IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-47708-4.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-47708-4
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-47708-4?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. Eric D. Brown & Gerard D. Wright, 2016. "Antibacterial drug discovery in the resistance era," Nature, Nature, vol. 529(7586), pages 336-343, January.
    4. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Kalinga Pavan T. Silva & Ganesh Sundar & Anupama Khare, 2023. "Efflux pump gene amplifications bypass necessity of multiple target mutations for resistance against dual-targeting antibiotic," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Elsa Hansen & Jason Karslake & Robert J Woods & Andrew F Read & Kevin B Wood, 2020. "Antibiotics can be used to contain drug-resistant bacteria by maintaining sufficiently large sensitive populations," PLOS Biology, Public Library of Science, vol. 18(5), pages 1-20, May.
    3. Takeshi Nakaya & Miyuki Yabe & Ellene H. Mashalidis & Toyotaka Sato & Kazuki Yamamoto & Yuta Hikiji & Akira Katsuyama & Motoko Shinohara & Yusuke Minato & Satoshi Takahashi & Motohiro Horiuchi & Shin-, 2022. "Synthesis of macrocyclic nucleoside antibacterials and their interactions with MraY," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Hajkowicz, Stefan & Naughtin, Claire & Sanderson, Conrad & Schleiger, Emma & Karimi, Sarvnaz & Bratanova, Alexandra & Bednarz, Tomasz, 2022. "Artificial intelligence for science – adoption trends and future development pathways," MPRA Paper 115464, University Library of Munich, Germany.
    5. Alberto Signoroni & Alessandro Ferrari & Stefano Lombardi & Mattia Savardi & Stefania Fontana & Karissa Culbreath, 2023. "Hierarchical AI enables global interpretation of culture plates in the era of digital microbiology," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    6. Chenyuan Wang & Yushan Xia & Runming Wang & Jingru Li & Chun-Lung Chan & Richard Yi-Tsun Kao & Patrick H. Toy & Pak-Leung Ho & Hongyan Li & Hongzhe Sun, 2023. "Metallo-sideromycin as a dual functional complex for combating antimicrobial resistance," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    7. Shih-Chi Luo & Min-Chi Yeh & Yu-Hsiang Lien & Hsin-Yi Yeh & Huei-Lun Siao & I-Ping Tu & Peter Chi & Meng-Chiao Ho, 2023. "A RAD51–ADP double filament structure unveils the mechanism of filament dynamics in homologous recombination," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    8. Asmalia Md-Lasim & Farah Shafawati Mohd-Taib & Mardani Abdul-Halim & Ahmad Mohiddin Mohd-Ngesom & Sheila Nathan & Shukor Md-Nor, 2021. "Leptospirosis and Coinfection: Should We Be Concerned?," IJERPH, MDPI, vol. 18(17), pages 1-17, September.
    9. Wei Li Thong & Yingxin Zhang & Ying Zhuo & Katherine J. Robins & Joanna K. Fyans & Abigail J. Herbert & Brian J. C. Law & Jason Micklefield, 2021. "Gene editing enables rapid engineering of complex antibiotic assembly lines," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    10. Zhiwen Liu & Kangli Guo & Liemei Yan & Kai Zhang & Ying Wang & Xiaokang Ding & Nana Zhao & Fu-Jian Xu, 2023. "Janus nanoparticles targeting extracellular polymeric substance achieve flexible elimination of drug-resistant biofilms," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    11. Jin Feng & Youle Zheng & Wanqing Ma & Defeng Weng & Dapeng Peng & Yindi Xu & Zhifang Wang & Xu Wang, 2024. "A synthetic antibiotic class with a deeply-optimized design for overcoming bacterial resistance," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    12. Kade D. Roberts & Yan Zhu & Mohammad A. K. Azad & Mei-Ling Han & Jiping Wang & Lynn Wang & Heidi H. Yu & Andrew S. Horne & Jo-Anne Pinson & David Rudd & Nicolas H. Voelcker & Nitin A. Patil & Jinxin Z, 2022. "A synthetic lipopeptide targeting top-priority multidrug-resistant Gram-negative pathogens," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    13. Qian Zhang & Bin Song & Yanan Xu & Yunmin Yang & Jian Ji & Wenjun Cao & Jianping Lu & Jiali Ding & Haiting Cao & Binbin Chu & Jiaxu Hong & Houyu Wang & Yao He, 2023. "In vivo bioluminescence imaging of natural bacteria within deep tissues via ATP-binding cassette sugar transporter," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    14. Adéla Melcrová & Sourav Maity & Josef Melcr & Niels A. W. Kok & Mariella Gabler & Jonne Eyden & Wenche Stensen & John S. M. Svendsen & Arnold J. M. Driessen & Siewert J. Marrink & Wouter H. Roos, 2023. "Lateral membrane organization as target of an antimicrobial peptidomimetic compound," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    15. Sijia Guo & Shu Wang & Suze Ma & Zixin Deng & Wei Ding & Qi Zhang, 2022. "Radical SAM-dependent ether crosslink in daropeptide biosynthesis," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    16. Hesam Aldin Varpaei & Mohammad Yavari & Mohammad Mahdi Miremami & Amir Mahdi Farahani & Faeze Esmaeili & Saba Abachi & Pariya Onsori & Pedram Nouroozi & Hossein Esmaeili & Ali Kazemi, 2020. "Epidemiological Study of Antibiotic Self-Medication in Tehran 1399, A Descriptive Study," Biomedical Journal of Scientific & Technical Research, Biomedical Research Network+, LLC, vol. 31(1), pages 23870-23875, October.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47708-4. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.