Skip to main content
Log in

Bacillus subtilis SPB1 lipopeptide biosurfactant: antibacterial efficiency against the phytopathogenic bacteria Agrobacterium tumefaciens and compared production in submerged and solid state fermentation systems

  • Research Article
  • Published:
Food Science and Biotechnology Aims and scope Submit manuscript

Abstract

Bacillus subtilis SPB1 derived biosurfactants (BioS) proved its bio-control activity against Agrobacterium tumefaciens using tomato plant. Almost 83% of disease symptoms triggered by Agrobacterium tumefaciens were reduced. Aiming potential application, we studied lipopeptide cost-effective production in both fermentations systems, namely the submerged fermentation (SmF) and the solid-state fermentation (SSF) as well as the use of Aleppo pine waste and confectionery effluent as cheap substrates. Optimization studies using Box–Behnken (BB) design followed by the analysis with response surface methodology were applied. When using an effluent/sea water ratio of 1, Aleppo pine waste of 14.08 g/L and an inoculum size of 0.2, a best production yield of 17.16 ± 0.91 mg/g was obtained for the SmF. While for the SSF, the best production yield of 27.59 ± 1.63 mg/g was achieved when the value of Aleppo pine waste, moisture, and inoculum size were, respectively, equal to 25 g, 75%, and 0.2. Hence, this work demonstrated the superiority of SSF over SmF.

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

Similar content being viewed by others

Data availability

All data and materials are available.

Abbreviations

BB:

Box Behnken

BioS:

Biosurfactants

SmF:

Submerged fermentation

SSF:

Solid state fermentation

References

  • Almeida DG, Soares da Silva RdCF, Luna JM, Rufino RD, Santos VA, Sarubbo LA. Response surface methodology for optimizing the production of biosurfactant by Candida tropicalis on industrial waste substrates. Frontiers in Microbiology. 8: 157 (2017)

  • Al-Reza SM, Rahman A, Ahmed Y, Kang SC. Inhibition of plant pathogens in vitro and in vivo with essential oil and organic extracts of Cestrum nocturnum L. Pesticide Biochemistry and Physiology. 96: 86-92 (2010)

    Article  CAS  Google Scholar 

  • Banat IM, Carboué Q, Saucedo-Castañeda G, de Jesús Cázares-Marinero J. Biosurfactants: The green generation of speciality chemicals and potential production using Solid-State fermentation (SSF) technology. Bioresource Technology. 320: 124222 (2021)

    Article  CAS  PubMed  Google Scholar 

  • Bajpai VK, Kang S, Xu H, Lee S-G, Baek K-H, Kang SC. Potential Roles of Essential Oils on Controlling Plant Pathogenic Bacteria Xanthomonas Species: A Review. Plant Pathology Journal. 27: 207-224 (2011)

    Article  CAS  Google Scholar 

  • Barros FFC, Ponezi AN, Pastore GM. Production of biosurfactant by Bacillus subtilis LB5a on a pilot scale using cassava wastewater as substrate. Journal of Industrial Microbiology and Biotechnology. 35: 1071-1078 (2008)

    Article  CAS  PubMed  Google Scholar 

  • Ben Abdallah D, Frikha-Gargouri O, Tounsi S. Bacillus amyloliquefaciens strain 32a as a source of lipopeptides for biocontrol of Agrobacterium tumefaciensstrains. Journal of Applied Microbiology. 119: 196-207 (2015)

    Article  CAS  PubMed  Google Scholar 

  • Ben Gharsa H, Bouri M, Mougou Hamdane A. Schuster C, Leclerque A, Rhouma A. Bacillus velezensis strain MBY2, a potential agent for the management of crown gall disease. Plos one. 16: e0252823 (2021)

  • Bouassida M, Ghazala I, Ellouze-Chaabouni S, Ghribi D. Improved biosurfactant production by Bacillus subtilis SPB1 mutant obtained by random mutagenesis and its application in enhanced oil recovery in a sand system. Journal of Microbiology and Biotechnology. l28: 95–104 (2018)

  • Box GE, Behnken DW. Some new three level designs for the study of quantitative variables. Technometrics. 2: 455-475 (1960)

    Article  Google Scholar 

  • Bryant CM, McClements DJ. Influence of sucrose on NaCl-induced gelation of heat denatured whey protein solutions. Food Research International. 33: 649-653 (2000)

    Article  CAS  Google Scholar 

  • Camilios-Neto D, Meira JA, de Araújo JM, Mitchell DA, Krieger N. Optimization of the production of rhamnolipids by Pseudomonas aeruginosa UFPEDA 614 in solid-state culture. Applied Microbiology and Biotechnology. 81: 441-448 (2008)

    Article  CAS  PubMed  Google Scholar 

  • Cao Y, Xu Z, Ling N, Yuan Y, Yang X, Chen L, Shen B, Shen Q. Isolation and identification of lipopeptides produced by B. subtilis SQR 9 for suppressing Fusarium wilt of cucumber. Scientia Horticulturae. 135: 32–39 (2012)

  • Carolin CF, Kumar PS, Ngueagni PT. A review on new aspects of lipopeptide biosurfactant: Types, production, properties and its application in the bioremediation process. Journal of Hazardous Materials. 407: 124827 (2021)

    Article  Google Scholar 

  • Chen C, Li D, Li R, Shen F, Xiao G, Zhou JJCE. Enhanced biosurfactant production in a continuous fermentation coupled with in situ foam separation. Chemical Engineering Processing-Process Intensification. 159: 108206 (2020)

    Article  Google Scholar 

  • Chen L, Wang X, Liu Y. Contribution of macrolactin in Bacillus velezensis CLA178 to the antagonistic activities against Agrobacterium tumefaciens C58. Archives of Microbiology. 203: 1743-1752 (2021)

    Article  CAS  PubMed  Google Scholar 

  • Cho KM, Math RK, Hong SY, Islam SMA, Mandanna DK, Cho JJ, Yun MG, Kim JM, Yun HD. Iturin produced by Bacillus pumilusHY1 from Korean soybean sauce (kanjang) inhibits growth of aflatoxin producing fungi. Food Control. 20: 402-406 (2009)

    Article  CAS  Google Scholar 

  • Colla LM, Rizzardi J, Pinto MH, Reinehr CO, Bertolin TE, Costa JAV. Simultaneous production of lipases and biosurfactants by submerged and solid-state bioprocesses. Bioresource Technology. 101: 8308-8314 (2010)

    Article  CAS  PubMed  Google Scholar 

  • Damalas CA, Eleftherohorinos IG. Pesticide exposure, safety issues, and risk assessment indicators. International Journal of Environmental Research and Public Health. 8: 1402-1419 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das K, Mukherjee AK. Comparison of lipopeptide biosurfactants production by Bacillus subtilis strains in submerged and solid state fermentation systems using a cheap carbon source: some industrial applications of biosurfactants. Process Biochemistry. 42: 1191-1199 (2007)

    Article  CAS  Google Scholar 

  • Des Grades ZE, der Agrarwissenschaften D, Fakultät HL, Wilhelms RF. 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 06.06.2012 (2012)

  • Ebtsam MM, Abdel-Kawi KA, Khalil MNA. Efficiency of Trichoderma viride and Bacillus subtilis as biocontrol agents against Fusarium solani on tomato plants. Egyptian Journal of Phytopathology. 37: 47-57 (2009)

    Google Scholar 

  • El-Housseiny GS, Aboshanab KM, Aboulwafa MM, Hassouna NA. Rhamnolipid production by a gamma ray-induced Pseudomonas aeruginosa mutant under solid state fermentation. AMB Express. 9: 1-11 (2019)

    Article  CAS  Google Scholar 

  • Escobar MA, Dandekar AM. Agrobacterium tumefaciensas an agent of disease. Trends in Plant Science. 8: 380-386 (2003)

    Article  CAS  PubMed  Google Scholar 

  • Ferreira GB, Evangelista AF, Severo Junior JB, Souza RR, Santana JCC, Tambourgi EB, Jordão E. Partitioning optimization of proteins from Zea mays malt in ATPS PEG 6000/CaCl2. Food Science and Technology. 50: 557-564 (2007)

    CAS  Google Scholar 

  • Foldes T, Banhegyi I, Herpai Z, Varga L, Szigeti J. Isolation of Bacillus strains from the rhizosphere of cereals and in vitro screening for antagonism against phytopathogenic, food‐borne pathogenic and spoilage micro‐organisms. Journal of Applied Microbiology. 89: 840-846 (2000)

    Article  CAS  PubMed  Google Scholar 

  • Frikha-Gargouri O, Ben Abdallah D, Ghorbel I, Charfeddine I, Jlaiel L, Triki MA, Tounsi S. Lipopeptides from a novel Bacillus methylotrophicus 39b strain suppress Agrobacteriumcrown gall tumours on tomato plants. Pest Management Science. 73: 568-574 (2017)

    Article  CAS  PubMed  Google Scholar 

  • Francis F, Sabu A, Nampoothiri KM, Ramachandran S, Ghosh S, Szakacs G, Pandey AJ. Use of response surface methodology for optimizing process parameters for the production of α-amylase by Aspergillus oryzae. Biochemical Engineering Journal. 15: 107-115 (2003)

    Article  CAS  Google Scholar 

  • Franco CM, Michelsen PP, Percy NJ, Conn V, Listiana BE, Moll S, Loria R, Coombs JT. Actinobacterial endophytes for improved crop performance Australas. Plant Pathology. 36: 524-531 (2007)

    Google Scholar 

  • Gakuubi MM, Wagacha JM, Dossaji SF, Wanzala W. Chemical Composition and Antibacterial Activity of Essential Oils ofTagetes minuta (Asteraceae) against Selected Plant Pathogenic Bacteria. International Journal of Microbiology. https://doi.org/10.1155/2016/7352509 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  • Ghribi D, Abdelkefi-Mesrati L, Mnif I, Kammoun R, Ayadi I, Saadaoui I, Maktouf S, Chaabouni-Ellouze S. Investigation of antimicrobial activity and statistical optimization of Bacillus subtilis SPB1 biosurfactant production in solid-state fermentation. Journal of Biomedicine and Biotechnology. 2012: 373682 (2012)

    Article  PubMed  PubMed Central  Google Scholar 

  • Ghribi D, Ellouze-Chaabouni S. Enhancement of Bacillus subtilis lipopeptide biosurfactants production through optimization of medium composition and adequate control of aeration. Biotechnology Research International. 653654 (2011)

  • Ghribi D, Mnif I, Boukedi H, Kammoun R, Ellouze-Chaabouni S. Statistical optimization of low-cost medium for economical production of Bacillus subtilis biosurfactant, a biocontrol agent for the olive moth Prays oleae. African Journal of Microbiological Research. 5: 4927-4936 (2011)

    Google Scholar 

  • Ghribi D, Zouari N, Trigui W, Jaoua S. Use of sea water as salts source in starch-and soya bean-based media, for the production of Bacillus thuringiensis bioinsecticides. Process Biochemistry. 42: 374-378 (2007)

    Article  CAS  Google Scholar 

  • Goes AP, Sheppard JD. Effect of surfactants on α-amylase production in a solid substrate fermentation process. Journal of Chemical Technology and Biotechnology. 74: 709-712 (1999)

    Article  CAS  Google Scholar 

  • Hammami I, Rhouma A, Jaouadi B, Rebai A, Xavier N. Optimization and biochemical characterization of a bacteriocin from a newly isolated Bacillus subtilis strain 14B for biocontrol of Agrobacterium spp. Strains. Letters in Applied Microbiology. 48: 253-260 (2009)

    Article  CAS  PubMed  Google Scholar 

  • Hammami I, Triki MA, Rebai A. Purification and characterization of the novel bacteriocin Back IH7 with antifungal and antibacterial properties. Journal of Plant Pathology. 93: 443-445 (2011)

    Google Scholar 

  • Hölker U, Höfer M, Lenz JJ. Biotechnological advantages of laboratory-scale solid-state fermentation with fungi. Applied Microbiology and Biotechnology. 64: 175-186 (2004)

    Article  PubMed  Google Scholar 

  • Hu LB, Shi ZQ, Zhang T, Yang ZM. Fengycin antibiotics isolated from B-FS01 culture inhibit the growth of Fusarium moniliforme Sheldon ATCC38932. FEMS Microbiology Letters. 272: 91-98 (2007)

    Article  CAS  PubMed  Google Scholar 

  • Joshi S, Bharucha C, Jha S, Yadav S, Nerurkar A, Desai AJ. Biosurfactant production using molasses and whey under thermophilic conditions. Bioresource Technology. 99: 195-199 (2008)

    Article  CAS  PubMed  Google Scholar 

  • Kim KM, Lee JY, Kim CK, Kang JS. Isolation and Characterization of Surfactin Produced by Bacillus polyfermenticusKJS-2. Archives of Pharmaceutical Research. 32: 711-715 (2009)

    Article  CAS  Google Scholar 

  • Kita N, Ohya T, Uekusa H, Nomura K, Manago M, Shoda M. Biological control of damping-off of tomato seedlings and cucumber Phomopsis root rot by Bacillus subtilis RB14-C. Japanese Agriculture Research Quarterly. 39: 109-114 (2005)

    Article  CAS  Google Scholar 

  • Kreling NE, Simon V, Fagundes VD, Thomé A, Colla LM. Simultaneous Production of Lipases and Biosurfactants in Solid-State Fermentation and Use in Bioremediation. Journal of Environmental Engineering. 146 (2020)

  • Kriaa M, Kammoun R. Producing Aspergillus tubingensis CTM507 glucose oxidase by solid state fermentation versus submerged fermentation: process optimization and enzyme stability by an intermediary metabolite in relation with diauxic growth. Journal of Chemical Technology and Biotechnology. 91: 1540-1550 (2016)

    Article  CAS  Google Scholar 

  • Kulkarni SS,Nene SN, Joshi KS. A comparative study of production of hydrophobin like proteins (HYD-LPs) in submerged liquid and solid state fermentation from white rot fungus Pleurotus ostreatus. Biocatalysis and Agricultural Biotechnology. 23: 101440 (2020)

    Article  Google Scholar 

  • Kuo CY. Optimization of cultivation conditions for iturin A production by Bacillus subtilis using solid state fermentation. M.S. thesis, Da-Yeh University, Taiwan (2006)

  • Leclère V, Béchet M, Adam A, Guez J-S, Wathelet B, Ongena M, Thonart P, Gancel F, Chollet-Imbert M, Jacques P. Mycosubtilin overproduction by Bacillus subtilis BBG100 enhances the organism’s antagonistic and biocontrol activities. Applied and Environmental Microbiology. 71: 4577-4584 (2005)

    Article  PubMed  PubMed Central  Google Scholar 

  • Leelasuphakul W, Hemmanee P, Chuenchitt S. Growth inhibitory properties of Bacillus subtilis strains and their metabolites against the green mold pathogen (Penicillium digitatum Sacc.) of citrus fruit. Postharvest Biology and Technology. 48: 113–121 (2008)

  • Li L, Ma MC, Huang R, Qu Q, Li GH, Zhou JW, Zhang KQ, Lu KP, Niu XM, Luo J. Induction of chlamydospore formation in Fusarium by cyclic lipopeptide antibiotics from Bacillus subtilis C2. Journal of Chemical Ecology. 38: 966-974 (2012)

    Article  PubMed  Google Scholar 

  • Liu K, Sun Y, Cao M, Wang J, Lu JR, Xu H. Rational design properties and applications of biosurfactants: a short review of recent advances. Current Opinion in Colloid and Interfacial Science. 45: 57-67 (2012)

    Article  Google Scholar 

  • Malviya D, Sahu PK, Singh UB, Paul S, Gupta A, Gupta AR, Singh S, Kumar M, Paul D, Rai JP, Singh HV, Brahmaprakash GP. Lesson from Ecotoxicity: Revisiting the Microbial Lipopeptides for the Management of Emerging Diseases for Crop Protection. International Journal of Environmental Research and Public Health. 17: 1434 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mathieu D. Phan-Tan-Lu R. Logiciel Nemrod: LPRAI, Marseille (2000)

  • Matsumoto Y, Saucedo-Castañeda G, Revah S, Shirai K. Production of β-N-acetyl hexosaminidase of Verticillium lecanii by solid state and submerged fermentations utilizing shrimp waste silage as substrate and inducer. Process Biochemistry. 39: 665-671 (2004)

    Article  CAS  Google Scholar 

  • McKeen C, Reily C, Pusey P. Production and partial characterization of antifungal substances antagonistic to Monilia fructicola from Bacillus subtilis. Phytopathology. 76: 136–139 (1986)

    Article  CAS  Google Scholar 

  • Mizumoto S, Hirai M, Shoda M. Production of lipopeptide antibiotic iturin A using soybean curd residue cultivated with Bacillus subtilis in solid-state fermentation. Applied Microbiology and Biotechnology. 72: 869-875 (2006)

    Article  CAS  PubMed  Google Scholar 

  • Mnif I, Bouallegue A, Bouassida M, Ghribi D. Surface properties and heavy metals chelation of lipopeptides biosurfactants produced from date lour by Bacillus subtilis ZNI5: optimized production for application in bioremediation. Bioprocess and Biosystems Engineering. https://doi.org/10.1007/s00449-021-02635-2 (2021a)

    Article  PubMed  Google Scholar 

  • Mnif I, Rajhi H, Bouallegue A, Trabelsi N, Ghribi D. Characterization of Lipopeptides Biosurfactants Produced by a Newly Isolated Strain Bacillus subtilis ZNI5: Potential Environmental Application. Journal of Polymers and The Environment. https://doi.org/10.1007/s10924-021-02361-6 (2021b)

    Article  Google Scholar 

  • Mnif I, Bouallegue A, Mekki S, Ghribi D. Valorization of date juice by the production of lipopeptide biosurfactants by a Bacillus mojavensis BI2 strain: bioprocess optimization by response surface methodology and study of surface activities. Bioprocess and Biosystems Engineering. https://doi.org/10.1007/s00449-021-02606-7 (2021c)

    Article  PubMed  Google Scholar 

  • Mnif I, Elleuch M, Chaabouni ES, Ghribi D. Bacillus subtilis SPB1 biosurfactant: Production optimization and insecticidal activity against the carob moth Ectomyelois ceratoniae. Crop Protection. 50: 66-72 (2013)

    Article  CAS  Google Scholar 

  • Mnif I, Ellouze-Chaabouni S, Ghribi D. Optimization of the Nutritional Parameters for Enhanced Production of B. subtilis SPB1 Biosurfactant in Submerged Culture Using Response Surface Methodology. Biotechnology Research International. Article ID 795430, 8 https://doi.org/10.1155/2012/795430 (2012)

  • Mnif I, Grau-Campistany A, Coronel-León J, Hammami I, Triki MA, Manresa A, Ghribi D. Purification and identification of Bacillus subtilis SPB1 lipopeptide biosurfactant exhibiting antifungal activity against Rhizoctonia bataticola and Rhizoctonia solani. Environmental Science and Pollution Research International. 23: 6690-6699 (2016)

    Article  CAS  PubMed  Google Scholar 

  • Mnif I, Hammami I, Triki M-A, Cheffi Azabou M, Ellouze-Chaabouni S, Ghribi D. Antifungal efficiency of a lipopeptide biosurfactant derived from Bacillus subtilis SPB1 versus the phytopathogenic fungus, Fusarium solani. Environmental Science and Pollution Research. https://doi.org/10.1007/s11356-015-5005-6 (2015)

    Article  PubMed  Google Scholar 

  • Montealegre JR, Errera R, Velásquez JC, Silva P, Besoaín X, Pérez LM. Biocontrol of root and crown rot in tomatoes under greenhouse conditions using Trichoderma harzianum and Paenibacillus lentimorbus, Additional effect of solarization. Electronic Journal of Biotechnology. 8: 250-257 (2005)

    Article  Google Scholar 

  • Mora I, Cabrefiga J, Montesinos E. Cyclic Lipopeptide Biosynthetic Genes and Products, and Inhibitory Activity of Plant-Associated Bacillus against Phytopathogenic Bacteria. PLOS ONE. 10: e0127738 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  • Mukherjee S, Das P, Sen R. Towards commercial production of microbial surfactants. Trends in Biotechnology. 24: 509-515 (2006)

    Article  CAS  PubMed  Google Scholar 

  • Nihorimbere V, Ongena M, Cawoy H, Brostaux Y, Kakana P, Jourdan E, Thonart P. Beneficial effects of Bacillus subtilis on field grown tomato in Burundi: reduction of local Fusarium disease and growth promotion. African Journal of Microbiological Research. 4: 1135-1142 (2010)

    Google Scholar 

  • Ohno A, Ano T, Shoda M. Production of a lipopeptide antibiotic surfactin by recombinant Bacillus subtilis in solid state fermentation. Biotechnology and Bioengineering. 47: 209-214 (1995)

    Article  CAS  PubMed  Google Scholar 

  • Ohno A, Ano T, Shoda MJ. Production of the antifungal peptide antibiotic iturin by Bacillus subtilis NB22 in solid state fermentation. Biochemical Engineering. 75: 23-27 (1993)

    CAS  Google Scholar 

  • Ongena M, Jacques P. Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends in Microbiology. 16: 115-125 (2008)

    Article  CAS  PubMed  Google Scholar 

  • Pearson D The chemical analysis of foods. Longman Group Ltd (1976)

  • Penyalver R, Lopez MM. Cocolonization of the rhizosphere by pathogenic agrobacterium strains and nonpathogenic strains K84 and K1026, used for crown gall biocontrol. Applied and Environmental Microbiology. 65: 1936-1940 (1999)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira JF, Gudiña EJ, Costa R, Vitorino R, Teixeira JA, Coutinho JA, Rodrigues LR. Optimization and characterization of biosurfactant production by Bacillus subtilis isolates towards microbial enhanced oil recovery applications. Fuel. 111: 259-268 (2013)

    Article  CAS  Google Scholar 

  • Phae C, Shoda M, Kubota N. Suppressive effect of Bacillus subtilis and it’s products on phytopathogenic microorganisms. Journal of Fermentation and Bioengineering. 69: 1–7 (1990)

  • Raveau R, Fontaine J, Lounès-Hadj AS. Essential Oils as Potential Alternative Biocontrol Products against Plant Pathogens and Weeds: A Review. Foods. 9: 365 (2020) https://doi.org/10.3390/foods9030365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rebib H, Hedi A, Rousset M, Boudabous A, Limam F, Sadfi-Zouaoui N. Biological control of Fusarium foot rot of wheat using fengycin-producing Bacillus subtilis isolated from salty soil. African Journal of Biotechnology. 11: 8464-8475 (2012)

    CAS  Google Scholar 

  • Rodríguez A, Gea T, Sánchez A, Font X. Agro-wastes and Inert Materials as Supports for the Production of Biosurfactants by Solid-state Fermentation Waste and Biomass Valorization. 1963–1976 (2020)

  • Sen R, Swaminathan T. Application of response-surface methodology to evaluate the optimum environmental conditions for the enhanced production of surfactin. Applied Microbiology and Biotechnology. 47: 358-363 (1997)

    Article  CAS  Google Scholar 

  • Sidney W. Official methods of analysis of the association of official analytical chemists. Register for the 2021 AOAC Annual Meeting, August 27 - September 2, 2021 in Boston, MA; 1984 (1984)

  • Singh A, Van Hamme JD, Ward OP. Surfactants in microbiology and biotechnology: Part 2; Application aspects. Biotechnology Advancements. 25: 99-121 (2007)

    Article  CAS  Google Scholar 

  • Smibert R, Krieg N, Gerhardt P, Murray R, Wood WJW. DC: American Society for Microbiology. Methods for General and Molecular Bacteriology. pp. 607–654 (1994)

  • Soylu EM, Kurt S, Soylu S. In vitro and in vivo antifungal activities of the essential oils of various plants against tomato grey mould disease agent Botrytis cinerea. International Journal of Food Microbiology. 143: 183-189 (2010)

    Article  CAS  PubMed  Google Scholar 

  • Tanyildizi MS, Özer D, Elibol M. Production of bacterial α-amylase by B. amyloliquefaciens under solid substrate fermentation. Biochemical Engineering Journal. 37: 294–297 (2007)

  • Thomas L, Larroche C, Pandey A. Current developments in solid-state fermentation. Biochemical Engineering Journal. 8: 146-161 (2013)

    Article  Google Scholar 

  • Todorova S, Kozhuharova L. Characteristics and antimicrobial activity of Bacillus subtilis strains isolated from soil. World Journal of Microbiology and Biotechnology. 26: 1207-1216 (2010)

    Article  CAS  PubMed  Google Scholar 

  • Trigui M, Ben Hsouna A, Hammami I, Culioli G, Ksantini M, Tounsi S, Jaoua S. Efficacy of Lawsonia inermis leaves extract and its phenolic compounds against olive knot and crown gall diseases. Crop Protection. 45: 83-88 (2013)

    Article  CAS  Google Scholar 

  • Triki MA, Hammami I, Krid Hadj-Taieb S, Daami-Remadi M, Mseddi A, El Mahjoub M, Gdoura R, Khammasy N. Biological control of atypical pink rot disease of potato in Tunisia. Global Science Books Pesticide Technology. 6:60-64 (2012)

    Google Scholar 

  • Van Hamme JD, Singh A, Ward OP. Physiological aspects. Part 1 in a series of papers devoted to surfactants in microbiology and biotechnology. Biotechnology Advances. 24: 604–620 (2006)

  • Wang J, Sun M, Liu Z, Yu Z. Co-producing lipopeptides and poly-γ-glutamic acid by solid-state fermentation of Bacillus subtilis using soybean and sweet potato residues and its biocontrol and fertilizer synergistic effects. Bioresource Technology. 99: 3318-3323 (2008)

    Article  CAS  PubMed  Google Scholar 

  • Xu H, Sun L-P, Shi Y-Z, Wu Y-H, Zhang B, Zhao D-Q. Optimization of cultivation conditions for extracellular polysaccharide and mycelium biomass by Morchella esculenta. Biochemical Engineering Journal. 39(1): 66-73 (2008)

    Article  CAS  Google Scholar 

  • Xu JX, Li ZY, Lv X, Yan H, Zhou GY, Cao LX, Yang Q, He YH. Isolation and characterization of Bacillus subtilis strain 1-L-29, an endophytic bacteria from Camellia oleifera with antimicrobial activity and efficient plant-root colonization. PLoS One. 15: e0232096 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yangui T, Sayadi S, Dhouib A. Sensitivity of Pectobacterium carotovorum to hydroxytyrosol-rich extracts and their effect on the development of soft rot in potato tubers during storage. Crop Protection. 53: 52-57 (2013)

    Article  CAS  Google Scholar 

  • Zoina A, Raio A. Susceptibility of some peach rootstocks to crown gall. Journal of Plant Pathology. 81: 181-187 (1999)

    Google Scholar 

  • Zouari R, Ben Abdallah-Kolsi R, Hamden K, Feki AE, Chaabouni K, Makni-Ayadi F, Sallemi F, Ellouze-Chaabouni S, Ghribi Aydi D. Assessment of the antidiabetic and antilipidemic properties of Bacillus subtilis SPB1 biosurfactant in alloxan induced diabetic rats. Biopolymers. 104: 764-774 (2015c)

    Article  CAS  PubMed  Google Scholar 

  • Zouari R, Chaabouni ES, Ghribi D. Optimization of Bacillus subtilis SPB1 Biosurfactant Production Under Solid-state Fermentation Using By-products of a Traditional Olive Mill Factory. Achievements in Life Science. 8: 162-169 (2015b)

    Article  Google Scholar 

  • Zouari R, Chaabouni ES, Ghribi D. Use of butter milk and poultry-transforming wastes for enhanced production of bacillus subtilis SPB1 biosurfactant in submerged fermentation. Journal of Microbiology and Biotechnology and Food Science. https://doi.org/10.15414/jmbfs.2015.4.5.462-46 (2015a)

    Article  Google Scholar 

Download references

Acknowledgements

The Ministry of Higher Education, Scientific Research, and Technology of Tunisia provided grants in support of this work. The authors want to sincerely thank Moulin TRIKI Group for their support.

Funding

The work is funded by the Ministry of Higher Education and Scientific Research and the Higher Education-Tunisia-Protection of Plants Researcher.

Author information

Authors and Affiliations

Authors

Contributions

The first author of the present manuscript Dr MB realized and writes this paper. The second author Dr IM helped in the redaction of the paper. Dr IH helped in the realization of the experiences. Professor MAT and Professor DG helped in the elaboration of the plan of this work and corrected this paper.

Corresponding author

Correspondence to Inès Mnif.

Ethics declarations

Conflict of interest

There is no conflict of interest to be declared.

Ethical approval

The studies were conducted in accordance with the ethical standards of the institution or practice at which. They don’t involve the use of animals.

Consent to participate

All individuals taking part in the study gave their informed consent.

Consent to publish

All the authors give the Publisher the permission to publish the Work in Food Science and Biotechnology.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) 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

Bouassida, M., Mnif, I., Hammami, I. et al. Bacillus subtilis SPB1 lipopeptide biosurfactant: antibacterial efficiency against the phytopathogenic bacteria Agrobacterium tumefaciens and compared production in submerged and solid state fermentation systems. Food Sci Biotechnol 32, 1595–1609 (2023). https://doi.org/10.1007/s10068-023-01274-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10068-023-01274-5

Keywords

Navigation