[en] Apple scab is an important disease conventionally controlled by chemical fungicides, which should be replaced by more environmentally friendly alternatives. One of these alternatives could be the use of lipopeptides produced by Bacillus subtilis. The objective of this work is to study the action of the three families of lipopeptides and different mixtures of them in vitro and in vivo against Venturia inaequalis. Firstly, the antifungal activity of mycosubtilin/surfactin and fengycin/surfactin mixtures was determined in vitro by measuring the median inhibitory concentration. Then, the best lipopeptide mixture ratio was produced using Design of Experiment (DoE) to optimize the composition of the culture medium. Finally, the lipopeptides mixtures efficiency against V. inaequalis was assessed in orchards as well as the evaluation of the persistence of lipopeptides on apple. In vitro tests show that the use of fengycin or mycosubtilin alone is as effective as a mixture, with the 50-50% fengycin/surfactin mixture being the most effective. Optimization of culture medium for the production of fengycin/surfactin mixture shows that the best composition is glycerol coupled with glutamic acid. Finally, lipopeptides showed in vivo antifungal efficiency against V. inaequalis regardless of the mixture used with a 70% reduction in the incidence of scab for both mixtures (fengycin/surfactin or mycosubtilin/surfactin). The reproducibility of the results over the two trial campaigns was significantly better with the mycosubtilin/surfactin mixture. The use of B. subtilis lipopeptides to control this disease is very promising.
Disciplines :
Microbiology
Author, co-author :
Leconte, Aline ; Université de Liège - ULiège > TERRA Research Centre ; UMRt BioEcoAgro 1158-INRAE, Equipe Métabolites Secondaires D'origine Microbienne, Institut Charles Viollette, Université de Lille, F-59000 Lille, France ; JUNIA, UMRt BioEcoAgro 1158-INRAE, Equipe Métabolites Spécialisés D'origine Végétale, Institut Charles Viollette, F-59000 Lille, France
Tournant, Ludovic; FREDON Hauts-de-France-265 rue Becquerel, F-62750 Loos-en-Gohelle, France
Muchembled, Jérôme; JUNIA, UMRt BioEcoAgro 1158-INRAE, Equipe Métabolites Spécialisés D'origine Végétale, Institut Charles Viollette, F-59000 Lille, France
Paucellier, Jonathan; UMRt BioEcoAgro 1158-INRAE, Equipe Métabolites Secondaires D'origine Microbienne, Institut Charles Viollette, Université de Lille, F-59000 Lille, France
Héquet, Arnaud; Lipofabrik SAS, 917 rue des Saules, F-59343 Lesquin, France
Deracinois, Barbara ; UMRt BioEcoAgro 1158-INRAE, Equipe Métabolites Secondaires D'origine Microbienne, Institut Charles Viollette, Université de Lille, F-59000 Lille, France
Deweer, Caroline ; JUNIA, UMRt BioEcoAgro 1158-INRAE, Equipe Métabolites Spécialisés D'origine Végétale, Institut Charles Viollette, F-59000 Lille, France
Krier, François ; UMRt BioEcoAgro 1158-INRAE, Equipe Métabolites Secondaires D'origine Microbienne, Institut Charles Viollette, Université de Lille, F-59000 Lille, France
Deleu, Magali ; Université de Liège - ULiège > TERRA Research Centre > Chimie des agro-biosystèmes
Oste, Sandrine; FREDON Hauts-de-France-265 rue Becquerel, F-62750 Loos-en-Gohelle, France
Jacques, Philippe ; Université de Liège - ULiège > TERRA Research Centre ; Lipofabrik SAS, 917 rue des Saules, F-59343 Lesquin, France
Coutte, François ; UMRt BioEcoAgro 1158-INRAE, Equipe Métabolites Secondaires D'origine Microbienne, Institut Charles Viollette, Université de Lille, F-59000 Lille, France ; Lipofabrik SAS, 917 rue des Saules, F-59343 Lesquin, France
Language :
English
Title :
Assessment of Lipopeptide Mixtures Produced by Bacillus subtilis as Biocontrol Products against Apple Scab (Venturia inaequalis).
ERDF - European Regional Development Fund [BE] SME Instrument H2020
Funding text :
These studies were carried out with the financial support of the ERDF (European Regional Development Fund) and the Hauts-de-France Region, as part of the Smartbiocontrol programme (BioProd and BioProtect) included in the INTERREG V France–Walloon–Vlaanderen programme, the ALIBIOTECH programme and the AgriBioPOM project financed by the call for projects on agricultural systems and the environment in the Hauts-de-France Region and for Lipofabrik in 2019 and 2020 by the grant agreement of the SME instrument no. 849713 under the European Union’s Horizon 2020 research and innovation programme.The authors would like to thank students from Polytech-lille (Sarah Berrada, Alexis Delrue, Nadine Halabi, Sarah Klai, Julia Morieux, Raphaël Leroux, Margot Thiblet et Mélissa Legrand) for their participation in the optimization Landy medium for the production of lipopeptides by B. subtilis ATCC 21332 and for the validation of QuEChERS method, as well as Emeline Bertrand from Institut Charles Viollette and Thomas Delhez from University of Liège for their help in lipopeptide production. DoE and mass spectrometry analysis were and performed on the REALCAT platform, funded by a French governmental subsidy managed by the French National Research Agency (ANR) within the framework of the “Future Investments’ program (ANR-11- EQPX-0037). The Hauts-de-France region, FEDER, Ecole Centrale de Lille, and Centrale Initiatives Foundation are also warmly acknowledged for their financial contributions to the acquisition of the REALCAT platform equipment.
MacHardy W.E. Apple Scab: Biology, Epidemiology, and Management APS Press St. Paul, MN, USA 1996
Holb I.J. Heijne B. Withagen J.C.M. Gáll J.M. Jeger M.J. Analysis of Summer Epidemic Progress of Apple Scab at Different Apple Production Systems in the Netherlands and Hungary Phytopathology 2005 95 1001 1020 10.1094/PHYTO-95-1001 18943298
Bowen J.K. Mesarich C.H. Bus V.G.M. Beresford R.M. Plummer K.M. Templeton M.D. Venturia inaequalis: The Causal Agent of Apple Scab: Venturia inaequalis Mol. Plant Pathol. 2011 12 105 122 10.1111/j.1364-3703.2010.00656.x 21199562
Chatzidimopoulos M. Lioliopoulou F. Sotiropoulos T. Vellios E. Efficient Control of Apple Scab with Targeted Spray Applications Agronomy 2020 10 217 10.3390/agronomy10020217
Cordero-Limon L. Shaw M.W. Passey T.A. Robinson J.D. Xu X. Cross-resistance between myclobutanil and tebuconazole and the genetic basis of tebuconazole resistance in Venturia inaequalis Pest Manag. Sci. 2020 77 844 850 10.1002/ps.6088
Shirane N. Takenaka H. Ueda K. Hashimoto Y. Katoh K. Ishii H. Sterol analysis of DMI-resistant and -sensitive strains of Venturia inaequalis Phytochemistry 1996 41 1301 1308 10.1016/0031-9422(95)00787-3
Gao L. Berrie A. Yang J. Xu X. Within- and between-Orchard Variability in the Sensitivity of Venturia inaequalis to Myclobutanil, a DMI Fungicide, in the UK Pest Manag. Sci. 2009 65 1241 1249 10.1002/ps.1816
Li X. Li H. Yu Z. Gao L. Yang J. Investigating the sensitivity of Venturia inaequalis isolates to difenoconazole and pyraclostrobin in apple orchards in China Eur. J. Plant Pathol. 2021 161 207 217 10.1007/s10658-021-02316-6
Villani S.M. Biggs A.R. Cooley D.R. Raes J.J. Cox K.D. Prevalence of Myclobutanil Resistance and Difenoconazole Insensitivity in Populations of Venturia inaequalis Plant Dis. 2015 99 1526 1536 10.1094/PDIS-01-15-0002-RE
Xu X.-M. Gao L.-Q. Yang J.-R. Are Insensitivities of Venturia inaequalis to Myclobutanil and Fenbuconazole Correlated? Crop Prot. 2010 29 183 189 10.1016/j.cropro.2009.07.002
Yaegashi H. Hirayama K. Akahira T. Ito T. Point mutation in CYP51A1 of Venturia inaequalis is associated with low sensitivity to sterol demethylation inhibitors J. Gen. Plant Pathol. 2020 86 245 249 10.1007/s10327-020-00924-4
European Food Safety Conclusion on the Peer Review of the Pesticide Risk Assessment of Confirmatory Data Submitted for the Active Substance Copper (I), Copper (II) Variants Namely Copper Hydroxide, Copper Oxychloride, Tribasic Copper Sulfate, Copper (I) Oxide, Bordeaux Mixture EFSA J. 2013 11 3235
Coutte F. Niehren J. Dhali D. John M. Versari C. Jacques P. Modeling Leucine’s Metabolic Pathway and Knockout Prediction Improving the Production of Surfactin, a Biosurfactant from Bacillus subtilis Biotechnol. J. 2015 10 1216 1234 10.1002/biot.201400541 26220295
Tan W. Yin Y. Wen J. Increasing fengycin production by strengthening the fatty acid synthesis pathway and optimizing fermentation conditions Biochem. Eng. J. 2021 177 108235 10.1016/j.bej.2021.108235
Jiang J. Han M. Fu S. Du J. Wang S. Zhang H. Li W. Enhanced Production of Iturin A-2 Generated from Bacillus velezensis T701 and the Antitumor Activity of Iturin A-2 against Human Gastric Carcinoma Cells Int. J. Pept. Res. Ther. 2021 28 27 10.1007/s10989-021-10340-7
Zhao X. Han Y. Tan X.-Q. Wang J. Zhou Z.-J. Optimization of antifungal lipopeptide production from Bacillus sp. BH072 by response surface methodology J. Microbiol. 2014 52 324 332 10.1007/s12275-014-3354-3 24535741
Mizumoto S. Shoda M. Medium optimization of antifungal lipopeptide, iturin A, production by Bacillus subtilis in solid-state fermentation by response surface methodology Appl. Microbiol. Biotechnol. 2007 76 101 108 10.1007/s00253-007-0994-9
Akpa E. Jacques P. Wathelet B. Paquot M. Fuchs R. Budzikiewicz H. Thonart P. Influence of Culture Conditions on Lipopeptide Production by Bacillus subtilis Appl. Biochem. Biotechnol. 2001 91 551 561 10.1385/ABAB:91-93:1-9:551
Huang X. Lu Z. Zhao H. Bie X. Lü F. Yang S. Antiviral Activity of Antimicrobial Lipopeptide from Bacillus subtilis fmbj Against Pseudorabies Virus, Porcine Parvovirus, Newcastle Disease Virus and Infectious Bursal Disease Virus in Vitro Int. J. Pept. Res. Ther. 2006 12 373 377 10.1007/s10989-006-9041-4
Chen M. Wang J. Zhu Y. Liu B. Yang W. Ruan C. Antibacterial activity against Ralstonia solanacearum of the lipopeptides secreted from the Bacillus amyloliquefaciens strain FJAT-2349 J. Appl. Microbiol. 2019 126 1519 1529 10.1111/jam.14213
Zhao H. Shao D. Jiang C. Shi J. Li Q. Huang Q. Rajoka M.S.R. Yang H. Jin M. Biological activity of lipopeptides from Bacillus Appl. Microbiol. Biotechnol. 2017 101 5951 5960 10.1007/s00253-017-8396-0
Moyne A.-L. Shelby R. Cleveland T.E. Tuzun S. Bacillomycin D: An iturin with antifungal activity against Aspergillus flavus J. Appl. Microbiol. 2001 90 622 629 10.1046/j.1365-2672.2001.01290.x 11309075
Desmyttere H. Deweer C. Muchembled J. Sahmer K. Jacquin J. Coutte F. Jacques P. Antifungal Activities of Bacillus subtilis Lipopeptides to Two Venturia inaequalis Strains Possessing Different Tebuconazole Sensitivity Front. Microbiol. 2019 10 2327 10.3389/fmicb.2019.02327 31695685
Jacques P. Surfactin and Other Lipopeptides from Bacillus Spp Biosurfactants Soberón-Chávez G. Microbiology Monographs Springer Berlin/Heidelberg, Germany 2011 Volume 20 57 91
Krishnan N. Velramar B. Velu R.K. Investigation of antifungal activity of surfactin against mycotoxigenic phytopathogenic fungus Fusarium moniliforme and its impact in seed germination and mycotoxicosis Pestic. Biochem. Physiol. 2019 155 101 107 10.1016/j.pestbp.2019.01.010 30857619
Mnif I. Ghribi G. Lipopeptide Surfactants: Production, Recovery and Pore Forming Capacity Peptides 2015 71 100 112
Liu J. Hagberg I. Novitsky L. Hadj-Moussa H. Avis T.J. Interaction of antimicrobial cyclic lipopeptides from Bacillus subtilis influences their effect on spore germination and membrane permeability in fungal plant pathogens Fungal Biol. 2014 118 855 861 10.1016/j.funbio.2014.07.004
Deravel J. Lemière S. Coutte F. Krier F. Van Hese N. Béchet M. Sourdeau N. Höfte M. Leprêtre A. Jacques P. Mycosubtilin and Surfactin Are Efficient, Low Ecotoxicity Molecules for the Biocontrol of Lettuce Downy Mildew Appl. Microbiol. Biotechnol. 2014 98 6255 6264 10.1007/s00253-014-5663-1
Ben Ayed H. Nasri R. Jemil N. Ben Amor I. Gargouri J. Hmidet N. Nasri M. Acute and sub-chronic oral toxicity profiles of lipopeptides from Bacillus mojavensis A21 and evaluation of their in vitro anticoagulant activity Chem. Interactions 2015 236 1 6 10.1016/j.cbi.2015.04.018
Mnif I. Ghribi D. Review lipopeptides biosurfactants: Mean classes and new insights for industrial, biomedical, and environmental applications Biopolymers 2015 104 129 147 10.1002/bip.22630
Cawoy H. Mariutto M. Henry G. Fisher C. Vasilyeva N. Thonart P. Dommes J. Ongena M. Plant Defense Stimulation by Natural Isolates of Bacillus Depends on Efficient Surfactin Production Mol. Plant-Microbe Interact. 2014 27 87 100 10.1094/MPMI-09-13-0262-R
Ongena M. Jacques P. Bacillus lipopeptides: Versatile weapons for plant disease biocontrol Trends Microbiol. 2008 16 115 125 10.1016/j.tim.2007.12.009
Deleu M. Paquot M. Nylander T. Effect of Fengycin, a Lipopeptide Produced by Bacillus subtilis, on Model Biomembranes Biophys. J. 2008 94 2667 2679 10.1529/biophysj.107.114090
Falardeau J. Wise C. Novitsky L. Avis T.J. Ecological and Mechanistic Insights Into the Direct and Indirect Antimicrobial Properties of Bacillus subtilis Lipopeptides on Plant Pathogens J. Chem. Ecol. 2013 39 869 878 10.1007/s10886-013-0319-7 23888387
Roy A. Mahata D. Paul D. Korpole S. Franco O.L. Mandal S.M. Purification, biochemical characterization and self-assembled structure of a fengycin-like antifungal peptide from Bacillus thuringiensis strain SM1 Front. Microbiol. 2013 4 332 10.3389/fmicb.2013.00332 24312083
Gao L. Han J. Liu H. Qu X. Lu Z. Bie X. Plipastatin and surfactin coproduction by Bacillus subtilis pB2-L and their effects on microorganisms Antonie Van Leeuwenhoek 2017 110 1007 1018 10.1007/s10482-017-0874-y
Fan H. Ru J. Zhang Y. Wang Q. Li Y. Fengycin produced by Bacillus subtilis 9407 plays a major role in the biocontrol of apple ring rot disease Microbiol. Res. 2017 199 89 97 10.1016/j.micres.2017.03.004 28454713
Singh P. Xie J. Qi Y. Qin Q. Jin C. Wang B. Fang W. A Thermotolerant Marine Bacillus amyloliquefaciens S185 Producing Iturin A5 for Antifungal Activity against Fusarium oxysporum f. Sp. Cubense Mar. Drugs 2021 19 516 10.3390/md19090516 34564178
Farzaneh M. Shi Z.-Q. Ahmadzadeh M. Hu L.-B. Ghassempour A. Inhibition of the Aspergillus flavus Growth and Aflatoxin B1 Contamination on Pistachio Nut by Fengycin and Surfactin-Producing Bacillus subtilis UTBSP1 Plant Pathol. J. 2016 32 209 215 10.5423/PPJ.OA.11.2015.0250
Mejri S. Siah A. Coutte F. Magnin-Robert M. Randoux B. Tisserant B. Krier F. Jacques P. Reignault P. Halama P. Biocontrol of the wheat pathogen Zymoseptoria tritici using cyclic lipopeptides from Bacillus subtilis Environ. Sci. Pollut. Res. 2017 25 29822 29833 10.1007/s11356-017-9241-9
Toral L. Rodríguez M. Béjar V. Sampedro I. Antifungal Activity of Lipopeptides From Bacillus XT1 CECT 8661 Against Botrytis cinerea Front. Microbiol. 2018 9 1315 10.3389/fmicb.2018.01315
Fickers P. Leclère V. Guez J.-S. Béchet M. Coucheney F. Joris B. Jacques P. Temperature dependence of mycosubtilin homologue production in Bacillus subtilis ATCC6633 Res. Microbiol. 2008 159 449 457 10.1016/j.resmic.2008.05.004
Fahim S. Dimitrov K. Gancel F. Vauchel P. Jacques P. Nikov I. Impact of energy supply and oxygen transfer on selective lipopeptide production by Bacillus subtilis BBG21 Bioresour. Technol. 2012 126 1 6 10.1016/j.biortech.2012.09.019 23073082
Coutte F. Lecouturier D. Yahia S.A. Leclère V. Béchet M. Jacques P. Dhulster P. Production of surfactin and fengycin by Bacillus subtilis in a bubbleless membrane bioreactor Appl. Microbiol. Biotechnol. 2010 87 499 507 10.1007/s00253-010-2504-8 20221757
Yaseen Y. Gancel F. Béchet M. Drider D. Jacques P. Study of the correlation between fengycin promoter expression and its production by Bacillus subtilis under different culture conditions and the impact on surfactin production Arch. Microbiol. 2017 199 1371 1382 10.1007/s00203-017-1406-x 28735377
Ghribi D. Ellouze-Chaabouni S. Enhancement of Bacillus subtilis Lipopeptide Biosurfactants Production through Optimization of Medium Composition and Adequate Control of Aeration Biotechnol. Res. Int. 2011 2011 1 6 10.4061/2011/653654
Etchegaray A. Coutte F. Chataigné G. Béchet M. dos Santos R.H.Z. Leclère V. Jacques P. Production of Bacillus amyloliquefaciens OG and Its Metabolites in Renewable Media: Valorisation for Biodiesel Production and p-Xylene Decontamination Can. J. Microbiol. 2017 63 46 60 10.1139/cjm-2016-0288 27912317
Jacques P. Hbid C. Destain J. Razafindralambo H. Paquot M. De Pauw E. Thonart P. Optimization of Biosurfactant Lipopeptide Production from Bacillus Subtilis S499 by Plackett-Burman Design Twentieth Symposium on Biotechnology for Fuels and Chemicals: Presented as Volumes 77–79 of Applied Biochemistry and Biotechnology Davison B.H. Finkelstein M. Applied Biochemistry and Biotechnology Humana Press Totowa, NJ, USA 1999 223 233
Motta Dos Santos L.F. Coutte F. Ravallec R. Dhulster P. Tournier-Couturier L. Jacques P. An Improvement of Surfactin Production by Bacillus subtilis BBG131 Using Design of Experiments in Microbioreactors and Continuous Process in Bubbleless Membrane Bioreactor Bioresour. Technol. 2016 218 944 952 10.1016/j.biortech.2016.07.053 27447921
Wei Y.-H. Lai C.-C. Chang J.-S. Using Taguchi experimental design methods to optimize trace element composition for enhanced surfactin production by Bacillus subtilis ATCC 21332 Process Biochem. 2007 42 40 45 10.1016/j.procbio.2006.07.025
Vassaux A. Rannou M. Peers S. Daboudet T. Jacques P. Coutte F. Impact of the Purification Process on the Spray-Drying Performances of the Three Families of Lipopeptide Biosurfactant Produced by Bacillus subtilis Front. Bioeng. Biotechnol. 2021 9 815337 10.3389/fbioe.2021.815337 35004661
Muchembled J. Deweer C. Sahmer K. Halama P. Antifungal activity of essential oils on two Venturia inaequalis strains with different sensitivities to tebuconazole Environ. Sci. Pollut. Res. 2017 25 29921 29928 10.1007/s11356-017-0507-z
Kensy F. Zang E. Faulhammer C. Tan R.-K. Büchs J. Validation of a high-throughput fermentation system based on online monitoring of biomass and fluorescence in continuously shaken microtiter plates Microb. Cell Factories 2009 8 31 10.1186/1475-2859-8-31
Funke M. Diederichs S. Kensy F. Müller C. Büchs J. The baffled microtiter plate: Increased oxygen transfer and improved online monitoring in small scale fermentations Biotechnol. Bioeng. 2009 103 1118 1128 10.1002/bit.22341 19449392
Tiryaki O. Validation of QuEChERS method for the determination of some pesticide residues in two apple varieties J. Environ. Sci. Health Part B 2016 51 722 729 10.1080/03601234.2016.1191922
Romero D. De Vicente A. Rakotoaly R.H. Dufour S.E. Veening J.-W. Arrebola E. Cazorla F.M. Kuipers O.P. Paquot M. Pérez-García A. The Iturin and Fengycin Families of Lipopeptides Are Key Factors in Antagonism of Bacillus subtilis Toward Podosphaera fusca Mol. Plant Microbe Interact. 2007 20 430 440 10.1094/MPMI-20-4-0430 17427813
Jimenez M. Castillo F. Alcal E. Morales G. Valdes R. Reyes F. Biological Effectiveness of Bacillus Spp. and Trichoderma Spp. on Apple Scab (Venturia inaequalis) in Vitro and under Field Conditions Eur. J. Phys. Agric. Sci. 2018 6 11
Kucheryava N. Fiss M. Auling G. Kroppenstedt R.M. Isolation and Characterization of Epiphytic Bacteria from the Phyllosphere of Apple, Antagonistic in vitro to Venturia inaequalis, the Causal Agent of Apple Scab Syst. Appl. Microbiol. 1999 22 472 478 10.1016/S0723-2020(99)80057-5
Köhl J.J. Molhoek W.W.M.L. Haas B.B.H.G.-D. De Geijn H.H.M.G.-V. Selection and orchard testing of antagonists suppressing conidial production by the apple scab pathogen Venturia inaequalis Eur. J. Plant Pathol. 2008 123 401 414 10.1007/s10658-008-9377-z
Köhl J. Scheer C. Holb I.J. Masny S. Molhoek W. Toward an Integrated Use of Biological Control by Cladosporium cladosporioides H39 in Apple Scab (Venturia inaequalis) Management Plant Dis. 2015 99 535 543 10.1094/PDIS-08-14-0836-RE
Saxena A.k. Kumar M. Chakdar H. Anuroopa N. Bagyaraj D.j. Bacillus Species in Soil as a Natural Resource for Plant Health and Nutrition J. Appl. Microbiol. 2020 128 1583 1594 10.1111/jam.14506
Kensy F. Engelbrecht C. Büchs J. Scale-up from microtiter plate to laboratory fermenter: Evaluation by online monitoring techniques of growth and protein expression in Escherichia coli and Hansenula polymorpha fermentations Microb. Cell Factories 2009 8 68 10.1186/1475-2859-8-68
Janek T. Gudiña E. Połomska X. Biniarz P. Jama D. Rodrigues L. Rymowicz W. Lazar Z. Sustainable Surfactin Production by Bacillus subtilis Using Crude Glycerol from Different Wastes Molecules 2021 26 3488 10.3390/molecules26123488
Sousa M. Melo V. Rodrigues S. Sant’Ana H.B. Gonçalves L.R.B. Screening of biosurfactant-producing Bacillus strains using glycerol from the biodiesel synthesis as main carbon source Bioprocess Biosyst. Eng. 2012 35 897 906 10.1007/s00449-011-0674-0 22218992
de Faria A.F. Stéfani D. Vaz B.G. Silva Í.S. Garcia J.S. Eberlin M.N. Grossman M.J. Alves O.L. Durrant L.R. Purification and Structural Characterization of Fengycin Homologues Produced by Bacillus subtilis LSFM-05 Grown on Raw Glycerol J. Ind. Microbiol. Biotechnol. 2011 38 863 871 10.1007/s10295-011-0980-1 21607611
Denoirjean T. Doury G. Poli P. Coutte F. Ameline A. Effects of Bacillus lipopeptides on the survival and behavior of the rosy apple aphid Dysaphis plantaginea Ecotoxicol. Environ. Saf. 2021 226 112840 10.1016/j.ecoenv.2021.112840 34619473
Denoirjean T. Ameline A. Couty A. Dubois F. Coutte F. Doury G. Effects of surfactins, Bacillus lipopeptides, on the behavior of an aphid and host selection by its parasitoid Pest Manag. Sci. 2021 78 929 937 10.1002/ps.6702
Toure Y. Ongena M. Jacques P. Guiro A. Thonart P. Role of lipopeptides produced by Bacillus subtilis GA1 in the reduction of grey mould disease caused by Botrytis cinerea on apple J. Appl. Microbiol. 2004 96 1151 1160 10.1111/j.1365-2672.2004.02252.x
Kourmentza K. Gromada X. Michael N. Degraeve C. Vanier G. Ravallec R. Coutte F. Karatzas K.A. Jauregi P. Antimicrobial Activity of Lipopeptide Biosurfactants Against Foodborne Pathogen and Food Spoilage Microorganisms and Their Cytotoxicity Front. Microbiol. 2021 11 561060 10.3389/fmicb.2020.561060 33505362
