.1365-2672.2004.02252

    Article  Google Scholar 

  • Velmurugan N, Choi MS, Han SS, Lee YS (2009) Evaluation of antagonistic activities of Bacillus subtilis and Bacillus licheniformis against wood-staining fungi: in vitro and in vivo experiments. J Microbiol 47:385–392. doi:10.1007/s12275-009-0018-9

    Article  CAS  Google Scholar 

  • Wu L, Wu HJ, Qiao J, Gao X, Borriss R (2015) Novel routes for improving biocontrol activity of Bacillus-based bioinoculants. Front Microbiol 6:1–13. doi:10.3389/fmicb.2015.01395

    Article  Google Scholar 

  • Yánez-Mendizábal V, Zeriouh H, Viñas I, Torres R, Usall J, de Vicente A, Teixidó N (2012) Biological control of peach brown rot (Monilinia spp.) by Bacillus subtilis CPA-8 is based on production of fengycin-like lipopeptides. Eur J Plant Pathol 132:609–619. doi:10.1007/s10658-011-9905-0

    Article  CAS  Google Scholar 

  • Yildirim I, Turhan H, Özgen B (2010) The effects of head rot disease (Rhizopus stolonifer) on sunflower genotypes at two different growth stages. Turk J Field Crops 15:94–98

    Google Scholar 

  • Zhang X, Li B, Wang Y, Guo Q, Lu X, Li S, Ma P (2013) Lipopeptides, a novel protein, and volatile compounds contribute to the antifungal activity of the biocontrol agent Bacillus atrophaeus CAB-1. Appl Microbiol Biotechnol 97:9525–9534. doi:10.1007/s00253

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the scholarship program Brot für die Welt-Germany in the context of partnership with the Evangelical University in Africa of Bukavu, eastern of democratic republic of Congo. The authors also thank Laurent Franzil for UPLC-MS analyzes. M. Ongena is Senior Research Associate at the F.R.S.-FNRS (Fonds National de la Recherche Scientifique) in Belgium.

Author information

Authors and Affiliations

  1. Microbial Processes and Interactions Laboratory, Faculty Gembloux Agro-BioTech, University of Liège, Passage des Déportés 2, 5030, Gembloux, Belgium

    Parent Zihalirwa Kulimushi, Philippe Thonart & Marc Ongena

  2. Laboratory of Biotechnology and Molecular Biology, Faculty of Agricultural and Environmental Sciences, Université Evangélique en Afrique, 3323, Bukavu, Democratic Republic of the Congo

    Parent Zihalirwa Kulimushi

  3. Laboratory of Ecophysiology and Plants Nutrition, Faculty of Agricultural and Environmental Sciences, Université Evangélique en Afrique, 3323, Bukavu, Democratic Republic of the Congo

    Géant Chuma Basime & Gustave Mushagalusa Nachigera

Authors
  1. Parent Zihalirwa Kulimushi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Géant Chuma Basime
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gustave Mushagalusa Nachigera
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Philippe Thonart
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marc Ongena
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marc Ongena.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kulimushi, P.Z., Basime, G.C., Nachigera, G.M. et al. Efficacy of Bacillus amyloliquefaciens as biocontrol agent to fight fungal diseases of maize under tropical climates: from lab to field assays in south Kivu. Environ Sci Pollut Res 25, 29808–29821 (2018). https://doi.org/10.1007/s11356-017-9314-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-9314-9

Keywords

Search

Navigation