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In situ captured antibacterial action of membrane-incising peptide lamellae

Author

Listed:
  • Kamal el Battioui

    (HUN-REN Research Centre for Natural Sciences
    Eötvös Loránd University)

  • Sohini Chakraborty

    (HUN-REN Research Centre for Natural Sciences)

  • András Wacha

    (HUN-REN Research Centre for Natural Sciences)

  • Dániel Molnár

    (HUN-REN Research Centre for Natural Sciences
    Eötvös Loránd University)

  • Mayra Quemé-Peña

    (HUN-REN Research Centre for Natural Sciences
    Eötvös Loránd University)

  • Imola Cs. Szigyártó

    (HUN-REN Research Centre for Natural Sciences)

  • Csenge Lilla Szabó

    (Eötvös Loránd University
    Analytical and BioNMR Laboratory)

  • Andrea Bodor

    (Analytical and BioNMR Laboratory)

  • Kata Horváti

    (Research Centre for Natural Sciences)

  • Gergő Gyulai

    (Research Centre for Natural Sciences
    Laboratory of Interfaces and Nanostructures)

  • Szilvia Bősze

    (Eötvös Loránd University)

  • Judith Mihály

    (HUN-REN Research Centre for Natural Sciences)

  • Bálint Jezsó

    (HUN-REN Research Centre for Natural Sciences
    Eötvös Loránd University)

  • Loránd Románszki

    (HUN-REN Research Centre for Natural Sciences)

  • Judit Tóth

    (HUN-REN Research Centre for Natural Sciences
    Budapest University of Technology and Economics)

  • Zoltán Varga

    (HUN-REN Research Centre for Natural Sciences
    Budapest University of Technology and Economics, Műegyetem rkp. 3)

  • István Mándity

    (HUN-REN Research Centre for Natural Sciences
    Semmelweis University)

  • Tünde Juhász

    (HUN-REN Research Centre for Natural Sciences)

  • Tamás Beke-Somfai

    (HUN-REN Research Centre for Natural Sciences)

Abstract

Developing unique mechanisms of action are essential to combat the growing issue of antimicrobial resistance. Supramolecular assemblies combining the improved biostability of non-natural compounds with the complex membrane-attacking mechanisms of natural peptides are promising alternatives to conventional antibiotics. However, for such compounds the direct visual insight on antibacterial action is still lacking. Here we employ a design strategy focusing on an inducible assembly mechanism and utilized electron microscopy (EM) to follow the formation of supramolecular structures of lysine-rich heterochiral β3-peptides, termed lamellin-2K and lamellin-3K, triggered by bacterial cell surface lipopolysaccharides. Combined molecular dynamics simulations, EM and bacterial assays confirmed that the phosphate-induced conformational change on these lamellins led to the formation of striped lamellae capable of incising the cell envelope of Gram-negative bacteria thereby exerting antibacterial activity. Our findings also provide a mechanistic link for membrane-targeting agents depicting the antibiotic mechanism derived from the in-situ formation of active supramolecules.

Suggested Citation

  • Kamal el Battioui & Sohini Chakraborty & András Wacha & Dániel Molnár & Mayra Quemé-Peña & Imola Cs. Szigyártó & Csenge Lilla Szabó & Andrea Bodor & Kata Horváti & Gergő Gyulai & Szilvia Bősze & Judit, 2024. "In situ captured antibacterial action of membrane-incising peptide lamellae," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47708-4
    DOI: 10.1038/s41467-024-47708-4
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    References listed on IDEAS

    as
    1. Eric D. Brown & Gerard D. Wright, 2016. "Antibacterial drug discovery in the resistance era," Nature, Nature, vol. 529(7586), pages 336-343, January.
    2. Emilie A. Porter & Xifang Wang & Hee-Seung Lee & Bernard Weisblum & Samuel H. Gellman, 2000. "Non-haemolytic β-amino-acid oligomers," Nature, Nature, vol. 404(6778), pages 565-565, April.
    3. Zhucheng Chen & Haijuan Yang & Nikola P. Pavletich, 2008. "Mechanism of homologous recombination from the RecA–ssDNA/dsDNA structures," Nature, Nature, vol. 453(7194), pages 489-494, May.
    4. Rhythm Shukla & Francesca Lavore & Sourav Maity & Maik G. N. Derks & Chelsea R. Jones & Bram J. A. Vermeulen & Adéla Melcrová & Michael A. Morris & Lea Marie Becker & Xiaoqi Wang & Raj Kumar & João Me, 2022. "Teixobactin kills bacteria by a two-pronged attack on the cell envelope," Nature, Nature, vol. 608(7922), pages 390-396, August.
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