Skip to main content
SpringerLink
Log in

Formulation of biofungicides based on Streptomyces caeruleatus strain ZL-2 spores and efficacy against Rhizoctonia solani damping-off of tomato seedlings

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

Abstract

This work aims at exploring an antagonistic actinobacterial strain isolated from the roots of Ziziphus lotus in bioformulation processes and the biocontrol of Rhizoctonia solani damping-off of tomato seedlings. The strain Streptomyces caeruleatus ZL-2 was investigated for the principal in vitro biocontrol mechanisms and then formulated in three different biofungicides: wettable talcum powder (WTP), sodium alginate propagules (SAP) and clay sodium alginate propagules (CAP). Compared to a marketed control products (Serenade® and Acil 060FS®), the formulated biofungicides were investigated against the R. solani damping-off of tomato cv. Aïcha seedlings. The strain ZL-2 produced chitinases, cellulases, β-1,3-glucanases, cyanhydric acid and siderophores. It also showed strong antagonistic effect on the mycelial growth of R. solani. Bioautographic and HPLC analysis revealed the production of a single or several co-migrating antifungal compounds. The biofungicide WTP presented an attractive biocontrol effect by significantly reducing the disease severity index (DSI) compared to untreated seeds. No significant differences were obtained compared to the chemical treatment with Acil 060FS®. The viability of spores and biocontrol efficacy of the WTP were confirmed after 1-year storage. Strain ZL-2 has never been reported in the bioformulation of active biofungicides against Rhizoctonia solani damping-off and this work opens up very attractive prospects in the fields of biocontrol and crop improvement.

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.

Institutional subscriptions

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

Similar content being viewed by others

Data availability

All data and materials are available.

References

  • Ajayi-Oyetundea OO, Bradley CA (2018) Rhizoctonia solani: taxonomy, population biology and management of Rhizoctonia seedling disease of soybean. Plant Pathol 67:3–17. https://doi.org/10.1111/ppa.12733

    Article  CAS  Google Scholar 

  • Allali K, Goudjal Y, Zamoum M, Bouznada K, Sabaou N, Zitouni A (2019) Nocardiopsis dassonvillei strain MB22 from the Algerian Sahara promotes wheat seedlings growth and potentially controls the common root rot pathogen Bipolaris sorokiniana. J Plant Pathol 101:1115–1125

    Article  Google Scholar 

  • Aouiche A, Sabaou N, Zitouni A, Meklat A, Bijani C, Mathieu F, Lebrihi A (2012) Saccharothrix sp. PAL54, a new producing chloramphenicol strain isolated from a Saharan soil. World J Microbiol Biotechnol 28:943–951

    Article  CAS  Google Scholar 

  • Behera HT, Mojumdar A, Das SR, Jena S, Ray L (2020) Production of N-acetyl chitooligosaccharide by novel Streptomyces chilikensis strain RC1830 and its evaluation for anti-radical, anti-inflammatory, anti-proliferative and cell migration potential. Bioresource Technol Reports 11:100428

    Article  Google Scholar 

  • Bencheikh M, Setti B (2010) The talc formulation of Streptomyces antagonist against Mycosphaerella foot rot in pea (Pisum sativum L.). Arch Phytopathol Plant Protec 43(5):438–445

    Article  Google Scholar 

  • Betina V (1973) Bioautography in paper and thin layer chromatography and its scope in the antibiotic field. J Chromatogr 78:41–51

    Article  CAS  Google Scholar 

  • Blom D, Fabbri C, Eberl L, Weisskopf L (2011) Volatile mediated killing of Arabidopsis thaliana by bacteria is mainly mediated due to hydrogen cyanide. Appl Environ Microbiol 77:1000–1008

    Article  CAS  Google Scholar 

  • Bubici G (2018) Streptomyces spp. as biocontrol agents against Fusarium species. CAB Rev 13:50

    Google Scholar 

  • Buysens S, Heungens K, Poppe J, Hofte M (1996) Involvement of pyochelin and pyoverdin in suppression of Pythium-induced damping-off of tomato by Pseudomonas aeruginosa 7NSK2. Appl Environ Microbiol 62:865–871

    Article  CAS  Google Scholar 

  • Cao L, Qiu Z, You J, Tan H, Zhou S (2004) Isolation and characterization of endophytic Streptomyces strains from surface-sterilized tomato (Lycopersicon esculentum) roots. Lett Appl Microbiol 39:425–430

    Article  CAS  Google Scholar 

  • Dhanasekaran D, Sivamani P, Panneerselvam A, Thajuddin N, Rajakumar G, Selvamani S (2005) Biological control of tomato seedling damping-off with Streptomyces sp. Plant Pathol J 4:91–95

    Article  Google Scholar 

  • Elliott M, Shamoun SF, Sumampong G, James D, Masri S, Varga A (2009) Evaluation of several commercial biocontrol products on European and North American populations of Phytophthora ramorum. Biocontrol Sci Technol 99:1007–1021

    Article  Google Scholar 

  • Fox JE, Gulledge J, Engelhaupt E, Burow ME, McLachlan JA (2007) Pesticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants. Proc Natl Acad Sci USA 104(24):10282–10287. https://doi.org/10.1073/pnas.0611710104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geetha K, Vikineswary S (2002) Antagonistic effects of Streptomyces violaceusniger strain G10 on Fusarium oxysporum f. sp. cubense race 4: indirect evidence for the role of antibiosis in the antagonistic process. J Ind Microbiol Biotechnol 28:303–310

    Article  Google Scholar 

  • Getha K, Vikineswary S, Wong WH, Seki T, Ward A, Goodfellow M (2005) Evaluation of Streptomyces sp. strain g10 for suppression of Fusarium wilt and rhizosphere colonization in pot-grown banana plantlets. J Ind Microbiol Biotechnol 32:24–32

    Article  CAS  Google Scholar 

  • Ghasemi S, Safaie N, Shahbazi S, Shams-Bakhsh M, Askari H (2020) The role of cell wall degrading enzymes in antagonistic traits of Trichoderma virens against Rhizoctonia solani. Iran J Biotechnol 18(4):e2333. https://doi.org/10.30498/IJB.2020.2333

    Article  PubMed  PubMed Central  Google Scholar 

  • Goudjal Y, Toumatia O, Yekkour A, Sabaou N, Mathieu F, Zitouni A (2014) Biocontrol of Rhizoctonia solani damping-off and promotion of tomato plant growth by endophytic actinomycetes isolated from native plants of Algerian Sahara. Microbiol Res 169:59–65

    Article  CAS  Google Scholar 

  • Hoppin JA, Umbach DM, London SJ, Henneberger PK, Kullman GJ, Coble J, Alavanja MC, Beane Freeman LE, Sandler DP (2009) Pesticide use and adult-onset asthma among male farmers in the agricultural health study. Eur Respir J 34(6):1296–1303. https://doi.org/10.1183/09031936.00005509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horst RK (2013) Damping-off Westcott’s plant disease handbook. Springer, Netherlands, Dordrecht

    Book  Google Scholar 

  • Keinath AP (1995) Reduction in inoculum density of Rhizoctonia solani and control of belly rot on cucumberty with solarization. Plant Dis 79:1213–1219

    Article  Google Scholar 

  • Lamichhane JR, Dürr C, Schwanck AA, Robin MH, Sarthou JP, Cellier V, Messéan A, Aubertot JN (2017) Integrated management of damping-off diseases. Agron Sustain Dev 37:10. https://doi.org/10.1007/s13593-017-0417-y

    Article  Google Scholar 

  • Lumsden RD, Lewis JA, Fravel DR (1995) Formulation and delivery of biocontrol agents for use against soil-borne plant pathogens. In: Hall FR, Barry JW (eds) Biorational pest control agents. American chemical society, Washington, pp 165–182

    Google Scholar 

  • Minuto A, Spadaro D, Garibaldi A, Gullino ML (2006) Control of soil-borne pathogens of tomato using a commercial formulation of Streptomyces griseoviridis and solarization. Crop Prot 25(5):468–475

    Article  Google Scholar 

  • Mohamed OG, Khalil ZG, Salim A, Cui H, Blumenthal A, Robert J, Capon RJ (2021) Lincolnenins A-D: Isomeric Bactericidal Bianthracenes from Streptomyces lincolnensis. J Organic Chem 86(16):11011–11018. https://doi.org/10.1021/acs.joc.0c02492

    Article  CAS  Google Scholar 

  • Nirmala P, Sindhu A (2011) Production of endoglucanase by optimizing the environmental conditions of Bacillus circulans on submerged fermentation. Inter J Appl Engin Res 2:472–481

    CAS  Google Scholar 

  • Olanrewaju OS, Babalola OO (2019) Streptomyces: implications and interactions in plant growth promotion. Appl Microbiol Biotechnol 103:1179–1188

    Article  CAS  Google Scholar 

  • Passari AK, Mishra VK, Gupta VK, Yadav MK, Saikia R, Singh BP (2015) In vitro and in vivo plant growth promoting activities and DNA fingerprinting of antagonistic endophytic actinomycetes associates with medicinal plants. PLoS ONE 10:e0139468

    Article  Google Scholar 

  • Ramos-Solano B, Lucas García JA, Garcia-Villaraco A, Algar E, Garcia-Cristobal J, Mañero FJG (2010) Siderophore and chitinase producing isolates from the rhizosphere of Nicotiana glauca Graham enhance growth and induce systemic resistance in Solanum lycopersicum L. Plant Soil 334:189–197

    Article  CAS  Google Scholar 

  • Roskova Z, Sharohlid R, McGachy L (2022) Siderophores: an alternative bioremediation strategy? Sci Total Environnement 819:144–153

    Google Scholar 

  • Sabaratnam S, Traquair JA (2002) Formulation of a Streptomyces biocontrol agent for the suppression of Rhizoctonia damping-off in tomato transplants. Biol Control 23:245–253

    Article  CAS  Google Scholar 

  • Sankararamakrishnan N, Kumar Sharma A, Sanghi R (2005) Organochlorine and organophosphorous pesticide residues in ground water and surface waters of Kanpur, Uttar Pradesh. India Environ Int 31(1):113–120. https://doi.org/10.1016/j.envint.2004.08.001

    Article  CAS  PubMed  Google Scholar 

  • Santhosh G (2015) Formulation and shelf life of liquid biofertilizer inoculants using cell protectants. Int J Res Biosci Agric Technol 7:243–247

    Google Scholar 

  • Sarmiento-Vizcaíno A, Martín J, Reyes F, García LA, Blanco G (2021) Bioactive natural products in actinobacteria isolated in rainwater from storm clouds transported by western winds in spain. Frontiers Microbiol. https://doi.org/10.3389/fmicb.2021.773095

    Article  Google Scholar 

  • Singh BK, Walker A (2006) Microbial degradation of organophosphorus compounds. FEMS Microbiol Rev 30(3):428–471

    Article  CAS  Google Scholar 

  • Sneh B, Jabaji-Hare S, Neat S, Dijst G (1996) Rhizoctonia: taxonomie, molecular biology, ecology, pathology, and control. Kliwer Academic Publisher, Dordrecht, The Netherlands

    Google Scholar 

  • Spence C, Alff E, Johnson C, Ramos C, Donofrio N, Sundaresan V, Bais H (2014) Natural rice rhizospheric microbes suppress rice blast infections. BMC Plant Biol 14:1–17

    Article  Google Scholar 

  • Szilagyi-Zecchin VJ, Mógor ÁF, Figueiredo GGO (2016) Strategies for characterization of agriculturally important bacteria. In: Singh DP et al (eds) Microbial inoculants in sustainable agricultural productivity. Springer, Dordrecht

    Google Scholar 

  • Tamreihao K, Ningthoujam DS, Nimaichand S, Singh ES, Reena P, Singh SH, Nongthomba U (2016) Biocontrol and plant growth promoting activities of a Streptomyces corchorusii strain UCR3-16 and preparation of powder formulation for application as biofertilizer agents for rice plant. Microbiol Res 192:260–270

    Article  CAS  Google Scholar 

  • Yandigeri MS, Malviya N, Solanki MK, Shrivastava P, Sivakumar G (2015) Chitinolytic Streptomyces vinaceusdrappus S5MW2 isolated from Chilika lake, India enhances plant growth and biocontrol efficacy through chitin supplementation against Rhizoctonia solani. World J Microbiol Biotechnol 31:1217–1225

    Article  CAS  Google Scholar 

  • Yang Y, Wu Z, Li K (2019) The peculiar physiological responses of Rhizoctonia solani under the antagonistic interaction coupled by a novel antifungalmycin N2 from Streptomyces sp. N2. Arch Microbiol 201:787–794. https://doi.org/10.1007/s00203-019-01645-9

    Article  CAS  PubMed  Google Scholar 

  • Yekkour A, Sabaou N, Zitouni A, Errakhi R, Mathieu F, Lebrihi A (2012) Characterization and antagonistic properties of Streptomyces strains isolated from Saharan soils, and evaluation of their ability to control seedling blight of barley caused by Fusarium culmorum. Lett App Microbiol 55:427–435

    Article  CAS  Google Scholar 

  • Zacky FM, Ting ASY (2015) Biocontrol of Fusarium oxysporum f.sp. cubense tropical race 4 by formulated cells and cell-free extracts of Streptomyces griseus in sterile soil environment. Biocontrol Sci Technol 25:685–696

    Article  Google Scholar 

  • Zamoum M, Goudjal Y, Sabaou N, Barakate M, Mathieu F, Zitouni A (2015) Biocontrol capacities and plant growth-promoting traits of endophytic actinobacteria isolated from native plants of Algerian Sahara. J Plant Dis Prot 122:215–223

    Article  Google Scholar 

  • Zamoum M, Goudjal Y, Sabaou N, Mathieu F, Zitouni A (2017) Development of formulations based on Streptomyces rochei strain PTL2 spores for biocontrol of Rhizoctonia solani damping-off of tomato seedlings. Biocontrol Sci Technol 27:723–738

    Article  Google Scholar 

Download references

Acknowledgements

This paper is in the memory of the deceased Pr. Nasserdine Sabaou (1956-2019), an excellent researcher and a great professor of microbiology (Ecole Normale Supérieure de Kouba, Alger-Algeria) and the Director of our research laboratory, the LBSM (Laboratoire de Biologie des Systemes Microbiens). Professor Nasserdine Sabaou has been a constant source of knowledge and inspiration. The authors acknowledge the support of the Ministry of Higher Education and Scientific Research of Algeria.

Funding

Not applicable; we used the facilities available in our research laboratory.

Author information

Authors and Affiliations

  1. Laboratoire de Biologie Des Systèmes Microbiens (LBSM), Ecole Normale Supérieure de Kouba, Alger, Algeria

    Miyada Zamoum, Khadidja Allali, Abdelghani Zitouni & Yacine Goudjal

  2. Département d’Agronomie, Faculté Des Sciences, Université Amar Telidji, BP 37G, Laghouat, Algeria

    Miyada Zamoum, Khadidja Allali & Yacine Goudjal

  3. Laboratory of Natural Substances, Biomolecules and Biotechnological Applications, Department of Natural and Life Sciences, Larbi Ben M’hidi University, BP 358, 04000, Oum El Bouaghi, Algeria

    Abderrahmane Benadjila

Authors
  1. Miyada Zamoum
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Khadidja Allali
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Abderrahmane Benadjila
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Abdelghani Zitouni
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yacine Goudjal
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

We confirm that this research was conducted in our research laboratory. All authors contributed critically in performing and analyzing the results. YG, AZ and MZ conceived and designed the research. KA, MZ and AB conducted the experiments and analyzed the data. KA and YG wrote the manuscript. MZ supervised the research. All authors read and approved the manuscript.

Corresponding author

Correspondence to Miyada Zamoum.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Human and animal rights

This article does not contain any studies with human participants or animals.

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 807 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zamoum, M., Allali, K., Benadjila, A. et al. Formulation of biofungicides based on Streptomyces caeruleatus strain ZL-2 spores and efficacy against Rhizoctonia solani damping-off of tomato seedlings. Arch Microbiol 204, 629 (2022). https://doi.org/10.1007/s00203-022-03251-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00203-022-03251-8

Keywords

Search

Navigation