Skip to main content
Log in

Cyclic siloxane biosurfactant-producing Bacillus cereus BS14 biocontrols charcoal rot pathogen Macrophomina phaseolina and induces growth promotion in Vigna mungo L.

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Rhizobacteria are vital component of soil–plant interfaces which helps in plant growth responses and disease management. Precisely, the role of biosurfactant production by rhizobacteria in biocontrol mechanisms is underscored. The current study explores the destructive effect of a biosurfactant-producing bacterium Bacillus cereus BS14 on fungal growth under in vitro experiments and showed in vivo reduction of disease severity in pulse crop Vigna mungo. In this study, B. cereus BS14 was observed as plant growth-promoting rhizobacterium (PGPR) based on abilities of production of phytohormone and HCN, phosphate solubilization and biocontrol of Macrophomina phaseolina. The purified biosurfactant from BS14 inhibited the fungal growth by arresting radially growing mycelia. Scanning electron microscope (SEM) study revealed deformities at cellular level in the mycelia of M. phaseolina. The biosurfactant of Bacillus BS14 was identified as cyclic siloxane in GC–MS spectroscopy and FT-IR spectroscopy analyses. In the pot trial studies, B. cereus BS14 proved its efficiency for the growth promotion of Vigna mungo and significantly reduced disease severity index. The present study concludes that biosurfactant of rhizobacterial origin and rhizobacteria can serve for biological control, improvement in crop production and agricultural sustainability. In future, it can be developed as biological control and biofertilizer formulations for legume crops, and commercialized for routine farming practices.

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

Access this article

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

Similar content being viewed by others

References

  • Adu FA, Hunter CH (2021) Screening and identification of lipopeptide biosurfactants produced by two aerobic endospore-forming bacteria isolated from Mfabeni Peatland, South Africa. Curr Microbiol 14:1–8

    Google Scholar 

  • Agarwal M, Dheeman S, Dubey RC, Kumar P, Maheshwari DK, Bajpai VK (2017) Differential antagonistic responses of Bacillus pumilus MSUA3 against Rhizoctonia solani and Fusarium oxysporum causing fungal diseases in Fagopyrum esculentum Moench. Microbiol Res 205:40–47

    Article  PubMed  Google Scholar 

  • Al-Ali A, Deravel J, Krier F, Béchet M, Ongena M, Jacques P (2018) Biofilm formation is determinant in tomato rhizosphere colonization by Bacillus velezensis FZB42. Environ Sci Pollut Res 25(30):29910–29920

    Article  CAS  Google Scholar 

  • Arora NK, Kang SC, Maheshwari DK (2001) Isolation of siderophore-producing strains of Rhizobium meliloti and their biocontrol potential against Macrophomina phaseolina that causes charcoal rot of groundnut. Curr Sci 81:673–677

    Google Scholar 

  • Avakyan ZA, Pivovarova TA, Karavaiko GI (1986) Properties of new species Bacillus mucilaginosus. Mikrobiologiya 55:477–482

    CAS  Google Scholar 

  • Ayed HB, Azabou MC, Hmidet N, Triki MA, Nasri M (2019) Economic production and biocontrol efficiency of lipopeptide biosurfactants from Bacillus mojavenis A21. Biodegradation 30(4):273–286

    Article  CAS  PubMed  Google Scholar 

  • 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(1):307–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bakker AW, Schippers B (1987) Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas spp. mediated plant growth-stimulation. Soil Biol Biochem 19:451–457

    Article  CAS  Google Scholar 

  • Baliyan N, Dheeman S, Maheshwari DK, Dubey RC, Vishnoi VK (2018) Rhizobacteria isolated under field first strategy improved chickpea growth and productivity. Environ Sustain 4:461–469

    Article  Google Scholar 

  • Bee H, Khan MY, Sayyed RZ (2019) Microbial surfactants and their significance in agriculture. Plant growth promoting rhizobacteria (PGPR): prospects for sustainable agriculture. Springer, Singapore, pp 205–215

    Chapter  Google Scholar 

  • Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350

    Article  CAS  PubMed  Google Scholar 

  • Bogino PC, Oliva MDLM, Sorroche FG, Giordano W (2013) The role of bacterial biofilms and surface components in plant-bacterial associations. Int J Mol Sci 14:15838–15859

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cameotra SS, Makkar RS (2004) Recent applications of biosurfactants as biological and immunological molecules. Curr Opin Microbiol 7:262–266

    Article  CAS  PubMed  Google Scholar 

  • Castaldi S, Petrillo C, Donadio G, Piaz FD, Cimmino A, Masi M, Evidente A, Isticato R (2021) Plant growth promotion function of Bacillus sp. strains isolated from Salt-Pan rhizosphere and their biocontrol potential against Macrophomina phaseolina. Int J Mol Sci 22(7):3324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen F, Wang M, Zheng Y, Luo J, Yang X, Wang X (2010) Quantitative changes of plant defense enzymes and phytohormone in biocontrol of cucumber Fusarium wilt by Bacillus subtilis B579. World J Microbiol Biotechnol 26(4):675–684

    Article  CAS  Google Scholar 

  • Das P, Mukherjee S, Sen R (2008) Improved bioavailability and biodegradation of a model polyaromatic hydrocarbon by a biosurfactant producing bacterium of marine origin. Chemosphere 72(9):1229–1234

    Article  CAS  PubMed  Google Scholar 

  • De Freitas JR, Banerjee MR, Germida JJ (1997) Phosphate-solubilizing rhizobacteria enhance the growth and yield but not phosphorus uptake of canola (Brassica napus L.). Biol Fertil Soil 24(4):358–364

    Article  Google Scholar 

  • Dheeman S, Baliyan N, Dubey RC, Maheshwari DK, Kumar S, Chen L (2020) Combined effects of rhizo-competitive rhizosphere and non-rhizosphere Bacillus in plant growth promotion and yield improvement of Eleusine coracana (Ragi). Can J Microbiol 66(2):111–124

    Article  CAS  PubMed  Google Scholar 

  • Dubey RC, Maheshwari DK, Kumar V, Pandey RR (2012) Growth enhancement of Sesamum indicum L. by rhizosphere-competent Azotobacter chroococcum AZO2 and its antagonistic activity against Macrophomina phaseolina. Arch Phytopathol Plant Prot 45:437–454

    Article  Google Scholar 

  • Dunne C, Crowley JJ, Moënne-Loccoz Y, Dowling DN, O’Gara F (1997) Biological control of Pythium ultimum by Stenotrophomonas maltophilia W81 is mediated by an extracellular proteolytic activity. Microbiology 143:3921–3931

    Article  CAS  PubMed  Google Scholar 

  • Goswami M, Deka S (2021) Biosurfactant-mediated biocontrol of pathogenic microbes of crop plants. Biosurfactants for a sustainable future: production and applications in the environment and biomedicine. Wiley, pp 491–509

    Chapter  Google Scholar 

  • Green MR, Sambrook J (2012) Molecular cloning: a laboratory manual, 4th edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Gupta CP, Dubey RC, Maheshwari DK (2002) Plant growth enhancement and suppression of Macrophomina phaseolina causing charcoal rot of peanut by fluorescent Pseudomonas. Biol Fertil Soil 35:399–405

    Article  CAS  Google Scholar 

  • Haas D, Keel C (2003) Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Ann Rev Phytopathol 41:117–153

    Article  CAS  Google Scholar 

  • Hafeez FY, Naureen Z, Sarwar A (2019) Surfactin: an emerging biocontrol tool for agriculture sustainability. Plant growth promoting rhizobacteria for agricultural sustainability. Springer, Singapore, pp 203–213

    Chapter  Google Scholar 

  • Hänsel R, Kruse D, Sieverding E, Riedl C, Ludwig JS (2019) Use of polyether modified short-chain siloxanes in agriculture in order to increase harvest yield. US Patent Application No. 16/073,091

  • Helassa N, Quiquampoix H, Noinville S, Szponarski W, Staunton S (2009) Adsorption and desorption of mono-meric Bt (Bacillus thuringiensis) Cry1Aa toxin on mont-morillonite and kaolinite. Soil Biol Biochem 41:498–504

    Article  CAS  Google Scholar 

  • Hil RM (2002) Silicone surfactants-new developments. Curr Opin Colloid Interface Sci 7(5–6):255–261

    Article  Google Scholar 

  • Holt JG, Krieg NR, Sneath PHA, Staley JT (1994) Bergey’s manual of determinative bacteriology, 9th edn. The Williams and Wilkins Co, Baltimore, p 787

    Google Scholar 

  • Hussain T, Khan AA (2020) Determining the antifungal activity and characterization of Bacillus siamensis AMU03 against Macrophomina phaseolina (Tassi) Goid. Indian Phytopathol 73:507–516

    Article  Google Scholar 

  • Illakkiam D, Ponraj P, Shankar M, Muthusubramanian S, Rajendhran J, Gunasekaran P (2013) Identification and structure elucidation of a novel antifungal compound produced by Pseudomonas aeruginosa PGPR2 against Macrophomina phaseolina. Appl Biochem Biotechnol 171(8):2176–2185

    Article  CAS  PubMed  Google Scholar 

  • Jain DK, Collins-Thompson DL, Lee H, Trevors TA (1991) Drop collapsing test for screening surfactant-producing microorganisms. J Microbiol Method 13:271–279

    Article  Google Scholar 

  • Jorgensen JH, Turnidge JD (2015) Susceptibility test methods: dilution and disk diffusion methods. Man Clin Microbiol. https://doi.org/10.1128/9781555817381.ch71

    Article  Google Scholar 

  • Kirby WMM, Yoshihara GM, Sundsted KS, Warren JH (1957) Clinical usefulness of a single disc method for antibiotic sensitivity testing. Antibiot Annu 1956–1957:892

    Google Scholar 

  • Kumar A, Johri BN (2012) Antimicrobial lipopeptides of Bacillus: natural weapons for biocontrol of plant pathogens. In: Satyanarayana T et al (eds) Microorganisms in sustainable agriculture and biotechnology. Springer Netherlands, pp 91–111

    Chapter  Google Scholar 

  • Kumar P, Dubey RC, Maheshwari DK (2012) Bacillus strains isolated from rhizosphere showed plant growth promoting and antagonistic activity against phytopathogens. Microbiol Res 167:493–499

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Dubey RC, Maheshwari DK (2016) Biosurfactant-mediated biocontrol of Macrophomina phaseolina causing charcoal rot in Vigna mungo by a plant growth promoting Enterococcus sp. BS13. J Plant Pathol Microbiol 7(385):2

    Google Scholar 

  • Lunkenheimer K, Wantke KD (1981) Determination of the surface tension of surfactant solutions applying the method of Lecomte du Noüy (ring tensiometer). Colloid Polym Sci 259:354–366

    Article  CAS  Google Scholar 

  • Lynch JM, Audus LJ (1976) Products of soil microorganisms in relation to plant growth. Crit Rev Microbiol 5(1):67–107

    Article  CAS  Google Scholar 

  • Maheshwari DK (2015) Bacterial metabolites in sustainable agroecosystem. Springer Science & Business Media

    Book  Google Scholar 

  • Maheshwari DK, Saraf M, Aeron A (2013) Bacteria in agrobiology: crop productivity. Springer Science & Business Media

    Book  Google Scholar 

  • Mehta P, Chauhan A, Mahajan R, Mahajan PK, Shirkot CK (2010) Strain of Bacillus circulans isolated from apple rhizosphere showing plant growth promoting potential. Curr Sci 98:538–542

  • Menéndez E, Paço A (2020) Is the application of plant probiotic bacterial consortia always beneficial for plants? Exploring synergies between rhizobial and non-rhizobial bacteria and their effects on agro-economically valuable crops. Life 10(3):24

    Article  PubMed Central  CAS  Google Scholar 

  • Mishra I, Fatima T, Egamberdieva D, Arora NK (2020) Novel bioformulations developed from Pseudomonas putida BSP9 and its biosurfactant for growth promotion of Brassica juncea (L.). Plants 9(10):1349

    Article  CAS  PubMed Central  Google Scholar 

  • Mnif I, Mnif S, Sahnoun R, Maktouf S, Ayedi Y, Ellouze-Chaabouni S, Ghribi D (2015) Biodegradation of diesel oil by a novel microbial consortium: comparison between co-inoculation with biosurfactant-producing strain and exogenously added biosurfactants. Environ Sci Pollut Res 22:14852–14861

    Article  CAS  Google Scholar 

  • Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726

    Article  CAS  PubMed  Google Scholar 

  • O’Toole GA (2011) Microtiter dish biofilm formation assay. JoVE 47:e2437

    Google Scholar 

  • Pandey AK, Burlakoti RR, Rathore A, Nair RM (2020) Morphological and molecular characterization of Macrophomina phaseolina isolated from three legume crops and evaluation of mungbean genotypes for resistance to dry root rot. Crop Prot 127:104962

    Article  CAS  Google Scholar 

  • Pandya U, Saraf M (2015) Isolation and identification of allelochemicals produced by B. sonorensis for suppression of charcoal rot of Arachis hypogaea L. J Basic Microbiol 55:635–644

    Article  CAS  PubMed  Google Scholar 

  • Prakash J, Arora NK (2019) Phosphate-solubilizing Bacillus sp. enhances growth, phosphorus uptake and oil yield of Mentha arvensis L. 3 Biotech 9(4):126

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodrigues LR, Teixeira JA, van der Mei HC, Oliveira R (2006) Physicochemical and functional characterization of a biosurfactant produced by Lactococcus lactis 53. Colloids Surf b: Biointerfaces 49:79–86

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues AI, Gudiña EJ, Teixeira JA, Rodrigues LR (2021) Biosurfactants as biocontrol agents against mycotoxigenic fungi. Biosurfactants for a sustainable future: production and applications in the environment and biomedicine, vol 5. Wiley, pp 465–490

    Chapter  Google Scholar 

  • Romano A, Vitullo D, Senatore M, Lima G, Lanzotti V (2013) Antifungal cyclic lipopeptides from Bacillus amyloliquefaciens strain BO5A. J Nat Prod 76:2019–2025

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg M, Gutnick D, Rosenberg E (1980) Adherence of bacteria to hydrocarbons a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol Lett 9:29–33

    Article  CAS  Google Scholar 

  • Sachdev DP, Cameotra SS (2013) Biosurfactants in agriculture. Appl Microbiol Biotechnol 97(3):1005–1016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanchez M, Aranda FJ, Espuny MJ, Marqués A, Teruel JA, Manresa A, Ortiz A (2007) Aggregation behavior of a dirhamnolipid biosurfactant secreted by Pseudomonas aeruginosa in aqueous media. J Colloid Interface Sci 307:246–253

    Article  CAS  PubMed  Google Scholar 

  • Sarwar A, Brader G, Corretto E, Aleti G, Abaidullah M, Sessitsch A, Hafeez FY (2018a) Qualitative analysis of biosurfactants from Bacillus species exhibiting antifungal activity. PLoS ONE 13(6):e0198107

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sarwar A, Hassan MN, Imran M, Iqbal M, Majeed S, Brader G, Sessitsch A, Hafeez FY (2018b) Biocontrol activity of surfactin A purified from Bacillus NH-100 and NH-217 against rice bakanae disease. Microbiol Res 209:1–13

    Article  CAS  PubMed  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  CAS  PubMed  Google Scholar 

  • Shahid S, Khan MR (2019) Evaluation of biocontrol agents for the management of root-rot of mung bean caused by Macrophomina phaseolina. Indian Phytopathol 72(1):89–98

    Article  Google Scholar 

  • Sharma CK, Vishnoi VK, Dubey RC, Maheshwari DK (2018) A twin rhizospheric bacterial consortium induces systemic resistance to a phytopathogen Macrophomina phaseolina in mung bean. Rhizosphere 5:71–75

    Article  Google Scholar 

  • Si O (2006) Need to assess efficacy of public health actions. In: Meeting of the California environmental contaminant biomonitoring program (CECBP) scientific guidance panel (SGP) December 4–5.

  • Siegmund I, Wagner F (1991) New method for detecting rhamnolipids excreted by Pseudomonas species during growth on mineral agar. Biotechnol Tech 5:265–268

    Article  CAS  Google Scholar 

  • Singh N, Kumar S, Bajpai VK, Dubey RC, Maheshwari DK, Kang SC (2010) Biological control of Macrophomina phaseolina by chemotactic fluorescent Pseudomonas aeruginosa PN1 and its plant growth promotory activity in chir-pine. Crop Prot 29(10):1142–1147

    Article  Google Scholar 

  • Singh R, Kumar M, Mittal A, Mehta PK (2017) Microbial metabolites in nutrition, healthcare and agriculture. 3Biotech 7(1):15

    Google Scholar 

  • Skidmore AM, Dickinson CH (1976) Colony interactions and hyphal interference between Septoria nodorum and phylloplane fungi. Trans Br Mycol Soc 66:57–64

    Article  Google Scholar 

  • Sotoyama K, Akutsu K, Nakajima N (2015) Biological control of Fusarium wilt by Bacillus amyloliquefaciens IUMC7 isolated from mushroom compost. J Gen Plant Pathol 82(2):105–109

    Article  CAS  Google Scholar 

  • Youssef NH, Duncan KE, Nagle DP, Savage KN, Knapp RM, McInerney MJ (2004) Comparison of methods to detect biosurfactant production by diverse microorganisms. J Microbiol Methods 56:339–347

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are thankful to the Head, Department of Botany & Microbiology for providing laboratory facilities.

Funding

This research is not supported by any funding.

Author information

Authors and Affiliations

Authors

Contributions

SK designed and conceived the experiment under mentorship of RCD. SD assisted during the experiments and prepared manuscript. NB helped during manuscript writing. RCD and DKM read the manuscript for scientific correction and approved for communication. SD corrected and revised the manuscript up to publication stage.

Corresponding authors

Correspondence to Shrivardhan Dheeman or Ramesh C. Dubey.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical approval

This research did not involve any animal and/ or human participants.

Additional information

Communicated by Erko Stackebrandt.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 15 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumar, S., Dheeman, S., Dubey, R.C. et al. Cyclic siloxane biosurfactant-producing Bacillus cereus BS14 biocontrols charcoal rot pathogen Macrophomina phaseolina and induces growth promotion in Vigna mungo L.. Arch Microbiol 203, 5043–5054 (2021). https://doi.org/10.1007/s00203-021-02492-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-021-02492-3

Keywords

Navigation