[en] The role of membrane lipids is increasingly claimed to explain biological activities of natural amphiphile molecules. To decipher this role, biophysical studies with biomimetic membrane models are often helpful to obtain insights at the molecular and atomic levels. In this review, the added value of biophysics to study lipid-driven biological processes is illustrated using the case of surfactins, a class of natural lipopeptides produced by Bacillus sp. showing a broad range of biological activities. The mechanism of interaction of surfactins with biomimetic models showed to be dependent on the surfactins-to-lipid ratio with action as membrane disturber without membrane lysis at low and intermediate ratios and a membrane permeabilizing effect at higher ratios. These two mechanisms are relevant to explain surfactins’ biological activities occurring without membrane lysis, such as their antiviral and plant immunity-eliciting activities, and the one involving cell lysis, such as their antibacterial and hemolytic activities. In both biological and biophysical studies, influence of surfactin structure and membrane lipids on the mechanisms was observed with a similar trend. Hence, biomimetic models represent interesting tools to elucidate the biological mechanisms targeting membrane lipids and can contribute to the development of new molecules for pharmaceutical or agronomic applications.
Research Center/Unit :
TERRA Research Centre. Chimie des agro-biosystèmes - ULiège
FU - Fondation Universitaire F.R.S.-FNRS - Fonds de la Recherche Scientifique FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture Interreg France-Wallonie-Vlaanderen
Cordelier S. Crouzet J. Gilliard G. Dorey S. Deleu M. Dhondt-Cordelier S. Deciphering the Role of Plant Plasma Membrane Lipids in Response to Invasion Patterns: How Could Biology and Biophysics Help? J. Exp. Bot. 2022 73 2765 2784 10.1093/jxb/erab517 35560208
Balleza D. Alessandrini A. Beltrán García M.J. Role of Lipid Composition, Physicochemical Interactions, and Membrane Mechanics in the Molecular Actions of Microbial Cyclic Lipopeptides J. Membrane Biol. 2019 252 131 157 10.1007/s00232-019-00067-4 31098678
Otzen D.E. Biosurfactants and Surfactants Interacting with Membranes and Proteins: Same but Different? Biochim. Biophys. Acta (BBA) Biomembr. 2017 1859 639 649 10.1016/j.bbamem.2016.09.024 27693345
Yuan L. Zhang S. Wang Y. Li Y. Wang X. Yang Q. Surfactin Inhibits Membrane Fusion during Invasion of Epithelial Cells by Enveloped Viruses J. Virol. 2018 92 e00809 e00818 10.1128/JVI.00809-18 30068648
Vollenbroich D. Özel M. Vater J. Kamp R.M. Pauli G. Mechanism of Inactivation of Enveloped Viruses by the Biosurfactant Surfactin from Bacillus Subtilis Biologicals 1997 25 289 297 10.1006/biol.1997.0099 9324997
Monnier N. Furlan A.L. Buchoux S. Deleu M. Dauchez M. Rippa S. Sarazin C. Exploring the Dual Interaction of Natural Rhamnolipids with Plant and Fungal Biomimetic Plasma Membranes through Biophysical Studies Int. J. Mol. Sci. 2019 20 1009 10.3390/ijms20051009
Carravilla P. Nieva J.L. HIV Antivirals: Targeting the Functional Organization of the Lipid Envelope Future Virol. 2018 13 129 140 10.2217/fvl-2017-0114
Silverman J.A. Perlmutter N.G. Shapiro H.M. Correlation of Daptomycin Bactericidal Activity and Membrane Depolarization in Staphylococcus Aureus Antimicrob. Agents Chemother. 2003 47 2538 2544 10.1128/AAC.47.8.2538-2544.2003
González-Jaramillo L.M. Aranda F.J. Teruel J.A. Villegas-Escobar V. Ortiz A. Antimycotic Activity of Fengycin C Biosurfactant and Its Interaction with Phosphatidylcholine Model Membranes Colloids Surf. B Biointerfaces 2017 156 114 122 10.1016/j.colsurfb.2017.05.021
Huang H.W. Daptomycin, Its Membrane-Active Mechanism vs. That of Other Antimicrobial Peptides Biochim. Biophys. Acta (BBA) Biomembr. 2020 1862 183395 10.1016/j.bbamem.2020.183395
Gray D.A. Wenzel M. More Than a Pore: A Current Perspective on the In Vivo Mode of Action of the Lipopeptide Antibiotic Daptomycin Antibiotics 2020 9 17 10.3390/antibiotics9010017 31947747
Schellenberger R. Crouzet J. Nickzad A. Shu L.-J. Kutschera A. Gerster T. Borie N. Dawid C. Cloutier M. Villaume S. et al. Bacterial Rhamnolipids and Their 3-Hydroxyalkanoate Precursors Activate Arabidopsis Innate Immunity through Two Independent Mechanisms Proc. Natl. Acad. Sci. USA 2021 118 e2101366118 10.1073/pnas.2101366118 34561304
Henry G. Deleu M. Jourdan E. Thonart P. Ongena M. The Bacterial Lipopeptide Surfactin Targets the Lipid Fraction of the Plant Plasma Membrane to Trigger Immune-Related Defence Responses Cell. Microbiol. 2011 13 1824 1837 10.1111/j.1462-5822.2011.01664.x
Hoff G. Arguelles Arias A. Boubsi F. Pršić J. Meyer T. Ibrahim H.M.M. Steels S. Luzuriaga P. Legras A. Franzil L. et al. Surfactin Stimulated by Pectin Molecular Patterns and Root Exudates Acts as a Key Driver of the Bacillus-Plant Mutualistic Interaction mBio 2021 12 e01774-21 10.1128/mBio.01774-21
Lam V.B. Meyer T. Arias A.A. Ongena M. Oni F.E. Höfte M. Bacillus Cyclic Lipopeptides Iturin and Fengycin Control Rice Blast Caused by Pyricularia oryzae in Potting and Acid Sulfate Soils by Direct Antagonism and Induced Systemic Resistance Microorganisms 2021 9 1441 10.3390/microorganisms9071441 34361878
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
Das P. Mukherjee S. Sen R. Antimicrobial Potential of a Lipopeptide Biosurfactant Derived from a Marine Bacillus circulans J. Appl. Microbiol. 2008 104 1675 1684 10.1111/j.1365-2672.2007.03701.x
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
Cao X. Wang A. Wang C. Mao D. Lu M. Cui Y. Jiao R. Surfactin Induces Apoptosis in Human Breast Cancer MCF-7 Cells through a ROS/JNK-Mediated Mitochondrial/Caspase Pathway Chem. Biol. Interact. 2010 183 357 362 10.1016/j.cbi.2009.11.027
Walvekar S. Yasaswi S. Shetty K. Yadav K.S. Chapter 11—Applications of Surfactin and Other Biosurfactants in Anticancer Activity Green Sustainable Process for Chemical and Environmental Engineering and Science Inamuddin Adetunji C.O. Ahamed M.I. Academic Press Cambridge, MA, USA 2022 223 234 978-0-323-85146-6
Kracht M. Rokos H. Özel M. Kowall M. Pauli G. Vater J. Antiviral and Hemolytic Activities of Surfactin Isoforms and Their Methyl Ester Derivatives J. Antibiot. 1999 52 613 619 10.7164/antibiotics.52.613
Johnson B.A. Hage A. Kalveram B. Mears M. Plante J.A. Rodriguez S.E. Ding Z. Luo X. Bente D. Bradrick S.S. et al. Peptidoglycan-Associated Cyclic Lipopeptide Disrupts Viral Infectivity J. Virol. 2019 93 e0128219 10.1128/JVI.01282-19 31462558
Meena K.R. Kanwar S.S. Lipopeptides as the Antifungal and Antibacterial Agents: Applications in Food Safety and Therapeutics BioMed Res. Int. 2015 2015 e473050 10.1155/2015/473050 25632392
Ongena M. Jourdan E. Adam A. Paquot M. Brans A. Joris B. Arpigny J.-L. Thonart P. Surfactin and Fengycin Lipopeptides of Bacillus subtilis as Elicitors of Induced Systemic Resistance in Plants Environ. Microbiol. 2007 9 1084 1090 10.1111/j.1462-2920.2006.01202.x
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 18289856
Pérez-García A. Romero D. de Vicente A. Plant Protection and Growth Stimulation by Microorganisms: Biotechnological Applications of Bacilli in Agriculture Curr. Opin. Biotechnol. 2011 22 187 193 10.1016/j.copbio.2010.12.003 21211960
Pršić J. Ongena M. Elicitors of Plant Immunity Triggered by Beneficial Bacteria Front. Plant Sci. 2020 11 594530 10.3389/fpls.2020.594530 33304371
Théatre A. Cano-Prieto C. Bartolini M. Laurin Y. Deleu M. Niehren J. Fida T. Gerbinet S. Alanjary M. Medema M.H. et al. The Surfactin-Like Lipopeptides from Bacillus spp.: Natural Biodiversity and Synthetic Biology for a Broader Application Range Front. Bioeng. Biotechnol. 2021 9 623701 10.3389/fbioe.2021.623701
Chen X. Lu Y. Shan M. Zhao H. Lu Z. Lu Y. A Mini-Review: Mechanism of Antimicrobial Action and Application of Surfactin World J. Microbiol. Biotechnol. 2022 38 143 10.1007/s11274-022-03323-3
Pinkas D. Fišer R. Kozlík P. Dolejšová T. Hryzáková K. Konopásek I. Mikušová G. Bacillus subtilis Cardiolipin Protects Its Own Membrane against Surfactin-Induced Permeabilization Biochim. Biophys. Acta (BBA) Biomembr. 2020 1862 183405 10.1016/j.bbamem.2020.183405
Oftedal L. Myhren L. Jokela J. Gausdal G. Sivonen K. Døskeland S.O. Herfindal L. The Lipopeptide Toxins Anabaenolysin A and B Target Biological Membranes in a Cholesterol-Dependent Manner Biochim. Biophys. Acta (BBA) Biomembr. 2012 1818 3000 3009 10.1016/j.bbamem.2012.07.015
Gerbeau-Pissot P. Der C. Thomas D. Anca I.-A. Grosjean K. Roche Y. Perrier-Cornet J.-M. Mongrand S. Simon-Plas F. Modification of Plasma Membrane Organization in Tobacco Cells Elicited by Cryptogein Plant Physiol. 2014 164 273 286 10.1104/pp.113.225755 24235133
Deleu M. Crowet J.-M. Nasir M.N. Lins L. Complementary Biophysical Tools to Investigate Lipid Specificity in the Interaction between Bioactive Molecules and the Plasma Membrane: A Review Biochim. Biophys. Acta (BBA) Biomembr. 2014 1838 3171 3190 10.1016/j.bbamem.2014.08.023 25175476
Peetla C. Stine A. Labhasetwar V. Biophysical Interactions with Model Lipid Membranes: Applications in Drug Discovery and Drug Delivery Mol. Pharm. 2009 6 1264 1276 10.1021/mp9000662
Yeagle P.L. Chapter 6—Laboratory Membrane Systems The Membranes of Cells 3rd ed. Yeagle P.L. Academic Press Boston, MA, USA 2016 95 114 978-0-12-800047-2
Munusamy S. Conde R. Bertrand B. Munoz-Garay C. Biophysical Approaches for Exploring Lipopeptide-Lipid Interactions Biochimie 2020 170 173 202 10.1016/j.biochi.2020.01.009
Heerklotz H. Seelig J. Detergent-Like Action of the Antibiotic Peptide Surfactin on Lipid Membranes Biophys. J. 2001 81 1547 1554 10.1016/S0006-3495(01)75808-0
Razafindralambo H. Dufour S. Paquot M. Deleu M. Thermodynamic Studies of the Binding Interactions of Surfactin Analogues to Lipid Vesicles: Application of Isothermal Titration Calorimetry J. Therm. Anal. Calorim. 2009 95 817 821 10.1007/s10973-008-9403-6
Deleu M. Bouffioux O. Razafindralambo H. Paquot M. Hbid C. Thonart P. Jacques P. Brasseur R. Interaction of Surfactin with Membranes: A Computational Approach Langmuir 2003 19 3377 3385 10.1021/la026543z
Heerklotz H. Wieprecht T. Seelig J. Membrane Perturbation by the Lipopeptide Surfactin and Detergents as Studied by Deuterium NMR J. Phys. Chem. B 2004 108 4909 4915 10.1021/jp0371938
Shen H.-H. Thomas R.K. Taylor P. The Location of the Biosurfactant Surfactin in Phospholipid Bilayers Supported on Silica Using Neutron Reflectometry Langmuir 2010 26 320 327 10.1021/la9034936
Fan H.Y. Nazari M. Raval G. Khan Z. Patel H. Heerklotz H. Utilizing Zeta Potential Measurements to Study the Effective Charge, Membrane Partitioning, and Membrane Permeation of the Lipopeptide Surfactin Biochim. Biophys. Acta (BBA) Biomembr. 2014 1838 2306 2312 10.1016/j.bbamem.2014.02.018
Fiedler S. Heerklotz H. Vesicle Leakage Reflects the Target Selectivity of Antimicrobial Lipopeptides from Bacillus subtilis Biophys. J. 2015 109 2079 2089 10.1016/j.bpj.2015.09.021 26588567
Patel H. Huynh Q. Bärlehner D. Heerklotz H. Additive and Synergistic Membrane Permeabilization by Antimicrobial (Lipo)Peptides and Detergents Biophys. J. 2014 106 2115 2125 10.1016/j.bpj.2014.04.006 24853740
Carrillo C. Teruel J.A. Aranda F.J. Ortiz A. Molecular Mechanism of Membrane Permeabilization by the Peptide Antibiotic Surfactin Biochim. Biophys. Acta (BBA) Biomembr. 2003 1611 91 97 10.1016/S0005-2736(03)00029-4
Liu J. Zou A. Mu B. Surfactin Effect on the Physicochemical Property of PC Liposome Colloids Surf. A Physicochem. Eng. Asp. 2010 361 90 95 10.1016/j.colsurfa.2010.03.021
Kell H. Holzwarth J.F. Boettcher C. Heenan R.K. Vater J. Physicochemical Studies of the Interaction of the Lipoheptapeptide Surfactin with Lipid Bilayers of L-α-Dimyristoyl Phosphatidylcholine Biophys. Chem. 2007 128 114 124 10.1016/j.bpc.2007.03.005
Deleu M. Lorent J. Lins L. Brasseur R. Braun N. El Kirat K. Nylander T. Dufrêne Y.F. Mingeot-Leclercq M.-P. Effects of Surfactin on Membrane Models Displaying Lipid Phase Separation Biochim. Biophys. Acta (BBA) Biomembr. 2013 1828 801 815 10.1016/j.bbamem.2012.11.007
Francius G. Dufour S. Deleu M. Paquot M. Mingeot-Leclercq M.-P. Dufrêne Y.F. Nanoscale Membrane Activity of Surfactins: Influence of Geometry, Charge and Hydrophobicity Biochim. Biophys. Acta (BBA) Biomembr. 2008 1778 2058 2068 10.1016/j.bbamem.2008.03.023
Brasseur R. Braun N. El Kirat K. Deleu M. Mingeot-Leclercq M.-P. Dufrêne Y.F. The Biologically Important Surfactin Lipopeptide Induces Nanoripples in Supported Lipid Bilayers Langmuir 2007 23 9769 9772 10.1021/la7014868
Buchoux S. Lai-Kee-Him J. Garnier M. Tsan P. Besson F. Brisson A. Dufourc E.J. Surfactin-Triggered Small Vesicle Formation of Negatively Charged Membranes: A Novel Membrane-Lysis Mechanism Biophys. J. 2008 95 3840 3849 10.1529/biophysj.107.128322
Heerklotz H. Seelig J. Leakage and Lysis of Lipid Membranes Induced by the Lipopeptide Surfactin Eur. Biophys. J. 2007 36 305 314 10.1007/s00249-006-0091-5
Ostroumova O.S. Malev V.V. Ilin M.G. Schagina L.V. Surfactin Activity Depends on the Membrane Dipole Potential Langmuir 2010 26 15092 15097 10.1021/la102691y 20828112
Liu X. Huang W. Wang E. An Electrochemical Study on the Interaction of Surfactin with a Supported Bilayer Lipid Membrane on a Glassy Carbon Electrode J. Electroanal. Chem. 2005 577 349 354 10.1016/j.jelechem.2004.12.010
Grau A. Gómez Fernández J.C. Peypoux F. Ortiz A. A Study on the Interactions of Surfactin with Phospholipid Vesicles Biochim. Biophys. Acta (BBA) Biomembr. 1999 1418 307 319 10.1016/S0005-2736(99)00039-5
Bouffioux O. Berquand A. Eeman M. Paquot M. Dufrêne Y.F. Brasseur R. Deleu M. Molecular Organization of Surfactin–Phospholipid Monolayers: Effect of Phospholipid Chain Length and Polar Head Biochim. Biophys. Acta (BBA) Biomembr. 2007 1768 1758 1768 10.1016/j.bbamem.2007.04.015
Eeman M. Berquand A. Dufrêne Y.F. Paquot M. Dufour S. Deleu M. Penetration of Surfactin into Phospholipid Monolayers: Nanoscale Interfacial Organization Langmuir 2006 22 11337 11345 10.1021/la061969p
Shen H.-H. Thomas R.K. Penfold J. Fragneto G. Destruction and Solubilization of Supported Phospholipid Bilayers on Silica by the Biosurfactant Surfactin Langmuir 2010 26 7334 7342 10.1021/la904212x
Watts A. NMR of Lipids Encyclopedia of Biophysics Roberts G.C.K. Springer Berlin/Heidelberg, Germany 2013 1727 1738 978-3-642-16712-6
Maget-Dana R. Ptak M. Interactions of Surfactin with Membrane Models Biophys. J. 1995 68 1937 1943 10.1016/S0006-3495(95)80370-X
Hovakeemian S.G. Liu R. H. Gellman S. Heerklotz H. Correlating Antimicrobial Activity and Model Membrane Leakage Induced by Nylon-3 Polymers and Detergents Soft Matter 2015 11 6840 6851 10.1039/C5SM01521A
Uttlová P. Pinkas D. Bechyňková O. Fišer R. Svobodová J. Seydlová G. Bacillus subtilis Alters the Proportion of Major Membrane Phospholipids in Response to Surfactin Exposure Biochim. Biophys. Acta (BBA) Biomembr. 2016 1858 2965 2971 10.1016/j.bbamem.2016.09.006
Dufour S. Deleu M. Nott K. Wathelet B. Thonart P. Paquot M. Hemolytic Activity of New Linear Surfactin Analogs in Relation to Their Physico-Chemical Properties Biochim. Biophys. Acta (BBA) Gen. Subj. 2005 1726 87 95 10.1016/j.bbagen.2005.06.015
Coronel J.R. Aranda F.J. Teruel J.A. Marqués A. Manresa Á. Ortiz A. Kinetic and Structural Aspects of the Permeabilization of Biological and Model Membranes by Lichenysin Langmuir 2016 32 78 87 10.1021/acs.langmuir.5b04294 26652062
Coronel J.R. Marqués A. Manresa Á. Aranda F.J. Teruel J.A. Ortiz A. Interaction of the Lipopeptide Biosurfactant Lichenysin with Phosphatidylcholine Model Membranes Langmuir 2017 33 9997 10005 10.1021/acs.langmuir.7b01827 28885026
Grangemard I. Wallach J. Maget-Dana R. Peypoux F. Lichenysin Appl. Biochem. Biotechnol. 2001 90 199 210 10.1385/ABAB:90:3:199
Maget-Dana R. Ptak M. Interfacial Properties of Surfactin J. Colloid Interface Sci. 1992 153 285 291 10.1016/0021-9797(92)90319-H
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
D’Auria L. Deleu M. Dufour S. Mingeot-Leclercq M.-P. Tyteca D. Surfactins Modulate the Lateral Organization of Fluorescent Membrane Polar Lipids: A New Tool to Study Drug:Membrane Interaction and Assessment of the Role of Cholesterol and Drug Acyl Chain Length Biochim. Biophys. Acta (BBA) Biomembr. 2013 1828 2064 2073 10.1016/j.bbamem.2013.05.006
Wójtowicz K. Czogalla A. Trombik T. Łukaszewicz M. Surfactin Cyclic Lipopeptides Change the Plasma Membrane Composition and Lateral Organization in Mammalian Cells Biochim. Biophys. Acta (BBA) Biomembr. 2021 1863 183730 10.1016/j.bbamem.2021.183730
Seydlová G. Svobodová J. Review of Surfactin Chemical Properties and the Potential Biomedical Applications Cent. Eur. J. Med. 2008 3 123 133 10.2478/s11536-008-0002-5
Fei D. Liu F.-F. Gang H.-Z. Liu J.-F. Yang S.-Z. Ye R.-Q. Mu B.-Z. A New Member of the Surfactin Family Produced by Bacillus subtilis with Low Toxicity on Erythrocyte Process Biochem. 2020 94 164 171 10.1016/j.procbio.2020.04.022
Seydlová G. Fišer R. Cabala R. Kozlík P. Svobodová J. Pátek M. Surfactin Production Enhances the Level of Cardiolipin in the Cytoplasmic Membrane of Bacillus subtilis Biochim. Biophys. Acta 2013 1828 2370 2378 10.1016/j.bbamem.2013.06.032
Jourdan E. Henry G. Duby F. Dommes J. Barthélemy J.P. Thonart P. Ongena M. Insights into the Defense-Related Events Occurring in Plant Cells Following Perception of Surfactin-Type Lipopeptide from Bacillus subtilis MPMI 2009 22 456 468 10.1094/MPMI-22-4-0456 19271960
Mohd Isa M.H. Shamsudin N.H. Al-Shorgani N.K.N. Alsharjabi F.A. Kalil M.S. Evaluation of Antibacterial Potential of Biosurfactant Produced by Surfactin-Producing Bacillus Isolated from Selected Malaysian Fermented Foods Food Biotechnol. 2020 34 1 24 10.1080/08905436.2019.1710843
Bahadur S. Pathak K. Pattnaik S. Swain K. Chapter 29—Biosurfactants for Optimal Delivery of Poorly Soluble Therapeutic Agents Green Sustainable Process for Chemical and Environmental Engineering and Science Inamuddin Adetunji C.O. Ahamed M.I. Academic Press Cambridge, MA, USA 2022 543 558 978-0-323-85146-6
Sarkar S. Saha A. Biswas A. Islam S.K.M. Chapter 12—Inhibitory Activity of Biosurfactants against H+-K+ ATPases and Defense against Gastric Ulcers Green Sustainable Process for Chemical and Environmental Engineering and Science Inamuddin Adetunji C.O. Ahamed M.I. Academic Press Cambridge, MA, USA 2022 235 242 978-0-323-85146-6
Colpitts C.C. Ustinov A.V. Epand R.F. Epand R.M. Korshun V.A. Schang L.M. 5-(Perylen-3-Yl)Ethynyl-Arabino-Uridine (AUY11), an Arabino-Based Rigid Amphipathic Fusion Inhibitor, Targets Virion Envelope Lipids To Inhibit Fusion of Influenza Virus, Hepatitis C Virus, and Other Enveloped Viruses J. Virol. 2013 87 3640 3654 10.1128/JVI.02882-12 23283943
Herzog M. Tiso T. Blank L.M. Winter R. Interaction of Rhamnolipids with Model Biomembranes of Varying Complexity Biochim. Biophys. Acta (BBA)—Biomembr. 2020 1862 183431 10.1016/j.bbamem.2020.183431 32750318
