{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,29]],"date-time":"2026-05-29T21:32:39Z","timestamp":1780090359709,"version":"3.54.0"},"reference-count":41,"publisher":"MDPI AG","issue":"15","license":[{"start":{"date-parts":[[2023,7,27]],"date-time":"2023-07-27T00:00:00Z","timestamp":1690416000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Individual project for a young scientist at the Institute of Biological Sciences of the Maria Curie-Sk\u0142odowska University","award":["MN\/2021\/7"],"award-info":[{"award-number":["MN\/2021\/7"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Legionella gormanii is a fastidious, Gram-negative bacterium known to be the etiological agent of atypical community-acquired pneumonia. The human cathelicidin LL-37 exhibits a dose-dependent bactericidal effect on L. gormanii. The LL-37 peptide at the concentration of 10 \u00b5M causes the bacteria to become viable but not cultured. The antibacterial activity of the peptide is attributed to its effective binding to the bacterial membrane, as demonstrated by the fluorescence lifetime imaging microscopy. In this study, to mimic the L. gormanii membranes and their response to the antimicrobial peptide, Langmuir monolayers were used with the addition of the LL-37 peptide to the subphase of the Langmuir trough to represent the extracellular fluid. The properties of the model membranes (Langmuir monolayers) formed by phospholipids (PL) isolated from the L.\u00a0gormanii bacteria cultured on the non-supplemented (PL\u2212choline) and choline-supplemented (PL+choline) medium were determined, along with the effect of the LL-37 peptide on the intermolecular interactions, packing, and ordering under the monolayer compression. Penetration tests at the constant surface pressure were carried out to investigate the mechanism of the LL-37 peptide action on the model membranes. The peptide binds to the anionic bacterial membranes preferentially, due to its positive charge. Upon binding, the LL-37 peptide can penetrate into the hydrophobic tails of phospholipids, destabilizing membrane integrity. The above process can entail membrane disruption and ultimately cell death. The ability to evoke such a great membrane destabilization is dependent on the share of electrostatic, hydrogen bonding and Lifshitz\u2013van der Waals LL-37\u2212PL interactions. Thus, the LL-37 peptide action depends on the changes in the lipid membrane composition caused by the utilization of exogenous choline by the L. gormanii.<\/jats:p>","DOI":"10.3390\/ijms241512039","type":"journal-article","created":{"date-parts":[[2023,7,28]],"date-time":"2023-07-28T01:51:47Z","timestamp":1690509107000},"page":"12039","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Insight into the Mechanism of Interactions between the LL-37 Peptide and Model Membranes of Legionella gormanii Bacteria"],"prefix":"10.3390","volume":"24","author":[{"given":"Katarzyna","family":"Pastuszak","sequence":"first","affiliation":[{"name":"Department of Interfacial Phenomena, Institute of Chemical Sciences, Faculty of Chemistry, Maria Curie-Sk\u0142odowska University, Maria Curie-Sk\u0142odowska Sq. 3, 20-031 Lublin, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bozena","family":"Kowalczyk","sequence":"additional","affiliation":[{"name":"Department of Genetics and Microbiology, Institute of Biological Sciences, Faculty of Biology and Biotechnology, Maria Curie-Sk\u0142odowska University, Akademicka 19, 20-033 Lublin, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jacek","family":"Tarasiuk","sequence":"additional","affiliation":[{"name":"Department of Genetics and Microbiology, Institute of Biological Sciences, Faculty of Biology and Biotechnology, Maria Curie-Sk\u0142odowska University, Akademicka 19, 20-033 Lublin, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1156-8059","authenticated-orcid":false,"given":"Rafal","family":"Luchowski","sequence":"additional","affiliation":[{"name":"Department of Biophysics, Institute of Physics, Faculty of Mathematics, Physics and Informatics, Maria Curie-Sk\u0142odowska University, Radziszewskiego 10, 20-031 Lublin, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8245-3913","authenticated-orcid":false,"given":"Wieslaw I.","family":"Gruszecki","sequence":"additional","affiliation":[{"name":"Department of Biophysics, Institute of Physics, Faculty of Mathematics, Physics and Informatics, Maria Curie-Sk\u0142odowska University, Radziszewskiego 10, 20-031 Lublin, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5365-7677","authenticated-orcid":false,"given":"Ma\u0142gorzata","family":"Jurak","sequence":"additional","affiliation":[{"name":"Department of Interfacial Phenomena, Institute of Chemical Sciences, Faculty of Chemistry, Maria Curie-Sk\u0142odowska University, Maria Curie-Sk\u0142odowska Sq. 3, 20-031 Lublin, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marta","family":"Palusinska-Szysz","sequence":"additional","affiliation":[{"name":"Department of Genetics and Microbiology, Institute of Biological Sciences, Faculty of Biology and Biotechnology, Maria Curie-Sk\u0142odowska University, Akademicka 19, 20-033 Lublin, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,7,27]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"726","DOI":"10.1097\/00006454-198910000-00014","article-title":"Legionella gormanii pneumonia in a child with chronic granulomatous disease","volume":"8","author":"Ephros","year":"1989","journal-title":"Pediatr. Infect. Dis. J."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2180","DOI":"10.1128\/JCM.00380-15","article-title":"Microbiological and clinical studies of legionellosis in 33 patients with cancer","volume":"53","author":"Han","year":"2015","journal-title":"J. Clin. Microbiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"819425","DOI":"10.3389\/fmed.2022.819425","article-title":"Case report: Community-acquired Legionella gormanii pneumonia in an immunocompetent patient detected by metagenomic next-generation sequencing","volume":"9","author":"Lei","year":"2022","journal-title":"Front. Med."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1091964","DOI":"10.3389\/fmicb.2022.1091964","article-title":"Genomic characterization and assessment of pathogenic potential of Legionella spp. Isolates from environmental monitoring","volume":"13","author":"Svetlicic","year":"2023","journal-title":"Front. Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"388","DOI":"10.3389\/fmicb.2017.00388","article-title":"Distribution of secretion systems in the genus Legionella and its correlation with pathogenicity","volume":"8","author":"Qin","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Chmiel, E., Galuska, C.E., Koper, P., Kowalczyk, B., Urbanik-Sypniewska, T., Palusi\u0144ska-Szysz, M., and Fuchs, B. (2022). Unusual lipid components of Legionella gormanii membranes. Metabolites, 12.","DOI":"10.3390\/metabo12050418"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"ftz065","DOI":"10.1093\/femspd\/ftz065","article-title":"Genetic diversity of Legionella pcs and PmtA genes and the effect of utilization of choline by Legionella spp. on induction of proinflammatory cytokines","volume":"77","author":"Janczarek","year":"2019","journal-title":"Pathog. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Pastuszak, K., Chmiel, E., Kowalczyk, B., Tarasiuk, J., Jurak, M., and Palusi\u0144ska-Szysz, M. (2023). Physicochemical characteristics of model membranes composed of Legionella gormanii lipids. Membranes, 13.","DOI":"10.3390\/membranes13030356"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1186\/1465-9921-11-93","article-title":"Legionella pneumophila induces human beta defensin-3 in pulmonary cells","volume":"11","author":"Scharf","year":"2010","journal-title":"Respir. Res."},{"key":"ref_10","first-page":"8349712","article-title":"Significance of LL-37 on immunomodulation and disease outcome","volume":"2020","author":"Yang","year":"2020","journal-title":"BioMed Res. Int."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Zeth, K., and Sancho-Vaello, E. (2021). Structural plasticity of LL-37 indicates elaborate functional adaptation mechanisms to bacterial target structures. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22105200"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Ridyard, K.E., and Overhage, J. (2021). The potential of human peptide LL-37 as an antimicrobial and anti-biofilm agent. Antibiotics, 10.","DOI":"10.3390\/antibiotics10060650"},{"key":"ref_13","unstructured":"Davies, J.T., and Rideal, E.K. (1963). Interfacial Phenomena, Academic Press."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"5601","DOI":"10.1021\/acs.langmuir.1c00434","article-title":"Analysis of molecular interactions between components in phospholipid-immunosuppressant-antioxidant mixed Langmuir films","volume":"37","author":"Jurak","year":"2021","journal-title":"Langmuir"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"10957","DOI":"10.1007\/s11033-012-1997-x","article-title":"Cathelicidins: Family of antimicrobial peptides. A review","volume":"39","author":"Lisowski","year":"2012","journal-title":"Mol. Biol. Rep."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1275","DOI":"10.1529\/biophysj.105.067595","article-title":"Lipid headgroup discrimination by antimicrobial peptide LL-37: Insight into mechanism of action","volume":"90","author":"Neville","year":"2006","journal-title":"Biophys. J."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"4688","DOI":"10.1529\/biophysj.107.123620","article-title":"Interaction of LL-37 with model membrane systems of different complexity: Influence of the lipid matrix","volume":"94","author":"Sevcsik","year":"2008","journal-title":"Biophys. J."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.colsurfb.2004.06.007","article-title":"Interactions between phosphatidylcholines and cholesterol in monolayers at the air\/water interface","volume":"37","year":"2004","journal-title":"Colloids Surf. B"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1007\/s00232-018-0025-z","article-title":"Properties of artificial phospholipid membranes containing lauryl gallate or cholesterol","volume":"251","author":"Jurak","year":"2013","journal-title":"J. Membr. Biol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1016\/0021-9797(88)90140-3","article-title":"Local surface potentials and electric dipole moments of lipid monolayers: Contributions of the water\/lipid and the lipid\/air interfaces","volume":"126","author":"Vogel","year":"1988","journal-title":"J. Colloid Interface Sci."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Chachaj-Brekiesz, A., Kobierski, J., Wn\u0119trzak, A., and Dynarowicz-Latka, P. (2021). Electrical properties of membrane phospholipids in Langmuir monolayers. Membranes, 11.","DOI":"10.3390\/membranes11010053"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1067","DOI":"10.1046\/j.1365-2958.2003.03614.x","article-title":"Phosphatidylethanolamine and phosphatidylglycerol are segregated into different domains in bacterial membrane. A study with pyrene-labelled phospholipids","volume":"49","author":"Vanounou","year":"2003","journal-title":"Mol. Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"580","DOI":"10.1039\/b900278m","article-title":"Domains in bacterial membranes and the action of antimicrobial agents","volume":"5","author":"Epand","year":"2009","journal-title":"Mol. BioSyst."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"983","DOI":"10.1016\/j.bbamem.2007.11.016","article-title":"Binding of LL-37 to model biomembranes: Insight into target vs host cell recognition","volume":"1778","author":"Sood","year":"2008","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"107842","DOI":"10.1016\/j.bioelechem.2021.107842","article-title":"Interaction of LL-37 human cathelicidin peptide with a model microbial-like lipid membrane","volume":"141","author":"Majewska","year":"2021","journal-title":"Bioelectrochemistry"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/S0005-2736(99)00203-5","article-title":"The monolayer technique: A potent tool for studying the interfacial properties of antimicrobial and membrane-lytic peptides and their interactions with lipid membranes","volume":"1462","year":"1999","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Crosio, M.A., Via, M.A., Camara, C.I., Mangiarotti, A., P\u00f3polo, M.G.D., and Wilke, N. (2019). Interaction of polyarginine peptide with membranes of different mechanical properties. Biomolecules, 9.","DOI":"10.3390\/biom9100625"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Rojewska, M., Smu\u0142ek, W., Kaczorek, E., and Prochaska, K. (2021). Langmuir monolayer techniques for the investigation of model bacterial membranes and antibiotic biodegradation mechanisms. Membranes, 11.","DOI":"10.3390\/membranes11090707"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"27185","DOI":"10.1074\/jbc.M109.026021","article-title":"Phospholipase PlaB of Legionella pneumophila represents a novel lipase family: Protein residues essential for lipolytic activity, substrate specificity, and hemolysis","volume":"284","author":"Bender","year":"2009","journal-title":"J. Biol. Chem."},{"key":"ref_30","first-page":"159138","article-title":"The human LL-37 peptide exerts antimicrobial activity against Legionella micdadei interacting with membrane phospholipids","volume":"1867","author":"Jurak","year":"2022","journal-title":"Biochim. Biophys. Acta Mol. Cell Biol. Lipids"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Ducret, A., Chabalier, M., and Dukan, S. (2014). Characterization and resuscitation of \u2018non-culturable\u2019 cells of Legionella pneumophila. BMC Microbiol., 14.","DOI":"10.1186\/1471-2180-14-3"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"914540","DOI":"10.1155\/2013\/914540","article-title":"Penetration of milk-derived antimicrobial peptides into phospholipid monolayers as model biomembranes","volume":"2013","author":"Barzyk","year":"2013","journal-title":"Biochem. Res. Int."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1042\/bj3410501","article-title":"Structure and organization of the human antimicrobial peptide LL-37 in phospholipid membranes: Relevance to the molecular basis for its non-cell-selective activity","volume":"341","author":"Oren","year":"1999","journal-title":"Biochem. J."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"944147","DOI":"10.3389\/fphar.2022.944147","article-title":"Renovation as innovation: Repurposing human antibacterial peptide LL-37 for cancer therapy","volume":"13","author":"Lu","year":"2022","journal-title":"Front. Pharmacol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"8459","DOI":"10.1021\/bi036284s","article-title":"Perturbation of the hydrophobic core of lipid bilayers by the human antimicrobial peptide LL-37","volume":"43","author":"Martinez","year":"2004","journal-title":"Biochemistry"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1214","DOI":"10.1021\/acsinfecdis.9b00066","article-title":"Salmonella membrane structural remodeling increases resistance to antimicrobial peptide LL-37","volume":"5","author":"Martynowicz","year":"2019","journal-title":"ACS Infect. Dis."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2586","DOI":"10.1016\/j.bbamem.2007.06.015","article-title":"How lipids influence the mode of action of membrane-active peptides","volume":"1768","author":"Sevcsik","year":"2007","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1340","DOI":"10.1021\/acs.bioconjchem.7b00114","article-title":"Synthetic random copolymers as a molecular platform to mimic host-defense antimicrobial peptides","volume":"28","author":"Takahashi","year":"2017","journal-title":"Bioconjug. Chem."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Pastuszak, K., Kowalczyk, B., Tarasiuk, J., Jurak, M., and Palusi\u0144ska-Szysz, M. (2023). Influence of the antimicrobial LL-37 peptide on Legionella dumoffii phospholipids adsorbed at the air\u2013liquid interface. Sustainability, 15.","DOI":"10.3390\/su15086670"},{"key":"ref_40","first-page":"911","article-title":"A rapid method of total lipid extraction and purification. Can","volume":"37","author":"Bligh","year":"1959","journal-title":"J. Biochem. Physiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"954","DOI":"10.1016\/j.bbrc.2004.08.180","article-title":"Legioliulin, a new isocoumarin compound responsible for blue-white autofluorescence in Legionella (Fluoribacter) dumoffi under long-wavelength UV light","volume":"323","author":"Hayakawa","year":"2004","journal-title":"Biochem. Biophys. Res. Commun."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/15\/12039\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:20:42Z","timestamp":1760127642000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/15\/12039"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,7,27]]},"references-count":41,"journal-issue":{"issue":"15","published-online":{"date-parts":[[2023,8]]}},"alternative-id":["ijms241512039"],"URL":"https:\/\/doi.org\/10.3390\/ijms241512039","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,7,27]]}}}