Trans-kingdom conservation of mechanism between bacterial actifensin and eukaryotic defensins

Abstract Antimicrobial peptides are defense molecules found across all domains of life holding promise for developing therapies against drug-resistant pathogens. Actifensin, from Actinomyces ruminicola DPC7226, exhibits potent activity against gram-positive bacteria and shares structural similaritie...

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Main Authors: Ivan Sugrue, Carolin Ade, Paula M. O’Connor, Jan-Martin Daniel, Paolo Innocenti, Nico Kirsch, Nathaniel I. Martin, Günther Weindl, Colin Hill, Tanja Schneider, R. Paul Ross
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:npj Antimicrobials and Resistance
Online Access:https://doi.org/10.1038/s44259-025-00135-x
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author Ivan Sugrue
Carolin Ade
Paula M. O’Connor
Jan-Martin Daniel
Paolo Innocenti
Nico Kirsch
Nathaniel I. Martin
Günther Weindl
Colin Hill
Tanja Schneider
R. Paul Ross
author_facet Ivan Sugrue
Carolin Ade
Paula M. O’Connor
Jan-Martin Daniel
Paolo Innocenti
Nico Kirsch
Nathaniel I. Martin
Günther Weindl
Colin Hill
Tanja Schneider
R. Paul Ross
author_sort Ivan Sugrue
collection DOAJ
description Abstract Antimicrobial peptides are defense molecules found across all domains of life holding promise for developing therapies against drug-resistant pathogens. Actifensin, from Actinomyces ruminicola DPC7226, exhibits potent activity against gram-positive bacteria and shares structural similarities with eukaryotic defensins. This study characterized actifensin’s mechanism of action and therapeutic potential. The findings revealed that actifensin inhibits peptidoglycan synthesis by binding lipid II (Kd = 30 ± 20 nM). Unlike defensins, it also binds lipid I (Kd = 24 ± 27 nM) without significant difference, suggesting the N-acetyl glucosamine moiety of lipid II is not required for complexation. Membrane disruption was not observed with DiSC3(5) fluorescence, or synthetic unilamellar liposomes, indicating indirect cell death via cell wall weakening, visualised by phase contrast microscopy. Actifensin showed no haemolytic activity or toxicity up to 128 µg/ml in human erythrocytes and Hep G2 cells. The peptide was not immunogenic, demonstrating no induction of LDH release in PBMCs or any effect on TLR-mediated signalling. Structural motif analysis identified actifensin as part of a conserved trans-kingdom defensin subfamily, GXGCP, distinct from XTCD peptides in more recently evolved arthropods. These findings emphasise the conserved structure-function relationship of antimicrobials across kingdoms, suggesting a shared evolutionary history of defensins and highlight the therapeutic potential for them or their variants.
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spelling doaj-art-ccf4c1fb674142c0abb73a83c8d9d75b2025-08-20T03:42:10ZengNature Portfolionpj Antimicrobials and Resistance2731-87452025-07-013111210.1038/s44259-025-00135-xTrans-kingdom conservation of mechanism between bacterial actifensin and eukaryotic defensinsIvan Sugrue0Carolin Ade1Paula M. O’Connor2Jan-Martin Daniel3Paolo Innocenti4Nico Kirsch5Nathaniel I. Martin6Günther Weindl7Colin Hill8Tanja Schneider9R. Paul Ross10APC Microbiome Ireland, University College CorkInstitute for Pharmaceutical Microbiology, University of Bonn, University Hospital BonnTeagasc Food Research Centre, MooreparkInstitute for Pharmaceutical Microbiology, University of Bonn, University Hospital BonnBiological Chemistry Group, Institute of Biology, Leiden UniversityDepartment of Pharmacology and Toxicology, Pharmaceutical Institute, University of BonnBiological Chemistry Group, Institute of Biology, Leiden UniversityDepartment of Pharmacology and Toxicology, Pharmaceutical Institute, University of BonnAPC Microbiome Ireland, University College CorkInstitute for Pharmaceutical Microbiology, University of Bonn, University Hospital BonnAPC Microbiome Ireland, University College CorkAbstract Antimicrobial peptides are defense molecules found across all domains of life holding promise for developing therapies against drug-resistant pathogens. Actifensin, from Actinomyces ruminicola DPC7226, exhibits potent activity against gram-positive bacteria and shares structural similarities with eukaryotic defensins. This study characterized actifensin’s mechanism of action and therapeutic potential. The findings revealed that actifensin inhibits peptidoglycan synthesis by binding lipid II (Kd = 30 ± 20 nM). Unlike defensins, it also binds lipid I (Kd = 24 ± 27 nM) without significant difference, suggesting the N-acetyl glucosamine moiety of lipid II is not required for complexation. Membrane disruption was not observed with DiSC3(5) fluorescence, or synthetic unilamellar liposomes, indicating indirect cell death via cell wall weakening, visualised by phase contrast microscopy. Actifensin showed no haemolytic activity or toxicity up to 128 µg/ml in human erythrocytes and Hep G2 cells. The peptide was not immunogenic, demonstrating no induction of LDH release in PBMCs or any effect on TLR-mediated signalling. Structural motif analysis identified actifensin as part of a conserved trans-kingdom defensin subfamily, GXGCP, distinct from XTCD peptides in more recently evolved arthropods. These findings emphasise the conserved structure-function relationship of antimicrobials across kingdoms, suggesting a shared evolutionary history of defensins and highlight the therapeutic potential for them or their variants.https://doi.org/10.1038/s44259-025-00135-x
spellingShingle Ivan Sugrue
Carolin Ade
Paula M. O’Connor
Jan-Martin Daniel
Paolo Innocenti
Nico Kirsch
Nathaniel I. Martin
Günther Weindl
Colin Hill
Tanja Schneider
R. Paul Ross
Trans-kingdom conservation of mechanism between bacterial actifensin and eukaryotic defensins
npj Antimicrobials and Resistance
title Trans-kingdom conservation of mechanism between bacterial actifensin and eukaryotic defensins
title_full Trans-kingdom conservation of mechanism between bacterial actifensin and eukaryotic defensins
title_fullStr Trans-kingdom conservation of mechanism between bacterial actifensin and eukaryotic defensins
title_full_unstemmed Trans-kingdom conservation of mechanism between bacterial actifensin and eukaryotic defensins
title_short Trans-kingdom conservation of mechanism between bacterial actifensin and eukaryotic defensins
title_sort trans kingdom conservation of mechanism between bacterial actifensin and eukaryotic defensins
url https://doi.org/10.1038/s44259-025-00135-x
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