[en] Microbial natural products are widely explored for their therapeutic potential. Understanding the underlying evolutionary and adaptive forces driving their production remains a fundamental question in biology. Amphiphilic cyclic lipopeptides (CLPs), a prominent category of bacterial specialized metabolites, show strong antimicrobial activity, particularly against phytopathogens. It is thus assumed that these compounds are deployed by soil- or rhizosphere-dwelling bacteria as microbial weapons in competitive natural environments. Here, we challenge this reductionist perspective and present evidence that Bacillus CLPs are prominent chemical mediators of ecological interactions. They help Bacillus to communicate, compete, defend against predators, or cooperate and establish mutualistic relationships with other (micro)organisms. Additional parallel examples are highlighted in other genera, such as Pseudomonas. This broader perspective underscores the need for further investigation into the role of CLPs in shaping the adaptive strategies of key rhizobacterial species.
Höfte, Monica ✱; Laboratory of Phytopathology, Faculty of Bioscience Engineering, Ghent University, Ghent, 9000, Belgium
Arguelles-Arias, Anthony; Microbial Processes and Interactions laboratory, TERRA Research Centre, Gembloux Agro-Bio Tech, University of Liège, Gembloux, 5030, Belgium
Deleu, Magali ✱; Université de Liège - ULiège > TERRA Research Centre > Chemistry for Sustainable Food and Environmental Systems (CSFES)
Ongena, Marc ✱; Université de Liège - ULiège > TERRA Research Centre > Microbial technologies
✱ These authors have contributed equally to this work.
Language :
English
Title :
Bacillus lipopeptides as key players in rhizosphere chemical ecology.
F.R.S.-FNRS - Fonds de la Recherche Scientifique Interreg Europe
Funding text :
The authors would like to thank Thibault Meyer, Gregory Hoff, and Guillaume Gilliard for insightful discussions during the preparation of this review. G.B. is recipient of a FRIA fellowship at the F.R.S.-FNRS (National Fund for Scientific Research in Belgium). M.D. and M.O. are respectively senior research associate and research director at F.R.S.-FNRS. Work in the laboratory of M.O. was supported by the EU Interreg V France-Wallonie-Vlaanderen portfolio SmartBiocontrol (Agreement grant No. 731077 ), the PDR research project ID 26084552 and the EOS project ID 30650620 (FWO/F.R.S.-FNRS).
Clements-Decker, T., et al. Underexplored bacteria as reservoirs of novel antimicrobial lipopeptides. Front. Chem., 10, 2022, 1025979.
Zhang, S., et al. Structural diversity, biosynthesis, and biological functions of lipopeptides from Streptomyces. Nat. Prod. Rep. 40 (2023), 557–594.
Romanowski, S.B., et al. Identification of the lipodepsipeptide selethramide encoded in a giant nonribosomal peptide synthetase from a Burkholderia bacterium. Proc. Natl. Acad. Sci. U. S. A., 120, 2023, e2304668120.
Bach, E., et al. Burkholderia in the genomic era: from taxonomy to the discovery of new antimicrobial secondary metabolites. Crit. Rev. Microbiol. 48 (2022), 121–160.
Fewer, D.P., et al. Chemical diversity and cellular effects of antifungal cyclic lipopeptides from cyanobacteria. Physiol. Plant. 173 (2021), 639–650.
Naughton, P.J., et al. Microbial biosurfactants: current trends and applications in agricultural and biomedical industries. J. Appl. Microbiol. 127 (2019), 12–28.
Olishevska, S., et al. Bacillus and Paenibacillus secreted polyketides and peptides involved in controlling human and plant pathogens. Appl. Microbiol. Biotechnol. 103 (2019), 1189–1215.
Cesa-Luna, C., et al. Charting the lipopeptidome of nonpathogenic Pseudomonas. mSystems, 8, 2023, e00988–22.
Dang, Y., et al. Enhanced production of antifungal lipopeptide iturin A by Bacillus amyloliquefaciens LL3 through metabolic engineering and culture conditions optimization. Microb. Cell Factories, 18, 2019, 68.
Blake, C., et al. Molecular aspects of plant growth promotion and protection by Bacillus subtilis. Mol. Plant-Microbe Interact. 34 (2021), 15–25.
Rabbee, M.F., et al. Bacillus velezensis: a beneficial biocontrol agent or facultative phytopathogen for sustainable agriculture. Agronomy, 13, 2023, 840.
Götze, S., Stallforth, P., Structure, properties, and biological functions of nonribosomal lipopeptides from pseudomonads. Nat. Prod. Rep. 37 (2020), 29–54.
Kaspar, F., et al. Bioactive secondary metabolites from Bacillus subtilis: a comprehensive review. J. Nat. Prod. 82 (2019), 2038–2053.
Kiesewalter, H.T., et al. Genomic and chemical diversity of Bacillus subtilis secondary metabolites against plant pathogenic fungi. mSystems, 6, 2021, e00770–20.
Hoff, G., et al. Surfactin stimulated by pectin molecular patterns and root exudates acts as a key driver of the Bacillus–plant mutualistic interaction. MBio, 12, 2021, e01774–21.
Andrić, S., et al. Plant-associated Bacillus mobilizes its secondary metabolites upon perception of the siderophore pyochelin produced by a Pseudomonas competitor. ISME J. 17 (2023), 263–275.
Duban, M., et al. Nonribosomal peptide synthesis definitely working out of the rules. Microorganisms, 10, 2022, 577.
Théatre, A., et al. Bacillus sp.: a remarkable source of bioactive lipopeptides. Adv. Biochem. Eng. Biotechnol. 181 (2022), 123–179.
Luo, C., et al. Unusual biosynthesis and structure of locillomycins from Bacillus subtilis 916. Appl. Environ. Microbiol. 81 (2015), 6601–6609.
Béchet, M., et al. Structure, biosynthesis, and properties of kurstakins, nonribosomal lipopeptides from Bacillus spp. Appl. Microbiol. Biotechnol. 95 (2012), 593–600.
Lee, S.C., et al. Isolation and structural analysis of bamylocin A, novel lipopeptide from Bacillus amyloliquefaciens LP03 having antagonistic and crude oil-emulsifying activity. Arch. Microbiol. 188 (2007), 307–312.
Biria, D., et al. Purification and characterization of a novel biosurfactant produced by Bacillus licheniformis MS3. World J. Microbiol. Biotechnol. 26 (2010), 871–878.
Steinke, K., et al. Phylogenetic distribution of secondary metabolites in the Bacillus subtilis species complex. mSystems, 6, 2021, e00057–21.
Girard, L., et al. Lipopeptide families at the interface between pathogenic and beneficial Pseudomonas–plant interactions. Crit. Rev. Microbiol. 46 (2020), 397–419.
Zhou, L., et al. Does regulation hold the key to optimizing lipopeptide production in Pseudomonas for biotechnology?. Front. Bioeng. Biotechnol., 12, 2024, 1363183.
Jautzus, T., et al. Complex extracellular biology drives surface competition during colony expansion in Bacillus subtilis. ISME J. 16 (2022), 2320–2328.
Grau, R.R., et al. A duo of potassium-responsive histidine kinases govern the multicellular destiny of Bacillus subtilis. MBio, 6, 2015, e00581.
Cao, Y., et al. Antagonism of two plant-growth promoting Bacillus velezensis isolates against Ralstonia solanacearum and Fusarium oxysporum. Sci. Rep., 8, 2018, 4360.
van Gestel, J., et al. From cell differentiation to cell collectives: Bacillus subtilis uses division of labor to migrate. PLoS Biol., 13, 2015, e1002141.
Ghelardi, E., et al. Contribution of surfactin and SwrA to flagellin expression, swimming, and surface motility in Bacillus subtilis. Appl. Environ. Microbiol. 78 (2012), 6540–6544.
Guan, Y., et al. The potential of Pseudomonas fluorescens SBW25 to produce viscosin enhances wheat root colonization and shapes root-associated microbial communities in a plant genotype-dependent manner in soil systems. mSphere, 21, 2024, e0029424.
Andrić, S., et al. Lipopeptide interplay mediates molecular interactions between soil bacilli and pseudomonads. Microbiol. Spectr., 9, 2021, e02038–21.
Arnaouteli, S., et al. Bacillus subtilis biofilm formation and social interactions. Nat. Rev. Microbiol. 19 (2021), 600–614.
Nordgaard, M., et al. Deletion of Rap-Phr systems in Bacillus subtilis influences in vitro biofilm formation and plant root colonization. Microbiologyopen, 10, 2021, e1212.
Boubsi, F., et al. Pectic homogalacturonan sensed by Bacillus acts as host associated cue to promote establishment and persistence in the rhizosphere. iScience, 26, 2023, 107925.
Thérien, M., et al. Surfactin production is not essential for pellicle and root-associated biofilm development of Bacillus subtilis. Biofilm, 2, 2020, 100021.
Luo, C., et al. Bacillomycin L and surfactin contribute synergistically to the phenotypic features of Bacillus subtilis 916 and the biocontrol of rice sheath blight induced by Rhizoctonia solani. Appl. Microbiol. Biotechnol. 99 (2015), 1897–1910.
Arnaouteli, S., et al. Just in case it rains: building a hydrophobic biofilm the Bacillus subtilis way. Curr. Opin. Microbiol. 34 (2016), 7–12.
Molina-Santiago, C., et al. The extracellular matrix protects Bacillus subtilis colonies from Pseudomonas invasion and modulates plant co-colonization. Nat. Commun., 10, 2019, 1919.
Danevčič, T., et al. Surfactin facilitates horizontal gene transfer in Bacillus subtilis. Front. Microbiol., 12, 2021, 657407.
Balleza, D., et al. Role of lipid composition, physicochemical interactions, and membrane mechanics in the molecular actions of microbial cyclic lipopeptides. J. Membr. Biol. 252 (2019), 131–157.
Aranda, F.J., et al. Recent advances on the interaction of glycolipid and lipopeptide biosurfactants with model and biological membranes. Curr. Opin. Colloid Interface Sci., 68, 2023, 101748.
Cochrane, S.A., Vederas, J.C., Lipopeptides from Bacillus and Paenibacillus spp.: a gold mine of antibiotic candidates. Med. Res. Rev. 36 (2016), 4–31.
Fiedler, S., Heerklotz, H., Vesicle leakage reflects the target selectivity of antimicrobial lipopeptides from Bacillus subtilis. Biophys. J. 109 (2015), 2079–2089.
Mantil, E., et al. Domain redistribution within ergosterol-containing model membranes in the presence of the antimicrobial compound fengycin. Biochim. Biophys. Acta Biomembr. 1861 (2019), 738–747.
Humisto, A., et al. Characterization of the interaction of the antifungal and cytotoxic cyclic glycolipopeptide hassallidin with sterol-containing lipid membranes. Biochim. Biophys. Acta Biomembr. 1861 (2019), 1510–1521.
Zakharova, A.A., et al. Fengycin induces ion channels in lipid bilayers mimicking target fungal cell membranes. Sci. Rep., 9, 2019, 16034.
Desmyttere, H., et al. Antifungal activities of Bacillus subtilis lipopeptides to two Venturia inaequalis strains possessing different tebuconazole sensitivity. Front. Microbiol., 10, 2019, 2327.
Gilliard, G., et al. Deciphering the distinct biocontrol activities of lipopeptides fengycin and surfactin through their differential impact on lipid membranes. Colloids Surf. B Biointerfaces, 239, 2024, 113933.
Richter, A., et al. Enhanced surface colonisation and competition during bacterial adaptation to a fungus. Nat. Commun., 15, 2024, 4486.
Zhang, L., Sun, C., Fengycins, cyclic lipopeptides from marine Bacillus subtilis strains, kill the plant-pathogenic fungus Magnaporthe grisea by inducing reactive oxygen species production and chromatin condensation. Appl. Environ. Microbiol., 84, 2018, e00445–18.
Wang, Z., et al. Bioinformatic prospecting and synthesis of a bifunctional lipopeptide antibiotic that evades resistance. Science 376 (2022), 991–996.
Wang, X., et al. Antifungal effects and biocontrol potential of lipopeptide-producing Streptomyces against banana Fusarium wilt fungus Fusarium oxysporum f. sp. cubense. Front. Microbiol., 14, 2023, 1177393.
Götze, S., et al. Ecological niche-inspired genome mining leads to the discovery of crop-protecting nonribosomal lipopeptides featuring a transient amino acid building block. J. Am. Chem. Soc. 145 (2023), 2342–2353.
Pflanze, S., et al. Nonribosomal peptides protect Pseudomonas nunensis 4A2e from amoebal and nematodal predation. Chem. Sci. 14 (2023), 11573–11581.
Medeot, D.B., et al. Fengycins from Bacillus amyloliquefaciens MEP218 exhibit antibacterial activity by producing alterations on the cell surface of the pathogens Xanthomonas axonopodis pv. vesicatoria and Pseudomonas aeruginosa PA01. Front. Microbiol., 10, 2020, 3107.
Peterson, S.B., et al. The central role of interbacterial antagonism in bacterial life. Curr. Biol. 30 (2020), R1203–R1214.
Straight, P.D., et al. Interactions between Streptomyces coelicolor and Bacillus subtilis: Role of surfactants in raising aerial structures. J. Bacteriol. 188 (2006), 4918–4925.
Almoneafy, A.A., et al. Tomato plant growth promotion and antibacterial related-mechanisms of four rhizobacterial Bacillus strains against Ralstonia solanacearum. Symbiosis 63 (2014), 59–70.
Bais, H.P., et al. Biocontrol of Bacillus subtilis against infection of arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol. 134 (2004), 307–319.
Nakamoto, H., et al. A cyclic lipopeptide surfactin is a species-selective Hsp90 inhibitor that suppresses cyanobacterial growth. J. Biochem. 170 (2021), 255–264.
Rosenberg, G., et al. Not so simple, not so subtle: the interspecies competition between Bacillus simplex and Bacillus subtilis and its impact on the evolution of biofilms. npj Biofilms Microbiomes, 2, 2016, 15027.
Hou, Y., et al. A cyclic lipopeptide produced by an antagonistic bacterium relies on its tail and transient receptor potential-type Ca2+ channels to immobilize a green alga. New Phytol. 237 (2023), 1620–1635.
Stubbendieck, R.M., et al. Linearmycins are lytic membrane-targeting antibiotics. J. Antibiot. (Tokyo) 71 (2018), 372–381.
Brown, L., et al. Bacillus subtilis are disrupted by the lipopeptide surfactin. Mol. Microbiol. 93 (2014), 183–198.
Luzzatto-Knaan, T., et al. Mass spectrometry uncovers the role of surfactin as an interspecies recruitment factor. ACS Chem. Biol. 14 (2019), 459–467.
Molina-Santiago, C., et al. Chemical interplay and complementary adaptative strategies toggle bacterial antagonism and co-existence. Cell Rep., 36, 2021, 109449.
Zhang, L., et al. Arbuscular mycorrhizal fungi conducting the hyphosphere bacterial orchestra. Trends Plant Sci. 27 (2022), 402–411.
Anckaert, A., et al. Deciphering the biology and chemistry of the mutualistic partnership between Bacillus velezensis and the arbuscular mycorrhizal fungus Rhizophagus irregularis. bioRxiv, 2023 Published online October 23, 2023. https://doi.org/10.1101/2023.10.28.564539.
Pršić, J., Ongena, M., Elicitors of plant immunity triggered by beneficial bacteria. Front. Plant Sci., 11, 2020, 594530.
Berlanga-Clavero, M.V., et al. Bacillus subtilis biofilm matrix components target seed oil bodies to promote growth and anti-fungal resistance in melon. Nat. Microbiol. 7 (2022), 1001–1015.
Pieterse, C.M.J., et al. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52 (2014), 347–375.
Omoboye, O.O., et al. Pseudomonas cyclic lipopeptides suppress the rice blast fungus Magnaporthe oryzae by induced resistance and direct antagonism. Front. Plant Sci., 10, 2019, 901.
Ma, Z., et al. The cyclic lipopeptide orfamide induces systemic resistance in rice to Cochliobolus miyabeanus but not to Magnaporthe oryzae. Plant Cell Rep. 36 (2017), 1731–1746.
Lam, V.B., et al. 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, 9, 2021, 1441.
Platel, R., et al. Deciphering immune responses primed by a bacterial lipopeptide in wheat towards Zymoseptoria tritici. Front. Plant Sci., 13, 2023, 1074447.
Hoefler, B.C., et al. Enzymatic resistance to the lipopeptide surfactin as identified through imaging mass spectrometry of bacterial competition. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 13082–13087.
Rigolet, A., et al. Lipopeptides as rhizosphere public goods for microbial cooperation. Microbiol. Spectr., 12, 2024, e03106–23.
Hermenau, R., et al. Helper bacteria halt and disarm mushroom pathogens by linearizing structurally diverse cyclolipopeptides. Proc. Natl. Acad. Sci. U. S. A. 117 (2020), 23802–23806.
Zhang, S., et al. Lipopeptide-mediated bacterial interaction enables cooperative predator defense. Proc. Natl. Acad. Sci. U. S. A., 118, 2021, e2013759118.
Hansen, M.L., et al. Resistance towards and biotransformation of a Pseudomonas -produced secondary metabolite during community invasion. ISME J., 18, 2024, wrae105.
Chevrette, M.G., et al. Microbiome composition modulates secondary metabolism in a multispecies bacterial community. Proc. Natl. Acad. Sci. U. S. A., 119, 2022, e2212930119.
Tian, T., et al. Sucrose triggers a novel signaling cascade promoting Bacillus subtilis rhizosphere colonization. ISME J. 15 (2021), 2723–2737.
Wu, K., et al. Pectin enhances bio-control efficacy by inducing colonization and secretion of secondary metabolites by Bacillus amyloliquefaciens SQY 162 in the rhizosphere of tobacco. PLoS One, 10, 2015, e0127418.
Wang, N., et al. The expression of genes encoding lipodepsipeptide phytotoxins by Pseudomonas syringae pv. syringae is coordinated in response to plant signal molecules. Mol. Plant Microbe Interact. 19 (2006), 257–269.
DeFilippi, S., et al. Fungal competitors affect production of antimicrobial lipopeptides in Bacillus subtilis strain B9–5. J. Chem. Ecol. 44 (2018), 374–383.
Pandin, C., et al. Biofilm formation and synthesis of antimicrobial compounds by the biocontrol agent Bacillus velezensis QST713 in an Agaricus bisporus compost micromodel. Appl. Environ. Microbiol., 85, 2019, e00327–19.
Ma, Q., et al. Effects of mixed culture fermentation of Bacillus amyloliquefaciens and Trichoderma longibrachiatum on its constituent strains and the biocontrol of tomato Fusarium wilt. J. Appl. Microbiol. 132 (2022), 532–546.
Albarracín Orio, A.G., et al. Fungal–bacterial interaction selects for quorum sensing mutants with increased production of natural antifungal compounds. Commun. Biol., 3, 2020, 670.
Xue, J., et al. Bacillus atrophaeus NX-12 utilizes exosmotic glycerol from Fusarium oxysporum f. sp. cucumerinum for fengycin production. J. Agric. Food Chem. 71 (2023), 10565–10574.
Liu, Y., et al. Antibiotic stimulation of a Bacillus subtilis migratory response. mSphere, 3, 2018, e00586–17.
Kakar, K.U., et al. A novel rhizobacterium Bk7 for biological control of brown sheath rot of rice caused by Pseudomonas fuscovaginae and its mode of action. Eur. J. Plant Pathol. 138 (2014), 819–834.
Hennessy, R.C., et al. Biosynthesis of the antimicrobial cyclic lipopeptides nunamycin and nunapeptin by Pseudomonas fluorescens strain In5 is regulated by the LuxR-type transcriptional regulator NunF. Microbiologyopen, 6, 2017, e516.
Christiansen, L., et al. Fungal-associated molecules induce key genes involved in the biosynthesis of the antifungal secondary metabolites nunamycin and nunapeptin in the biocontrol strain Pseudomonas fluorescens In5. Appl. Environ. Microbiol., 86, 2020, e01284–20.
Winn, M., et al. Recent advances in engineering nonribosomal peptide assembly lines. Nat. Prod. Rep. 33 (2016), 317–347.
Dunlap, C.A., Taxonomy of registered Bacillus spp. strains used as plant pathogen antagonists. Biol. Control 134 (2019), 82–86.
Rahman, F. Bin, et al. Molecular genetics of surfactin and its effects on different sub-populations of Bacillus subtilis. Biotechnol. Reports, 32, 2021, e00686.
Rojas-Tapias, D.F., Helmann, J.D., Roles and regulation of Spx family transcription factors in Bacillus subtilis and related species. Adv. Microb. Physiol. 75 (2019), 279–323.
Sun, J., et al. CodY, ComA, DegU and Spo0A controlling lipopeptides biosynthesis in Bacillus amyloliquefaciens fmbJ. J. Appl. Microbiol. 131 (2021), 1289–1304.
Zhi, Y., et al. Genome and transcriptome analysis of surfactin biosynthesis in Bacillus amyloliquefaciens MT45. Sci. Rep., 7, 2017, 40976.
Yu, C., et al. degQ associated with the degS/degU two-component system regulates biofilm formation, antimicrobial metabolite production, and biocontrol activity in Bacillus velezensis DMW1. Mol. Plant Pathol. 24 (2023), 1510–1521.
Koumoutsi, A., et al. DegU and YczE positively regulate the synthesis of bacillomycin D by Bacillus amyloliquefaciens strain FZB42. Appl. Environ. Microbiol. 73 (2007), 6953–6964.
Xu, Y., et al. Enhanced production of iturin A in Bacillus amyloliquefaciens by genetic engineering and medium optimization. Process Biochem. 90 (2020), 50–57.
Vahidinasab, M., et al. Construction and description of a constitutive plipastatin mono-producing Bacillus subtilis. Microb. Cell Factories, 19, 2020, 205.
Irigül-Sönmez, Ö., et al. In Bacillus subtilis LutR is part of the global complex regulatory network governing the adaptation to the transition from exponential growth to stationary phase. Microbiology 160 (2014), 243–260.
Guo, Q. gang, et al. The PhoR/PhoP two-component system regulates fengycin production in Bacillus subtilis NCD-2 under low-phosphate conditions. J. Integr. Agric. 17 (2018), 149–157.
Aleti, G., et al. Surfactin variants mediate species-specific biofilm formation and root colonization in Bacillus. Environ. Microbiol. 18 (2016), 2634–2645.
Steigenberger, J., et al. Complex electrostatic effects on the selectivity of membrane-permeabilizing cyclic lipopeptides. Biophys. J. 122 (2023), 950–963.
Steigenberger, J., et al. The optimal lipid chain length of a membrane-permeabilizing lipopeptide results from the balance of membrane partitioning and local damage. Front. Microbiol., 12, 2021, 669709.
Henry, G., et al. The bacterial lipopeptide surfactin targets the lipid fraction of the plant plasma membrane to trigger immune-related defence responses. Cell. Microbiol. 13 (2011), 1824–1837.
Luna-Bulbarela, A., et al. Effects of bacillomycin D homologues produced by Bacillus amyloliquefaciens 83 on growth and viability of Colletotrichum gloeosporioides at different physiological stages. Biol. Control 127 (2018), 145–154.
D'Auria, L., et al. 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 Biomembr. 1828 (2013), 2064–2073.
Nasir, M.N., Besson, F., Interactions of the antifungal mycosubtilin with ergosterol-containing interfacial monolayers. Biochim. Biophys. Acta Biomembr. 1818 (2012), 1302–1308.
Geudens, N., et al. Conformation and dynamics of the cyclic lipopeptide viscosinamide at the water-lipid interface. Molecules, 24, 2019, 24122257.
Gilliard, G., et al. Added value of biophysics to study lipid-driven biological processes: The case of surfactins, a class of natural amphiphile molecules. Int. J. Mol. Sci., 23, 2022, 232213831.
Mamode Cassim, A., et al. Plant lipids: key players of plasma membrane organization and function. Prog. Lipid Res. 73 (2019), 1–27.
Herrfurth, C., et al. Targeted analysis of the plant lipidome by UPLC-NanoESI-MS/MS. Methods Mol. Biol. 2295 (2021), 135–155.
Hsieh, M.K., et al. All-atom modeling of complex cellular membranes. Langmuir 38 (2022), 3–17.
Sur, S., et al. Selectivity and mechanism of fengycin, an antimicrobial lipopeptide, from molecular dynamics. J. Phys. Chem. B 122 (2018), 2219–2226.
