The Journal of Membrane Biology

, Volume 252, Issue 2–3, pp 131–157 | Cite as

Role of Lipid Composition, Physicochemical Interactions, and Membrane Mechanics in the Molecular Actions of Microbial Cyclic Lipopeptides

  • Daniel BallezaEmail author
  • Andrea Alessandrini
  • Miguel J. Beltrán García
Topical Review


Several experimental and theoretical studies have extensively investigated the effects of a large diversity of antimicrobial peptides (AMPs) on model lipid bilayers and living cells. Many of these peptides disturb cells by forming pores in the plasma membrane that eventually lead to the cell death. The complexity of these peptide–lipid interactions is mainly related to electrostatic, hydrophobic and topological issues of these counterparts. Diverse studies have shed some light on how AMPs act on lipid bilayers composed by different phospholipids, and how mechanical properties of membranes could affect the antimicrobial effects of such compounds. On the other hand, cyclic lipopeptides (cLPs), an important class of microbial secondary metabolites, have received comparatively less attention. Due to their amphipathic structures, cLPs exhibit interesting biological activities including interactions with biofilms, anti-bacterial, anti-fungal, antiviral, and anti-tumoral properties, which deserve more investigation. Understanding how physicochemical properties of lipid bilayers contribute and determining the antagonistic activity of these secondary metabolites over a broad spectrum of microbial pathogens could establish a framework to design and select effective strategies of biological control. This implies unravelling—at the biophysical level—the complex interactions established between cLPs and lipid bilayers. This review presents, in a systematic manner, the diversity of lipidated antibiotics produced by different microorganisms, with a critical analysis of the perturbing actions that have been reported in the literature for this specific set of membrane-active lipopeptides during their interactions with model membranes and in vivo. With an overview on the mechanical properties of lipid bilayers that can be experimentally determined, we also discuss which parameters are relevant in the understanding of those perturbation effects. Finally, we expose in brief, how this knowledge can help to design novel strategies to use these biosurfactants in the agronomic and pharmaceutical industries.


Cyclic lipopeptides Lipid bilayers Electrostatic and mechanical properties Antibiotic activity 



The authors would like to acknowledge CONACyT (Project No. 2016-269607) for funding. We also thank Dr. Gloria Macedo for her invaluable technical support in obtaining MALDI-TOF mass spectra, Ms. Flor Casillas for technical support, and Dr. N. Marín-Medina for critical reading of the manuscript. We specially thank the anonymous reviewers for their valuable suggestions and comments.

Author Contributions

Proposed the Review, M. B-G. Experiments were performed by D.B. and A.A. The manuscript was written/corrected by all the authors.

Compliance with Ethical Standards

Conflict of interest

The authors declare no conflict of interest.


  1. Akpa E, Jacques P, Wathelet B et al (2001) Influence of culture conditions on lipopeptide production by Bacillus subtilis. Appl Biochem Biotechnol 91–93:551–561Google Scholar
  2. Alessandrini A, Facci P (2012) Nanoscale mechanical properties of lipid bilayers and their relevance in biomembrane organization and function. Micron 43:1212–1223. Google Scholar
  3. Alvares DS, Viegas TG, Ruggiero-Neto J (2017) Lipid-packing perturbation of model membranes by pH-responsive antimicrobial peptides. Biophys Rev 9:669–682. Google Scholar
  4. Andersen OS, Koeppe RE 2nd (2007) Bilayer thickness and membrane protein function: an energetic perspective. Annu Rev Biophys Biomol Struct 36:107–130. Google Scholar
  5. Anderson TM, Clay MC, Cioffi AG et al (2014) Amphotericin forms an extramembranous and fungicidal sterol sponge. Nat Chem Biol 10:400–406. Google Scholar
  6. Anishkin A, Loukin SH, Teng J, Kung C (2014) Feeling the hidden mechanical forces in lipid bilayer is an original sense. Proc Natl Acad Sci USA 111:7898–7905. Google Scholar
  7. Anselmi M, Eliseo T, Zanetti-Polzi L et al (2011) Structure of the lipodepsipeptide syringomycin E in phospholipids and sodium dodecylsulphate micelle studied by circular dichroism, NMR spectroscopy and molecular dynamics. Biochim Biophys Acta 1808:2102–2110. Google Scholar
  8. Aranda FJ, Teruel JA, Ortiz A (2005) Further aspects on the hemolytic activity of the antibiotic lipopeptide iturin A. Biochim Biophys Acta 1713:51–56. Google Scholar
  9. Baltz RH (2014) Combinatorial biosynthesis of cyclic lipopeptide antibiotics: a model for synthetic biology to accelerate the evolution of secondary metabolite biosynthetic pathways. ACS Synth Biol 3:748–758. Google Scholar
  10. Becucci L, Tramonti V, Fiore A et al (2015) Channel-forming activity of syringomycin E in two mercury-supported biomimetic membranes. Biochim Biophys Acta 1848:932–941. Google Scholar
  11. Belbahri L, Chenari-Bouket A, Rekik I et al (2017) Comparative genomics of Bacillus amyloliquefaciens strains reveals a core genome with traits for habitat adaptation and a secondary metabolites rich accessory genome. Front Microbiol 8:1438. Google Scholar
  12. Beltran-Gracia E, Macedo-Raygoza G, Villafaña-Rojas J et al (2017) Production of lipopeptides by fermentation processes: endophytic bacteria, fermentation strategies and easy methods for bacterial selection. In: Menestrina G, Dalla Serra M, Faustino Jozala A (eds) Fermentation processes, 1st edn. Intech Open Science, London, pp 260–271Google Scholar
  13. Bensaci MF, Gurnev PA, Bezrukov SM, Takemoto JY (2011) Fungicidal activities and mechanisms of action of Pseudomonas syringae pv syringae lipodepsipeptide Syringopeptins 22A and 25A. Front Microbiol 2:216. Google Scholar
  14. Berglund NA, Piggot TJ, Jefferies D, et al (2015) Interaction of the antimicrobial peptide polymyxin B1 with both membranes of E. coli: a molecular dynamics study. PLoS Comput Biol 11(4):e1004180. Google Scholar
  15. Beriashvili D, Taylor R, Kralt B et al (2018) Mechanistic studies on the effect of membrane lipid acyl chain composition on daptomycin pore formation. Chem Phys Lipids 216:73–79. Google Scholar
  16. Berkovich AK, Lukashev EP, Melik-Nubarov NS (2012) Dipole potential as a driving force for the membrane insertion of polyacrylic acid in slightly acidic milieu. Biochim Biophys Acta 1818:375–383. Google Scholar
  17. Besson F, Peypoux F, Michel G, Delcambe L (1978) Mode of action of iturin A, an antibiotic isolated from Bacillus subtilis, on Micrococcus luteus. Biochem Biophys Res Commun 81:297–304Google Scholar
  18. Besson F, Peypoux F, Michel G, Delcambe L (1979) Antifungal activity upon Saccharomyces cerevisiae of iturin A, mycosubtilin, bacillomycin L and of their derivatives; inhibition of this antifungal activity by lipid antagonists. J Antibiot 32:828–833. Google Scholar
  19. Biniarz P, Łukaszewicz M, Janek T (2017) Screening concepts, characterization and structural analysis of microbial-derived bioactive lipopeptides: a review. Crit Rev Biotechnol 37:393–410. Google Scholar
  20. Biswaro LS, da Costa Sousa MG, Rezende TMB et al (2018) Antimicrobial peptides and nanotechnology: recent advances and challenges. Front Microbiol 9:855. Google Scholar
  21. Bouffioux O, Berquand A, Eeman M et al (2007) Molecular organization of surfactin-phospholipid monolayers: effect of phospholipid chain length and polar head. Biochim Biophys Acta 1768:1758–1768. Google Scholar
  22. Brack C, Mikolasch A, Schlueter R et al (2015) Antibacterial metabolites and bacteriolytic enzymes produced by Bacillus pumilus during bacteriolysis of Arthrobacter citreus. Mar Biotechnol (NY) 17:290–304. Google Scholar
  23. Braga PC, Ricci D (2002) Dal Sasso M (2002) Daptomycin morphostructural damage in Bacillus cereus visualized by atomic force microscopy. J Chemother 14(4):336–341Google Scholar
  24. Brasseur R, Braun N, El Kirat K et al (2007) The biologically important surfactin lipopeptide induces nanoripples in supported lipid bilayers. Langmuir 23:9769–9772. Google Scholar
  25. Brogden KA (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3:238–250. Google Scholar
  26. Bruch MD, Cajal Y, Koh JT, Jain MK (1999) Higher-order structure of Polymyxin B: the functional significance of topological flexibility. J Am Chem Soc 121(51):11993–12004. Google Scholar
  27. Brügger B (2014) Lipidomics: analysis of the lipid composition of cells and subcellular organelles by electrospray ionization mass spectrometry. Annu Rev Biochem 83:79–98. Google Scholar
  28. Buchoux S, Lai-Kee-Him J, Garnier M et al (2008) Surfactin-triggered small vesicle formation of negatively charged membranes: a novel membrane-lysis mechanism. Biophys J 95:3840–3849. Google Scholar
  29. Carrillo C, Teruel JA, Aranda FJ, Ortiz A (2003) Molecular mechanism of membrane permeabilization by the peptide antibiotic surfactin. Biochim Biophys Acta 1611:91–97. Google Scholar
  30. Caulier S, Gillis A, Colau G et al (2018) Versatile antagonistic activities of soil-borne Bacillus spp and Pseudomonas spp against Phytophthora infestans and other potato pathogens. Front Microbiol 9:143. Google Scholar
  31. Chen YF, Sun TL, Sun Y, Huang HW (2014) Interaction of daptomycin with lipid bilayers: a lipid extracting effect. Biochemistry 53:5384–5392. Google Scholar
  32. Clausell A, Garcia-Subirats M, Pujol M et al (2007) Gram-negative outer and inner membrane models: insertion of cyclic cationic lipopeptides. J Phys Chem B 111:551–563. Google Scholar
  33. Cochrane SA, Vederas JC (2014) Lipopeptides from Bacillus and Paenibacillus spp A gold mine of antibiotic candidates. Med Res Rev 36:4–31. Google Scholar
  34. Coronel JR, Aranda FJ, Teruel JA et al (2016) Kinetic and structural aspects of the permeabilization of biological and model membranes by lichenysin. Langmuir 32:78–87. Google Scholar
  35. Coronel JR, Marqués A, Manresa Á et al (2017) Interaction of the lipopeptide biosurfactant Lichenysin with phosphatidylcholine model membranes. Langmuir 26(33):9997–10005. Google Scholar
  36. Coutte F, Lecouturier D, Dimitrov K et al (2017) Microbial lipopeptide production and purification bioprocesses, current progress and future challenges. Biotechnol J 25:125. Google Scholar
  37. D’aes J, Kieu NP, Léclère V et al (2014) To settle or to move? The interplay between two classes of cyclic lipopeptides in the biocontrol strain Pseudomonas CMR12a. Environ Microbiol 16(7):2282Google Scholar
  38. Dalla-Serra M, Fagiuoli G, Nordera P et al (1999) The interaction of lipodepsipeptide toxins from Pseudomonas syringae pv. syringae with biological and model membranes: a comparison of syringotoxin, syringomycin, and two syringopeptins. Mol Plant Microbe Interact 12:391–400Google Scholar
  39. Dang Y, Zhao F, Liu X, et al (2019) Enhanced production of antifungal lipopeptide iturin A by Bacillus amyloliquefaciens LL3 through metabolic engineering and culture conditions optimization. Microb Cell Fact 18(1):68. Google Scholar
  40. Das P, Mukherjee S, Sen R (2008) Genetic regulations of the biosynthesis of microbial surfactants: an overview. Biotechnol Genet Eng Rev 25:165–185. Google Scholar
  41. Daugelaviĉius R, Bakiene E, Bamford DH (2000) Stages of polymyxin B interaction with the Escherichia coli cell envelope. Antimicrob Agents Chemother 44:2969–2978. Google Scholar
  42. D’Auria L, Deleu M, Dufour S et al (2013) 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 1828(9):2064–2073. Google Scholar
  43. de Cássia FS, Silva R, Almeida DG, Rufino RD et al (2014) Applications of biosurfactants in the petroleum industry and the remediation of oil spills. Int J Mol Sci 15:12523–12542. Google Scholar
  44. Deamer D (2016) Membranes and the Origin of Life: a century of conjecture. J Mol Evol 83(5–6):159–168. Google Scholar
  45. Deleu M, Paquot M, Jacques P et al (1999) Nanometer scale organization of mixed surfactin/phosphatidylcholine monolayers. Biophys J 77:2304–2310. Google Scholar
  46. Deleu M, Paquot M, Nylander T (2005) Fengycin interaction with lipid monolayers at the air-aqueous interface-implications for the effect of fengycin on biological membranes. J Colloid Interface Sci 283:358–365Google Scholar
  47. Deleu M, Paquot M, Nylander T (2008) Effect of fengycin, a lipopeptide produced by Bacillus subtilis, on model biomembranes. Biophys J 94:2667–2679. Google Scholar
  48. Deleu M, Lorent J, Lins L et al (2013) Effects of surfactin on membrane models displaying lipid phase separation. Biochim Biophys Acta 1828:801–815. Google Scholar
  49. Deleu M, Crowet JM, Nasir MN, Lins L (2014) Complementary biophysical tools to investigate lipid specificity in the interaction between bioactive molecules and the plasma membrane: a review. Biochim Biophys Acta 1838:3171–3190. Google Scholar
  50. Deol BS, Bermingham MA, Still JL et al (1973) The action of serratamolide on ion movement in lipid bilayers and biomembranes. Biochim Biophys Acta 330:192–195Google Scholar
  51. Dimova R (2019) Giant vesicles and their use in assays for assessing membrane phase state, curvature, mechanics, and electrical properties. Annu Rev Biophys. 48:93–119. Google Scholar
  52. Dupuy FG, Pagano I, Andenoro K, et al (2018) Selective interaction of Colistin with lipid model membranes. Biophys J 114(4):919–928. Google Scholar
  53. Dwivedi D, Jansen R, Molinari G et al (2008) Antimycobacterial serratamolides and diacyl peptoglucosamine derivatives from Serratia sp. J Nat Prod 71:637–641. Google Scholar
  54. Eeman M, Deleu M, Paquot M et al (2005) Nanoscale properties of mixed fengycin/ceramide monolayers explored using atomic force microscopy. Langmuir 21:2505–2511. Google Scholar
  55. Eeman M, Berquand A, Dufrêne YF et al (2006) Penetration of surfactin into phospholipid monolayers: nanoscale interfacial organization. Langmuir 22:11337–11345. Google Scholar
  56. Eeman M, Francius G, Dufrêne YF et al (2009a) Effect of cholesterol and fatty acids on the molecular interactions of fengycin with Stratum corneum mimicking lipid monolayers. Langmuir 25:3029–3039. Google Scholar
  57. Eeman M, Pegado L, Dufrêne YF et al (2009b) Influence of environmental conditions on the interfacial organisation of fengycin, a bioactive lipopeptide produced by Bacillus subtilis. J Colloid Interface Sci 329:253–264. Google Scholar
  58. Efimova SS, Zakharova AA, Schagina LV, Ostroumova OS (2016) Two types of syringomycin E channels in sphingomyelin-containing bilayers. Eur Biophys J 45:91–98. Google Scholar
  59. Efimova SS, Zakharova AA, Ismagilov AA et al (2018) Lipid-mediated regulation of pore-forming activity of syringomycin E by thyroid hormones and xanthene dyes. Biochim Biophys Acta 1860:691–699. Google Scholar
  60. Etchegaray A, de Castro Bueno C, de Melo IS et al (2008) Effect of a highly concentrated lipopeptide extract of Bacillus subtilis on fungal and bacterial cells. Arch Microbiol 190:611–622. Google Scholar
  61. Fahy E, Subramaniam S, Brown HA et al (2005) A comprehensive classification system for lipids. J Lipid Res 46(5):839–861Google Scholar
  62. Falardeau J, Wise C, Novitsky L, Avis TJ (2013) Ecological and mechanistic insights into the direct and indirect antimicrobial properties of Bacillus subtilis lipopeptides on plant pathogens. J Chem Ecol 39:869–878. Google Scholar
  63. Fanaei M, Emtiazi G (2018) Microbial assisted (Bacillus mojavensis) production of bio-surfactant lipopeptide with potential pharmaceutical applications and its characterization by MALDI-TOF-MS analysis. J Mol Ecol 268:707–714. Google Scholar
  64. Feigin AM, Takemoto JY, Wangspa R et al (1996) Properties of voltage-gated ion channels formed by syringomycin E in planar lipid bilayers. J Membr Biol 149:41–47Google Scholar
  65. Feigin AM, Schagina LV, Takemoto JY et al (1997) The effect of sterols on the sensitivity of membranes to the channel-forming antifungalantibiotic, syringomycin E. Biochim Biophys Acta 1324:102–110Google Scholar
  66. Fickers P, Guez JS, Damblon C et al (2009) High-level biosynthesis of the anteiso-C(17) isoform of the antibiotic mycosubtilin in Bacillus subtilis and characterization of its candidacidal activity. Appl Environ Microbiol 75:4636–4640. Google Scholar
  67. Fiedler S, Heerklotz H (2015) Vesicle leakage reflects the target selectivity of antimicrobial lipopeptides from Bacillus subtilis. Biophys J 109:2079–2089. Google Scholar
  68. Francius G, Dufour S, Deleu M et al (2008) Nanoscale membrane activity of surfactins: influence of geometry, charge and hydrophobicity. Biochim Biophys Acta 1778:2058–2068. Google Scholar
  69. Fuertes G, Giménez D, Esteban-Martín S et al (2011) A lipocentric view of peptide-induced pores. Eur Biophys J 40:399–415. Google Scholar
  70. Gao L, Han J, Liu H et al (2017) Plipastatin and surfactin coproduction by Bacillus subtilis pB2-L and their effects on microorganisms. Antonie Van Leeuwenhoek 110:1007–1018. Google Scholar
  71. Garcia-Manyes S, Sanz F (2010) Nanomechanics of lipid bilayers by force spectroscopy with AFM: a perspective. Biochim Biophys Acta 1798:741–749. Google Scholar
  72. Geudens N, Nasir MN, Crowet JM et al (2017) Membrane interactions of natural cyclic lipodepsipeptides of the viscosin group. Biochim Biophys Acta 1859(3):331–339. Google Scholar
  73. Goñi FM (2014) The basic structure and dynamics of cell membranes: an update of the Singer-Nicolson model. Biochim Biophys Acta 1838:1467–1476. Google Scholar
  74. González-Jaramillo LM, Aranda FJ, Teruel JA et al (2017) Antimycotic activity of fengycin C biosurfactant and its interaction with phosphatidylcholine model membranes. Colloids Surf B 156:114–122. Google Scholar
  75. Gordillo MA, Navarro AR, Maldonado MC (2015) Mode of action of metabolites from Bacillus sp. strain IBA 33 on Geotrichum citri-aurantii arthroconidia. Can J Microbiol 61:876–880. Google Scholar
  76. Grangemard I, Wallach J, Maget-Dana R, Peypoux F (2001) Lichenysin: a more efficient cation chelator than surfactin. Appl Biochem Biotechnol 90(3):199–210Google Scholar
  77. Grau A, Gómez Fernández JC, Peypoux F, Ortiz A (1999) A study on the interactions of surfactin with phospholipid vesicles. Biochim Biophys Acta 1418(2):307–319. Google Scholar
  78. Grau A, Ortiz A, de Godos A, Gómez-Fernández JC (2000) A biophysical study of the interaction of the lipopeptide antibiotic iturin A with aqueous phospholipid bilayers. Arch Biochem Biophys 377:315–323. Google Scholar
  79. Grau A, Gómez-Fernández JC, Peypoux F, Ortiz A (2001) Aggregational behavior of aqueous dispersions of the antifungal lipopeptide iturin A. Peptides 22:1–5. Google Scholar
  80. Hamley IW (2015) Lipopeptides: from self-assembly to bioactivity. Chem Commun (Camb) 51:8574–8583. Google Scholar
  81. Hamley IW, Dehsorkhi A, Jauregi P et al (2013) Self-assembly of three bacterially-derived bioactive lipopeptides. Soft Matter 9(40):9572–9578. Google Scholar
  82. Han ML, Shen HH, Hansford KA, et al (2017) Investigating the interaction of Octapeptin A3 with model bacterial membranes. ACS Infect Dis 3(8):606–619. Google Scholar
  83. Harnois I, Maget-Dana R, Ptak M (1989) Methylation of the antifungal lipopeptide iturin A modifies its interaction with lipids. Biochimie 71:111–116. Google Scholar
  84. Hartmann W, Galla HJ, Sackmann E (1978) Polymyxin binding to charged lipid membranes. An example of cooperative lipid-protein interaction. Biochim Biophys Acta 510(1):124–139. Google Scholar
  85. Heerklotz H (2008) Interactions of surfactants with lipid membranes. Q Rev Biophys 41:205–264. Google Scholar
  86. Heerklotz H, Seelig J (2001) Detergent-like action of the antibiotic peptide surfactin on lipid membranes. Biophys J . Google Scholar
  87. Heerklotz H, Seelig J (2007) Leakage and lysis of lipid membranes induced by the lipopeptide surfactin. Eur Biophys J 36:305–314. Google Scholar
  88. Heerklotz H, Wieprecht T, Seelig J (2004) Membrane perturbation by the lipopeptide surfactin and detergents as studied by deuterium NMR. J Phys Chem B 108:4909–4915. Google Scholar
  89. Henriksen JR, Ipsen JH (2004) Measurement of membrane elasticity by micro-pipette aspiration. Eur Phys J E Soft Matter 14:149–167. Google Scholar
  90. Hobbs JK, Miller K, O’Neill AJ, Chopra I (2008) Consequences of daptomycin-mediated membrane damage in Staphylococcus aureus. J Antimicrob Chemother 62:1003–1008. Google Scholar
  91. Horn JN, Cravens A, Grossfield A (2013) Interactions between fengycin and model bilayers quantified by coarse-grained molecular dynamics. Biophys J 105(7):1612–1623. Google Scholar
  92. Hutchison ML, Tester MA, Gross DC (1995) Role of biosurfactant and ion channel-forming activities of syringomycin in transmembrane ion flux: a model for the mechanism of action in the plant-pathogen interaction. Mol Plant Microbe Interact 4:610–620Google Scholar
  93. Ishigami Y, Osman M, Nakahara H et al (1995) Significance of β-sheet formation for micellization and surface adsorption of surfactin. Colloids Surf B 4:341–348. Google Scholar
  94. Janmey PA, Kinnunen PK (2006) Biophysical properties of lipids and dynamic membranes. Trends Cell Biol 16:538–546. Google Scholar
  95. Jemil N, Hmidet N, Manresa A et al (2019) Isolation and characterization of kurstakin and surfactin isoforms produced by Enterobacter cloacae C3 strain. J Mass Spectrom 54(1):7–18. Google Scholar
  96. Joanne P, Galanth C, Goasdoué N et al (2009) Lipid reorganization induced by membrane-active peptides probed using differential scanning calorimetry. Biochim Biophys Acta 1788:1772–1781. Google Scholar
  97. Jung D, Rozek A, Okon M, Hancock RE (2004) Structural transitions as determinants of the action of the calcium-dependent antibiotic daptomycin. Chem Biol 7:949–957. Google Scholar
  98. Karal MA, Alam JM, Takahashi T, Levadny V, Yamazaki M (2015) Stretch-activated pore of the antimicrobial peptide, magainin 2. Langmuir 31:3391–401. Google Scholar
  99. Kaulin YA, Schagina LV, Bezrukov SM et al (1998) Cluster organization of ion channels formed by the antibiotic syringomycin E in bilayer lipid membranes. Biophys J 74:2918–2925Google Scholar
  100. Kaulin YA, Takemoto JY, Schagina LV et al (2005) Sphingolipids influence the sensitivity of lipid bilayers to fungicide, syringomycin E. J Bioenerg Biomembr 37:339–348. Google Scholar
  101. Kaur P, Li Y, Cai J, Song L (2016) Selective membrane disruption mechanism of an antibacterial γ-AApeptide defined by EPR spectroscopy. Biophys J 110(8):1789–1799Google Scholar
  102. Khan A, Butt A (2016) Biosurfactants and their potential applications for microbes and mankind: an overview. Middle East J. of Business 11:9–18Google Scholar
  103. Kreutzberger MA, Pokorny A, Almeida PF (2017) Daptomycin-phosphatidylglycerol domains in lipid membranes. Langmuir 33:13669–13679. Google Scholar
  104. Krupovic M, Daugelavicius R, Bamford DH (2007) Polymyxin B induces lysis of marine pseudoalteromonads. Antimicrob Agents Chemother 51:3908–3914. Google Scholar
  105. Kuzmin PI, Akimov SA, Chizmadzhev YA et al (2005) Line tension and interaction energies of membrane rafts calculated from lipid splay and tilt. Biophys J 88:1120–1133. Google Scholar
  106. Landy M, Warren GH, Rosenman SB, Colio LG (1948) Bacillomycin; an antibiotic from Bacillus subtilis active against pathogenic fungi. Proc Soc Exp Biol Med 67:539–541Google Scholar
  107. Lee AG (2011) How to understand lipid-protein interactions in biological membranes. In: Yeagle Philip L (ed) The structure of biological membranes, 3rd edn. CRC Press, Boca Raton, pp 273–314Google Scholar
  108. Lee MT, Hung WC, Chen FY, Huang HW (2008) Mechanism and kinetics of pore formation in membranes by water-soluble amphipathic peptides. Proc Natl Acad Sci USA 105:5087–5092. Google Scholar
  109. Lee TH, Hall KN, Aguilar MI (2016) Antimicrobial peptide structure and mechanism of action: a focus on the role of membrane structure. Curr Top Med Chem 16:25–39Google Scholar
  110. Lee MT, Hung WC, Hsieh MH et al (2017) Molecular state of the membrane-active antibiotic Daptomycin. Biophys J 113:82–90. Google Scholar
  111. Lee MT, Yang PY, Charron NE et al (2018) Comparison of the effects of Daptomycin on bacterial and model membranes. Biochemistry 25:125. Google Scholar
  112. Li Y, Zou AH, Ye RQ, Mu BZ (2011) Effects of molecular structure on surfactin micellization activity. Acta Phys.-Chim. Sin. 27:1128–1134Google Scholar
  113. Li W, Rokni-Zadeh H, De Vleeschouwer M et al (2013) The antimicrobial compound xantholysin defines a new group of Pseudomonas cyclic lipopeptides. PLoS ONE 8:e62946Google Scholar
  114. Li J, Koh JJ, Liu S et al (2017) Membrane active antimicrobial peptides: translating mechanistic insights to design. Front Neurosci 11:73. Google Scholar
  115. Liao G, Shi T, Xie J (2012) Regulation mechanisms underlying the biosynthesis of daptomycin and related lipopeptides. J Cell Biochem 113:735–741. Google Scholar
  116. Lohner K (2014) Antimicrobial mechanisms: a sponge against fungal infections. Nat Chem Biol 10:411–412. Google Scholar
  117. Maget-Dana R, Peypoux F (1994) Iturins, a special class of pore-forming lipopeptides: biological and physicochemical properties. Toxicology 87:151–174Google Scholar
  118. Maget-Dana R, Ptak M, Peypoux F, Michel G (1985) Pore-forming properties of iturin A, a lipopeptide antibiotic. Biochim Biophys Acta 815:405–409. Google Scholar
  119. Malev VV, Schagina LV, Gurnev PA et al (2002) Syringomycin E channel: a lipidic pore stabilized by lipopeptide? Biophys J 82:1985–1994. Google Scholar
  120. Marín-Medina N, Ramírez DA, Trier S, Leidy C (2016) Mechanical properties that influence antimicrobial peptide activity in lipid membranes. Appl Microbiol Biotechnol 100:10251–10263. Google Scholar
  121. Marquette A, Bechinger B (2018) Biophysical investigations elucidating the mechanisms of action of antimicrobial peptides and their synergism. Biomolecules. 8:E18. Google Scholar
  122. Martins PC, Bastos CG, Granjeiro PA, Martins VG (2018) New lipopeptide produced by Corynebacterium aquaticum from a low-cost substrate. Bioprocess Biosyst Eng 41:1177–1183. Google Scholar
  123. McIntosh TJ, Simon SA (2006) Roles of bilayer material properties in function and distribution of membrane proteins. Annu Rev Biophys Biomol Struct 35:177–198. Google Scholar
  124. Meena KR, Kanwar SS (2015) Lipopeptides as the antifungal and antibacterial agents: applications in food safety and therapeutics. Biomed Res Int. Google Scholar
  125. Meena KR, Sharma A, Kanwar SS (2017) Microbial lipopeptides and their medical applications. Ann Pharmacol Pharm. 2(21):1111Google Scholar
  126. Mnif I, Ghribi D (2015) Lipopeptides biosurfactants: mean classes and new insights for industrial, biomedical, and environmental applications. Biopolymers 104:129–147. Google Scholar
  127. Morrison DC, Jacobs DM (1976) Binding of polymyxin B to the lipid A portion of bacterial lipopolysaccharides. Immunochemistry. 13:813–818Google Scholar
  128. Mularski A, Separovic F (2017) Atomic Force Microscopy studies of the interaction of antimicrobial peptides with bacterial cells. Aust J Chem 70:130–137. Google Scholar
  129. Müller A, Wenzel M, Strahl H et al (2016) Daptomycin inhibits cell envelope synthesis by interfering with fluid membrane microdomains. Proc Natl Acad Sci USA 113:E7077–E7086. Google Scholar
  130. Nakayama H, Kurokawa K, Lee BL (2012) Lipoproteins in bacteria: structures and biosynthetic pathways. FEBS J 279:4247–4268. Google Scholar
  131. Nakhate PH, Yadav VK (2013) Pathak AN (2013) A review on Daptomycin: the first US-FDA approved. Lipopeptide antibiotics. J Sci Innov Res. 2:970–980Google Scholar
  132. Naruse N, Tenmyo O, Kobaru S et al (1990) Pumilacidin, a complex of new antiviral antibiotics. Production, isolation, chemical properties, structure and biological activity. J Antibiot (Tokyo). 43:267–280Google Scholar
  133. Nasir MN, Besson F (2011) Specific interactions of mycosubtilin with cholesterol-containing artificial membranes. Langmuir 27:10785–10792. Google Scholar
  134. Nasir MN, Thawani A, Kouzayha A, Besson F (2010) Interactions of the natural antimicrobial mycosubtilin with phospholipid membrane models. Colloids Surf B Biointerfaces. 78:17–23. Google Scholar
  135. Nasir MN, Benichou E, Loison C et al (2013a) Influence of the tyrosine environment on the second harmonic generation of iturinic antimicrobial lipopeptides at the air-water interface. Phys Chem Chem Phys 45:19919–19924. Google Scholar
  136. Nasir MN, Laurent P, Flore C et al (2013b) Analysis of calcium-induced effects on the conformation of fengycin. Spectrochim Acta A 110:450–457. Google Scholar
  137. Olishevska S, Nickzad A, Déziel E (2019) Bacillus and Paenibacillus secreted polyketides and peptides involved in controlling human and plant pathogens. Appl Microbiol Biotechnol 103:1189–1215. Google Scholar
  138. Omardien S, Drijfhout JW, Vaz FM et al (2018) Bactericidal activity of amphipathic cationic antimicrobial peptides involves altering the membrane fluidity when interacting with the phospholipid bilayer. Biochim Biophys Acta Biomembr. 1860:2404–2415. Google Scholar
  139. Onaizi SA (2018) Dynamic surface tension and adsorption mechanism of surfactin biosurfactant at the air-water interface. Eur Biophys J 47:631–640. Google Scholar
  140. Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125. Google Scholar
  141. Ortíz-López FJ, Monteiro MC, González-Menéndez V et al (2015) Cyclic colisporifungin and linear cavinafungins, antifungal lipopeptides isolated from Colispora cavincola. J Nat Prod 78:468–475Google Scholar
  142. Ostroumova OS, Malev VV, Kaulin YA et al (2005) Voltage-dependent synchronization of gating of syringomycin E ion channels. FEBS Lett 579:5675–5679. Google Scholar
  143. Ostroumova OS, Malev VV, Bessonov AN et al (2008) Altering the activity of syringomycin E via the membrane dipole potential. Langmuir 24:2987–2991. Google Scholar
  144. Ostroumova OS, Malev VV, Ilin MG, Schagina LV (2010) Surfactin activity depends on the membrane dipole potential. Langmuir 26:15092–15097. Google Scholar
  145. Ottova A, Tien HT (2005) The lipid bilayer principle: a historic perspective and some highlights. Advances in planar lipid bilayers and liposomes 1:1–76. Google Scholar
  146. Patel H, Tscheka C, Edwards K et al (2011) All-or-none membrane permeabilization by fengycin-type lipopeptides from Bacillus subtilis QST713. Biochim Biophys Acta 1808(8):2000–2008. Google Scholar
  147. Patel S, Ahmed S, Eswari JS (2015) Therapeutic cyclic lipopeptides mining from microbes: latest strides and hurdles. World J Microbiol Biotechnol 31:1177–1193. Google Scholar
  148. Paterson DJ, Tassieri M, Reboud J et al (2017) Lipid topology and electrostatic interactions underpin lytic activity of linear cationic antimicrobial peptides in membranes. Proc Natl Acad Sci USA 114:E8324–E8332. Google Scholar
  149. Pearlstein RA, Dickson CJ, Hornak V (2017) Contributions of the membrane dipole potential to the function of voltage-gated cationchannels and modulation by small molecule potentiators. Biochim Biophys Acta Biomembr. 1859:177–194. Google Scholar
  150. Perez KJ, Viana JD, Lopes FC et al (2017) Bacillus spp. isolated from Puba as a source of biosurfactants and antimicrobial lipopeptides. Front Microbiol. 8:61. Google Scholar
  151. Peypoux F, Bonmatin JM, Wallach J (1999) Recent trends in the biochemistry of surfactin. Appl Microbiol Biotechnol 51:553–563Google Scholar
  152. Phillips R, Ursell T, Wiggins P, Sens P (2009) Emerging roles for lipids in shaping membrane-protein function. Nature 459:379–385. Google Scholar
  153. Phillips R, Kondev J, Theriot J, Garcia H (2012) Physical biology of the cell, 2nd edn. Garland Science, Taylor and Francis Group LLC, New YorkGoogle Scholar
  154. Pichichero ME (2011) Bacterial conjunctivitis in children: antibacterial treatment options in an era of increasing drug resistance. Clin Pediatr (Phila). 50:7–13. Google Scholar
  155. Pogliano J, Pogliano N, Silverman JA (2012) Daptomycin-mediated reorganization of membrane architecture causes mislocalization of essential cell division proteins. J Bacteriol 194:4494–4504. Google Scholar
  156. Qiu J, Kirsch LE (2014) Evaluation of lipopeptide (daptomycin) aggregation using fluorescence, light scattering, and nuclear magnetic resonance spectroscopy. J Pharm Sci 103(3):853–861. Google Scholar
  157. Raaijmakers JM, De Bruijn I, Nybroe O, Ongena M (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev 34:1037–1062. Google Scholar
  158. Rappolt M, Pabst G (2008) Flexibility and structure of fluid bilayer interfaces. In: Nag Kaushik (ed) Structure and dynamics of membranous interfaces. John Wiley & Sons Inc, Hoboken. Google Scholar
  159. Rawicz W, Olbrich KC, McIntosh T et al (2000) Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys J 79:328–339. Google Scholar
  160. Razafindralambo H, Popineau Y, Deleu M et al (1997) Surface-active properties of surfactin/iturin A mixtures produced by Bacillus subtilis. Langmuir 13:6026–6031. Google Scholar
  161. Razafindralambo H, Dufour S, Paquot M, Deleu M (2009) Thermodynamic studies of the binding interactions of surfactin analogues to lipid vesicles: application of isothermal titration calorimetry. J Therm Anal Calorim 95:817–821. Google Scholar
  162. Reidl HH, Takemoto JY (1987) Mechanism of action of bacterial phytotoxin, syringomycin. Simultaneous measurement of early responses in yeasts and maize. Biochim Biophys Acta 898:56–59Google Scholar
  163. Rosas-Galván NS, Martínez-Morales F, Marquina-Bahena S et al (2018) Improved production, purification, and characterization of biosurfactants produced by Serratia marcescens SM3 and its isogenic SMRG-5 strain. Biotechnol Appl Biochem 25:1254. Google Scholar
  164. Salnikov ES, Mason AJ, Bechinger B (2009) Membrane order perturbation in the presence of antimicrobial peptides by 2H solid-state NMR spectroscopy. Biochimie 91:734–743Google Scholar
  165. Schagina LV, Kaulin YA, Feigin AM et al (1998) Properties of ionic channels formed by the antibiotic syringomycin E in lipid bilayers: dependence on the electrolyte concentration in the bathing solution. Membr Cell Biol. 12:537–555Google Scholar
  166. Schagina LV, Gurnev PA, Takemoto JY, Malev VV (2003) Effective gating charge of ion channels induced by toxin syringomycin E in lipid bilayers. Bioelectrochemistry 60:21–27. Google Scholar
  167. Schneider T, Müller A, Miess H, Gross H (2014) Cyclic lipopeptides as antibacterial agents – potent antibiotic activity mediated by intriguing mode of actions. Int J Med Microbiol 304:37–43. Google Scholar
  168. Seydlová G, Sokol A, Lišková P et al (2018) Daptomycin pore formation and stoichiometry depend on membrane potential of target membrane. Antimicrob Agents Chemother 63(1):e01589-18. Google Scholar
  169. Shen HH, Thomas RK, Penfold J, Fragneto G (2010) Destruction and solubilization of supported phospholipid bilayers on silica by the biosurfactant surfactin. Langmuir 26:7334–7342. Google Scholar
  170. Sheppard JD, Jumarie C, Cooper DG, Laprade R (1991) Ionic channels induced by surfactin in planar lipid bilayer membranes. Biochim Biophys Acta 1064:13–23. Google Scholar
  171. Shishido TK, Humisto A, Jokela J et al (2015a) Antifungal compounds from cyanobacteria. Mar Drugs. 13:2124–2140. Google Scholar
  172. Shishido TK, Humisto A, Jokela J (2015b) Antifungal compounds from cyanobacteria. Mar Drugs. 13:2124–2140. Google Scholar
  173. Shoemaker DM, Simou J, Roland WE (2006) A review of daptomycin for injection (Cubicin) in the treatment of complicated skin and skin structure infections. Ther Clin Risk Manag 2:169–174Google Scholar
  174. Silverman JA, Perlmutter NG, Shapiro HM (2003) Correlation of Daptomycin bactericidal activity and membrane depolarization in Staphylococcus aureus. Antimicrob Agents Chemother 47:2538–2544. Google Scholar
  175. Singh SB, Ondeyka J, Harris G et al (2013) Isolation, structure, and biological activity of Phaeofungin, a cyclic lipodepsipeptide from a Phaeosphaeria sp. using the genome-wide Candida albicans fitness test. J Nat Prod 76:334–345. Google Scholar
  176. Sproul G (2015) Abiogenic syntheses of lipoamino acids and lipopeptides and their prebiotic significance. Orig Life Evol Biosph 45:427–437. Google Scholar
  177. Steenbergen JN, Alder J, Thorne GM, Tally FP (2005) Daptomycin: a lipopeptide antibiotic for the treatment of serious Gram-positive infections. J Antimicrob Chemother 55:283–288. Google Scholar
  178. Stefaniu C, Brezesinski G, Möhwald H (2014) Langmuir monolayers as models to study processes at membrane surfaces. Adv Colloid Interface Sci 208:197–213. Google Scholar
  179. Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56:845–857. Google Scholar
  180. Strobel GA, Morrison SL, Cassella M (2005) Protecting plants from oomycete pathogens by treatment with compositions containing serratamolide andoocydin A from Serratia marcescens. Patent Number: US2003049230-A1; US6926892-B2Google Scholar
  181. Sun Y, Sun TL, Huang HW (2016) Mode of action of antimicrobial peptides on E. coli spheroplasts. Biophys J 111:132–139. Google Scholar
  182. Sur S, Romo TD, Grossfield A (2018) Selectivity and mechanism of Fengycin, an antimicrobial lipopeptide, from molecular dynamics. J Phys Chem B. 122:2219–2226. Google Scholar
  183. Tabbene O, Kalai L, Ben Slimene I et al (2011) Anti-candida effect of bacillomycin D-like lipopeptides from Bacillus subtilis B38. FEMS Microbiol Lett 316:108–114. Google Scholar
  184. Takemoto JY, Giannini JL, Vassey T, Briskin DP (1989) Syringomycin effects on plasma membrane Ca2+ transport. In: Graniti A, Durbin RD, Ballio A (eds) Phytotoxins and plant pathogenesis. Springer-Verlag, Berlin, pp 167–175Google Scholar
  185. Takemoto JY, Brand JG, Kaulin YA et al (2003) The syringomycins. In: Menestrina G, Dalla Serra M, Lazarovici P (eds) Pore-forming peptides and protein toxins, 1st edn. Taylor & Francis, London, pp 260–271Google Scholar
  186. Taylor SD (2018) The lipopeptide antibiotic Daptomycin: Its interaction with calcium and membranes, and the effects of membrane lipid composition on its activity. Dissertation, University of Waterloo Taylor SD, Palmer M (2016). The action mechanism of daptomycin. Bioorg Med Chem. 24:6253-6268. -->Google Scholar
  187. Taylor R, Beriashvili D, Taylor S, Palmer M (2017) Daptomycin pore formation is restricted by lipid acyl chain composition. ACS Infect Dis. 3:797–801. Google Scholar
  188. Thasana N, Prapagdee B, Rangkadilok N et al (2010) Bacillus subtilis SSE4 produces subtulene A a new lipopeptide antibiotic possessing an unusual C15 unsaturated beta-amino acid. FEBS Lett 584:3209–3214. Google Scholar
  189. Thies S, Santiago-Schübel B, Kovačić F et al (2014) Heterologous production of the lipopeptide biosurfactant serrawettin W1 in Escherichia coli. J Biotechnol 181:27–30. Google Scholar
  190. Thimon L, Peypoux F, Wallach J, Michel G (1995) Effect of the lipopeptide antibiotic, iturin A, on morphology and membrane ultrastructure of yeast cells. FEMS Microbiol Lett 128:101–106. Google Scholar
  191. Vestola J, Shishido TK, Jokela J et al (2014) Hassallidins, antifungal glycolipopeptides, are widespread among cyanobacteria and are the end-product of a nonribosomal pathway. Proc Natl Acad Sci U S A. 111:E1909–E1917. Google Scholar
  192. Voinov MA, Rivera-Rivera I, Smirnov AI (2013) Surface electrostatics of lipid bilayers by EPR of a pH-sensitive spin-labeled lipid. Biophys J 104:106–116. Google Scholar
  193. Vollenbroich D, Ozel M, Vater J et al (1997a) Mechanism of inactivation of enveloped viruses by biosurfactant surfactin from Bacillus subtilis. Biologicals 25:289–297Google Scholar
  194. Vollenbroich D, Pauli G, Ozel M, Vater J (1997b) Antimycoplasma properties and application in cell culture of surfactin, a lipopeptide antibiotic from Bacillus subtilis. Appl Environ Microbiol 63:44–49Google Scholar
  195. Volpon L, Besson F, Lancelin JM (1999) NMR structure of active and inactive forms of the sterol-dependent antifungal antibiotic bacillomycin L. Eur J Biochem 264:200–210. Google Scholar
  196. Wangspa R, Takemoto JY (1998) Role of ergosterol in growth inhibition of Saccharomyces cerevisiae by syringomycin E. FEMS Microbiol Lett 167:215–220Google Scholar
  197. Wise C, Falardeau J, Hagberg I, Avis TJ (2014) Cellular lipid composition affects sensitivity of plant pathogens to fengycin, an antifungal compound produced by Bacillus subtilis strain CU12. Phytopathology. 104:1036–1041. Google Scholar
  198. Xiu P, Liu R, Zhang D, Sun C (2017) Pumilacidin-like lipopeptides derived from marine bacterium Bacillus sp. strain 176 suppress the motility of Vibrio alginolyticus. Appl Environ Microbiol 83(12):e00450-17. Google Scholar
  199. Xue Y, Wang M, Zhao P et al (2018) Gram-negative bacilli-derived peptide antibiotics developed since 20. Biotechnol Lett. Google Scholar
  200. Yamamoto S, Shiraishi S, Suzuki S (2015) Are cyclic lipopeptides produced by Bacillus amyloliquefaciens S13-3 responsible for the plant defence response in strawberry against Colletotrichum gloeosporioides? Lett Appl Microbiol 60:379–386. Google Scholar
  201. Yang Q, Guo Y, Li L, Hui SW (1997) Effects of lipid headgroup and packing stress on poly(ethylene glycol)-induced phospholipid vesicle aggregation and fusion. Biophys J 73:277–282. Google Scholar
  202. Yu WB, Ye BC (2016) High-level iron mitigates fusaricidin-induced membrane damage and reduces membrane fluidity leading to enhanced drug resistance in Bacillus subtilis. J Basic Microbiol 56(5):502–509. Google Scholar
  203. Zhang L, Takemoto JY (1987) Effects of Pseudomonas syringae phytotoxin, syringomycin, on plasma membrane fractions of Rhodotorula pilimanae. Phytopathology 77:297–303Google Scholar
  204. Zhang T, Muraih JK, MacCormick B et al (2014a) Daptomycin forms cation- and size-selective pores in model membranes. Biochim Biophys Acta 1838:2425–2430. Google Scholar
  205. Zhang T, Muraih JK, Tishbi N et al (2014b) Cardiolipin prevents membrane translocation and permeabilization by daptomycin. J Biol Chem 289:11584–11591. Google Scholar
  206. Zhang J, Scoten K, Straus SK (2016) Daptomycin leakage is selective. ACS Infect Dis. 2(10):682–687. Google Scholar
  207. Zhang J, Scott WRP, Gabel F et al (2017) On the quest for the elusive mechanism of action of daptomycin: binding, fusion, and oligomerization. Biochim Biophys Acta 1865:1490–1499. Google Scholar
  208. Zhao H, Shao D, Jiang C et al (2017) Biological activity of lipopeptides from Bacillus. Appl Microbiol Biotechnol 101:5951–5960. Google Scholar
  209. Zhao P, Xue Y, Gao W et al (2018) Bacillaceae-derived peptide antibiotics since 2000. Peptides 101:10–16. Google Scholar
  210. Zhao P, Xue Y, Li X et al (2019) Fungi-derived lipopeptide antibiotics developed since 2000. Peptides 113:52–65. Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Chemistry ICETUniversidad Autónoma de GuadalajaraZapopanMexico
  2. 2.CNR-Nanoscience Institute-S3ModenaItaly
  3. 3.Department of Physics, Informatics and MathematicsUniversity of Modena and Reggio EmiliaModenaItaly

Personalised recommendations