{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,24]],"date-time":"2026-10-24T00:13:02Z","timestamp":1792800782108,"version":"4.5.0"},"reference-count":54,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2026,1,27]],"date-time":"2026-01-27T00:00:00Z","timestamp":1769472000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:sec>\n                    <jats:title>Introduction<\/jats:title>\n                    <jats:p>\n                      Antimicrobial peptides (AMPs), key components of innate immunity, offer broad-spectrum activity against diverse pathogens. In\n                      <jats:italic>Medicago truncatula<\/jats:italic>\n                      , over 700 nodule-specific cysteine-rich (NCR) peptides with highly diverse sequences and physicochemical properties are produced in the symbiotic cells of root nodules, where cationic members block bacterial cell division and display potent antimicrobial activity\n                      <jats:italic>in vitro<\/jats:italic>\n                      . In contrast, anionic NCRs typically lack antimicrobial effects, and NCR147\u2014a neutral peptide\u2014is the only known non-cationic NCR that shows weak bactericidal activity. This unique property prompted us to identify the antimicrobial region of NCR147 and enhance its activity through targeted sequence modifications.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Materials and methods<\/jats:title>\n                    <jats:p>In this study, 13 truncated and substituted derivatives of NCR147 were chemically synthesized to identify peptide regions responsible for antimicrobial activity. Antimicrobial efficacy was evaluated against 18 pathogens by determining minimum bactericidal and minimum fungicidal concentrations. Inhibition and eradication of bacterial biofilms were assessed to determine peptide effects. Cytotoxicity was measured using hemolysis assays and multiple viability assays in human cell cultures. Peptide interactions with membrane lipids, effects on membrane permeability, and modulation of bacterial efflux pumps were analyzed using established biochemical and biophysical assays. Bacterial proteins interacting with selected peptides were identified by affinity chromatography followed by LC\u2013MS\/MS.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      The NCR147 derivatives displayed varying degrees of antimicrobial potency and spectrum. Analysis of the physicochemical properties and predicted 3D structures of 13 NCR peptide variants revealed that the antimicrobial region resides in the C-terminal portion of these intrinsically disordered peptides, where the WAW hydrophobic patch together with the positively charged amino acids contribute to antimicrobial activity, most likely through interactions with microbial membranes. The most active peptides provoked alteration of bacterial membranes, inhibited efflux pumps, and interfered with essential intracellular targets. Moreover, these peptides exhibited potent antibiofilm effects, including the ability to both prevent and degrade\n                      <jats:italic>Acinetobacter baumannii<\/jats:italic>\n                      biofilms. Incorporation of 5-fluoro-L-tryptophan enhanced both antimicrobial breadth and antifungal activity. Importantly, this fluorinated peptide was non-cytotoxic to human cells.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Discussion<\/jats:title>\n                    <jats:p>These findings reveal that NCR147-derived peptides function via a multihit mechanism and highlight the therapeutic promise of plant-derived AMPs as next-generation antimicrobials with reduced risk of resistance development.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.3389\/fmicb.2025.1720738","type":"journal-article","created":{"date-parts":[[2026,1,27]],"date-time":"2026-01-27T06:40:49Z","timestamp":1769496049000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":1,"title":["Multifaceted antimicrobial mechanisms of NCR147-derived peptides from Medicago truncatula"],"prefix":"10.3389","volume":"16","author":[{"given":"Hilda","family":"Tiricz","sequence":"first","affiliation":[{"name":"Institute of Plant Biology, HUN-REN Biological Research Centre","place":["Szeged, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rui M.","family":"Lima","sequence":"additional","affiliation":[{"name":"Institute of Plant Biology, HUN-REN Biological Research Centre","place":["Szeged, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ilona","family":"Pfeiffer","sequence":"additional","affiliation":[{"name":"Department of Biotechnology and Microbiology, Faculty of Science and Informatics, University of Szeged","place":["Szeged, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"N\u00f3ra","family":"Igaz","sequence":"additional","affiliation":[{"name":"Department of Biochemistry and Molecular Biology, University of Szeged","place":["Szeged, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ildik\u00f3","family":"Domonkos","sequence":"additional","affiliation":[{"name":"Institute of Plant Biology, HUN-REN Biological Research Centre","place":["Szeged, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S\u00e1ndor","family":"Jenei","sequence":"additional","affiliation":[{"name":"Institute of Plant Biology, HUN-REN Biological Research Centre","place":["Szeged, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dian H. O.","family":"Howan","sequence":"additional","affiliation":[{"name":"Department of Medical Chemistry, Albert Szent-Gy\u00f6rgyi Medical School, University of Szeged","place":["Szeged, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexandra","family":"P\u00e1l","sequence":"additional","affiliation":[{"name":"Institute of Plant Biology, HUN-REN Biological Research Centre","place":["Szeged, Hungary"]},{"name":"Doctoral School of Biology, University of Szeged","place":["Szeged, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Edit","family":"T\u00edm\u00e1r","sequence":"additional","affiliation":[{"name":"Institute of Plant Biology, HUN-REN Biological Research Centre","place":["Szeged, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"\u00c9va","family":"Hunyadi-Guly\u00e1s","sequence":"additional","affiliation":[{"name":"Proteomics Research Group, Core Facility, HUN-REN Biological Research Centre","place":["Szeged, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"G\u00e1bor K.","family":"T\u00f3th","sequence":"additional","affiliation":[{"name":"Department of Medical Chemistry, Albert Szent-Gy\u00f6rgyi Medical School, University of Szeged","place":["Szeged, Hungary"]},{"name":"MTA-SZTE Biomimetic Systems Research Group, University of Szeged","place":["Szeged, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zolt\u00e1n","family":"Bozs\u00f3","sequence":"additional","affiliation":[{"name":"Plant Protection Institute, HUN-REN Centre for Agricultural Research","place":["Budapest, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"\u00c9va","family":"Kondorosi","sequence":"additional","affiliation":[{"name":"Institute of Plant Biology, HUN-REN Biological Research Centre","place":["Szeged, Hungary"]},{"name":"Centre for Translational Medicine, Semmelweis University","place":["Budapest, Hungary"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2026,1,27]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"13779","DOI":"10.1038\/s41598-021-93115-w","article-title":"Interlaboratory study for the evaluation of three microtiter plate-based biofilm quantification methods","volume":"11","author":"Allkja","year":"2021","journal-title":"Sci. Rep."},{"key":"ref2","doi-asserted-by":"publisher","first-page":"1012","DOI":"10.1016\/j.bbamem.2015.12.023","article-title":"Recombinant expression, antimicrobial activity and mechanism of action of tritrpticin analogs containing fluoro-tryptophan residues","volume":"1858","author":"Arias","year":"2016","journal-title":"Biochim. Biophys. Acta"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1556\/AMicr.61.2014.2.12","article-title":"Anti-chlamydial effect of plant peptides","volume":"61","author":"Balogh","year":"2014","journal-title":"Acta Microbiol. Immunol. Hung."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"1280","DOI":"10.1089\/ars.2020.8039","article-title":"Bacterial oxidases of the cytochrome bd family: redox enzymes of unique structure, function, and utility as drug targets","volume":"34","author":"Borisov","year":"2021","journal-title":"Antioxid. Redox Signal."},{"key":"ref5","doi-asserted-by":"publisher","first-page":"453","DOI":"10.1002\/pro.2030","article-title":"Fluorine: A new element in protein design","volume":"21","author":"Buer","year":"2012","journal-title":"Protein Sci."},{"key":"ref6","doi-asserted-by":"publisher","first-page":"1007","DOI":"10.1016\/j.peptides.2009.01.018","article-title":"Plant defensins\u2014prospects for the biological functions and biotechnological properties","volume":"30","author":"Carvalho","year":"2009","journal-title":"Peptides"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"7967","DOI":"10.1073\/pnas.1721536115","article-title":"Specific cardiolipin-SecY interactions are required for proton-motive force stimulation of protein secretion","volume":"115","author":"Corey","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref8","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1128\/aem.51.2.323-327.1986","article-title":"Generation and characterization of Tn5 insertion mutations in Pseudomonas syringae pv. tomato","volume":"51","author":"Cuppels","year":"1986","journal-title":"Appl. Environ. Microbiol."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"4777","DOI":"10.1093\/nar\/13.13.4777","article-title":"Efficient octopine Ti plasmid-derived vectors for Agrobacterium-mediated gene transfer to plants","volume":"13","author":"Deblaere","year":"1985","journal-title":"Nucleic Acids Res."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"625","DOI":"10.1016\/j.str.2020.03.013","article-title":"Interactions of a bacterial RND transporter with a transmembrane small protein in a lipid environment","volume":"28","author":"Du","year":"2020","journal-title":"Structure"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1111\/j.1365-313X.2007.03303.x","article-title":"High-throughput quantitative luminescence assay of the growth in planta of Pseudomonas syringae chromosomally tagged with Photorhabdus luminescens luxCDABE","volume":"53","author":"Fan","year":"2008","journal-title":"Plant J."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"51","DOI":"10.3389\/fmicb.2017.00051","article-title":"Comparative analysis of the bacterial membrane disruption effect of two natural plant antimicrobial peptides","volume":"8","author":"Farkas","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"1146","DOI":"10.3389\/fmicb.2020.01146","article-title":"The critical role of tryptophan in the antimicrobial activity and cell toxicity of the duck antimicrobial peptide DCATH","volume":"11","author":"Feng","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"D377","DOI":"10.1093\/nar\/gkac933","article-title":"CAMPR4: a database of natural and synthetic antimicrobial peptides","volume":"51","author":"Gawde","year":"2023","journal-title":"Nucleic Acids Res."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"10044","DOI":"10.1073\/pnas.0914680107","article-title":"The action of cardiolipin on the bacterial translocon","volume":"107","author":"Gold","year":"2010","journal-title":"Proc. Natl. Acad. Sci."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"370","DOI":"10.1002\/cbic.200700643","article-title":"Using fluorous amino acids to modulate the biological activity of an antimicrobial peptide","volume":"9","author":"Gottler","year":"2008","journal-title":"Chembiochem"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"418","DOI":"10.1016\/S0140-6736(97)80051-7","article-title":"Peptide antibiotics","volume":"349","author":"Hancock","year":"1997","journal-title":"Lancet"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"1551","DOI":"10.1038\/nbt1267","article-title":"Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies","volume":"24","author":"Hancock","year":"2006","journal-title":"Nat. Biotechnol."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"128","DOI":"10.22503\/inftars.XXII.2022.2.8","article-title":"The past, present and future of the ELKH cloud","volume":"22","author":"H\u00e9der","year":"2022","journal-title":"Inform. T\u00e1rsadalom"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"2694","DOI":"10.3390\/ijms24032694","article-title":"Enhanced antibacterial activity of substituted derivatives of NCR169C peptide","volume":"24","author":"Howan","year":"2023","journal-title":"Int. J. Mol. Sci."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"29","DOI":"10.3390\/medicines6010029","article-title":"Medicinal potentialities of plant defensins: a review with applied perspectives","volume":"6","author":"Ishaq","year":"2019","journal-title":"Medicine"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"9923","DOI":"10.1038\/s41598-021-89485-w","article-title":"Structure and antimicrobial activity of NCR169, a nodule-specific cysteine-rich peptide of Medicago truncatula","volume":"11","author":"Isozumi","year":"2021","journal-title":"Sci. Rep."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"270","DOI":"10.3389\/fmicb.2020.00270","article-title":"Potent chimeric antimicrobial derivatives of the Medicago truncatula NCR247 symbiotic peptide","volume":"11","author":"Jenei","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"e10","DOI":"10.1017\/S0033583522000105","article-title":"Tryptophan, more than just an interfacial amino acid in the membrane activity of cationic cell-penetrating and antimicrobial peptides","volume":"55","author":"Khemaissa","year":"2022","journal-title":"Q. Rev. Biophys."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"611","DOI":"10.1146\/annurev-micro-092412-155630","article-title":"A paradigm for endosymbiotic life: cell differentiation of Rhizobium bacteria provoked by host plant factors","volume":"67","author":"Kondorosi","year":"2013","journal-title":"Ann. Rev. Microbiol."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"307","DOI":"10.3389\/fmicb.2020.01307","article-title":"Unexplored arsenals of legume peptides with potential for their applications in medicine and agriculture","volume":"11","author":"Lima","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"460","DOI":"10.3389\/fmolb.2022.870460","article-title":"Legume plant peptides as sources of novel antimicrobial molecules against human pathogens","volume":"9","author":"Lima","year":"2022","journal-title":"Front. Mol. Biosci."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"1143","DOI":"10.1039\/b909864j","article-title":"Fluorine--a new element in the design of membrane-active peptides","volume":"5","author":"Marsh","year":"2009","journal-title":"Mol. BioSyst."},{"key":"ref29","doi-asserted-by":"crossref","DOI":"10.5772\/55616","article-title":"Pseudomonas aeruginosa: multi-drug-resistance development and treatment options","volume-title":"Infection control","author":"Meletis","year":"2013"},{"key":"ref30","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1104\/pp.102.018192","article-title":"A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs","volume":"132","author":"Mergaert","year":"2003","journal-title":"Plant Physiol."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"5230","DOI":"10.1073\/pnas.0600912103","article-title":"Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium\u2013legume symbiosis","volume":"103","author":"Mergaert","year":"2006","journal-title":"Proc. Natl. Acad. Sci."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1186\/s12941-016-0159-8","article-title":"Antimicrobial nodule-specific cysteine-rich peptides disturb the integrity of bacterial outer and inner membranes and cause loss of membrane potential","volume":"15","author":"Mikul\u00e1ss","year":"2016","journal-title":"Ann. Clin. Microbiol. Antimicrob."},{"key":"ref33","doi-asserted-by":"publisher","first-page":"519","DOI":"10.1093\/jb\/mvr036","article-title":"Regulatory role of cardiolipin in the activity of an ATP-dependent protease, Lon, from Escherichia coli","volume":"149","author":"Minami","year":"2011","journal-title":"J. Biochem. (Tokyo)"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"5041","DOI":"10.1073\/pnas.1704217114","article-title":"Morphotype of bacteroids in different legumes correlates with the number and type of symbiotic NCR peptides","volume":"114","author":"Montiel","year":"2017","journal-title":"Proc. Natl. Acad. Sci."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1038\/s41573-019-0058-8","article-title":"Antimicrobial host defence peptides: functions and clinical potential","volume":"19","author":"Mookherjee","year":"2020","journal-title":"Nat. Rev. Drug Discov."},{"key":"ref36","doi-asserted-by":"publisher","first-page":"135","DOI":"10.4149\/gpb_2015002","article-title":"Interaction of cysteine-rich cationic antimicrobial peptides with intact bacteria and model membranes","volume":"34","author":"Nagy","year":"2015","journal-title":"Gen. Physiol. Biophys."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"2437","DOI":"10.3791\/2437","article-title":"Microtiter dish biofilm formation assay","volume":"47","author":"O\u2019Toole","year":"2011","journal-title":"J. Vis. Exp."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1155\/2014\/320796","article-title":"Symbiotic plant peptides eliminate Candida albicans both in vitro and in an epithelial infection model and inhibit the proliferation of immortalized human cells","volume":"2014","author":"\u00d6rd\u00f6gh","year":"2014","journal-title":"Biomed. Res. Int."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1016\/j.semcdb.2018.02.004","article-title":"The evolution, function and mechanisms of action for plant defensins","volume":"88","author":"Parisi","year":"2019","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"D543","DOI":"10.1093\/nar\/gkae1011","article-title":"The PRIDE database at 20 years: 2025 update","volume":"53","author":"Perez-Riverol","year":"2024","journal-title":"Nucleic Acids Res."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"2848","DOI":"10.1002\/1873-3468.12794","article-title":"Tat transport in Escherichia coli requires zwitterionic phosphatidylethanolamine but no specific negatively charged phospholipid","volume":"591","author":"Rathmann","year":"2017","journal-title":"FEBS Lett."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"1005","DOI":"10.1016\/j.freeradbiomed.2009.07.007","article-title":"Analysis of the mechanism by which tryptophan analogs inhibit human myeloperoxidase","volume":"47","author":"Sliskovic","year":"2009","journal-title":"Free Radic. Biol. Med."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"3733","DOI":"10.1128\/JB.00567-12","article-title":"Draft genome sequence of Pseudomonas syringae pathovar syringae strain FF5, causal agent of stem tip dieback disease on ornamental pear","volume":"194","author":"Sohn","year":"2012","journal-title":"J. Bacteriol."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"3666","DOI":"10.3390\/ijms22073666","article-title":"Symbiotic NCR peptide fragments affect the viability, morphology and biofilm formation of Candida species","volume":"22","author":"Szerencs\u00e9s","year":"2021","journal-title":"Int. J. Mol. Sci."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"100407","DOI":"10.1016\/j.crmicr.2025.100407","article-title":"Plant-derived nodule-specific cysteine-rich peptides as potent antifungal agents against Cryptococcus neoformans: mechanisms of action, chimeric peptide enhancement, and immunomodulatory effects","volume":"9","author":"Szerencs\u00e9s","year":"2025","journal-title":"Curr. Res. Microb. Sci."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"174151","DOI":"10.1016\/j.ejphar.2021.174151","article-title":"A comprehensive review on pharmacology of efflux pumps and their inhibitors in antibiotic resistance","volume":"903","author":"Thakur","year":"2021","journal-title":"Eur. J. Pharmacol."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"6737","DOI":"10.1128\/AEM.01791-13","article-title":"Antimicrobial nodule-specific cysteine-rich peptides induce membrane depolarization-associated changes in the transcriptome of Sinorhizobium meliloti","volume":"79","author":"Tiricz","year":"2013","journal-title":"Appl. Environ. Microbiol."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"1122","DOI":"10.1126\/science.1184057","article-title":"Plant peptides govern terminal differentiation of bacteria in symbiosis","volume":"327","author":"Van De Vel","year":"2010","journal-title":"Science"},{"key":"ref49","doi-asserted-by":"publisher","first-page":"16043","DOI":"10.1073\/pnas.2003526117","article-title":"Antifungal symbiotic peptide NCR044 exhibits unique structure and multifaceted mechanisms of action that confer plant protection","volume":"117","author":"Velivelli","year":"2020","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref50","doi-asserted-by":"publisher","first-page":"1221","DOI":"10.3390\/biomedicines11041221","article-title":"Mechanisms of antibiotic and biocide resistance that contribute to Pseudomonas aeruginosa persistence in the hospital environment","volume":"11","author":"Verdial","year":"2023","journal-title":"Biomedicine"},{"key":"ref51","doi-asserted-by":"publisher","first-page":"31","DOI":"10.2174\/0115680266266646231023091215","article-title":"Protein dynamics mediated by cardiolipin in bacteria","volume":"24","author":"Wang","year":"2024","journal-title":"Curr. Top. Med. Chem."},{"key":"ref52","volume-title":"WHO bacterial priority pathogens list 2024: Bacterial pathogens of public health importance, to guide research, development, and strategies to prevent and control antimicrobial resistance","year":"2024"},{"key":"ref53","doi-asserted-by":"publisher","first-page":"795","DOI":"10.1007\/s00294-018-0811-2","article-title":"Perspective: challenges and opportunities for the study of cardiolipin, a key player in bacterial cell structure and function","volume":"64","author":"Wood","year":"2018","journal-title":"Curr. Genet."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"e0004623","DOI":"10.1128\/iai.00046-23","article-title":"Regulation of bacterial two-component systems by cardiolipin","volume":"91","author":"Yeo","year":"2023","journal-title":"Infect. Immun."}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2025.1720738\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,1,27]],"date-time":"2026-01-27T06:40:51Z","timestamp":1769496051000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2025.1720738\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,1,27]]},"references-count":54,"alternative-id":["10.3389\/fmicb.2025.1720738"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2025.1720738","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,1,27]]},"article-number":"1720738"}}