IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-50799-8.html
   My bibliography  Save this article

Adaptative survival of Aspergillus fumigatus to echinocandins arises from cell wall remodeling beyond β−1,3-glucan synthesis inhibition

Author

Listed:
  • Malitha C. Dickwella Widanage

    (Michigan State University
    National High Magnetic Field Laboratory)

  • Isha Gautam

    (Michigan State University)

  • Daipayan Sarkar

    (MSU-DOE Plant Research Laboratory)

  • Frederic Mentink-Vigier

    (National High Magnetic Field Laboratory)

  • Josh V. Vermaas

    (MSU-DOE Plant Research Laboratory
    Michigan State University)

  • Shi-You Ding

    (Michigan State University)

  • Andrew S. Lipton

    (Pacific Northwest National Laboratory)

  • Thierry Fontaine
  • Jean-Paul Latgé

    (University of Crete)

  • Ping Wang

    (Louisiana State University Health Sciences Center)

  • Tuo Wang

    (Michigan State University)

Abstract

Antifungal echinocandins inhibit the biosynthesis of β−1,3-glucan, a major and essential polysaccharide component of the fungal cell wall. However, the efficacy of echinocandins against the pathogen Aspergillus fumigatus is limited. Here, we use solid-state nuclear magnetic resonance (ssNMR) and other techniques to show that echinocandins induce dynamic changes in the assembly of mobile and rigid polymers within the A. fumigatus cell wall. The reduction of β−1,3-glucan induced by echinocandins is accompanied by a concurrent increase in levels of chitin, chitosan, and highly polymorphic α−1,3-glucans, whose physical association with chitin maintains cell wall integrity and modulates water permeability. The rearrangement of the macromolecular network is dynamic and controls the permeability and circulation of the drug throughout the cell wall. Thus, our results indicate that echinocandin treatment triggers compensatory rearrangements in the cell wall that may help A. fumigatus to tolerate the drugs’ antifungal effects.

Suggested Citation

  • Malitha C. Dickwella Widanage & Isha Gautam & Daipayan Sarkar & Frederic Mentink-Vigier & Josh V. Vermaas & Shi-You Ding & Andrew S. Lipton & Thierry Fontaine & Jean-Paul Latgé & Ping Wang & Tuo Wang, 2024. "Adaptative survival of Aspergillus fumigatus to echinocandins arises from cell wall remodeling beyond β−1,3-glucan synthesis inhibition," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50799-8
    DOI: 10.1038/s41467-024-50799-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-50799-8
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-50799-8?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. Alex Kirui & Wancheng Zhao & Fabien Deligey & Hui Yang & Xue Kang & Frederic Mentink-Vigier & Tuo Wang, 2022. "Carbohydrate-aromatic interface and molecular architecture of lignocellulose," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    2. Arnab Chakraborty & Liyanage D. Fernando & Wenxia Fang & Malitha C. Dickwella Widanage & Pingzhen Wei & Cheng Jin & Thierry Fontaine & Jean-Paul Latgé & Tuo Wang, 2021. "A molecular vision of fungal cell wall organization by functional genomics and solid-state NMR," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    3. Liyanage D. Fernando & Yordanis Pérez-Llano & Malitha C. Dickwella Widanage & Anand Jacob & Liliana Martínez-Ávila & Andrew S. Lipton & Nina Gunde-Cimerman & Jean-Paul Latgé & Ramón Alberto Batista-Ga, 2023. "Structural adaptation of fungal cell wall in hypersaline environment," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Xue Kang & Alex Kirui & Artur Muszyński & Malitha C. Dickwella Widanage & Adrian Chen & Parastoo Azadi & Ping Wang & Frederic Mentink-Vigier & Tuo Wang, 2018. "Molecular architecture of fungal cell walls revealed by solid-state NMR," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    5. Thomas J. Simmons & Jenny C. Mortimer & Oigres D. Bernardinelli & Ann-Christin Pöppler & Steven P. Brown & Eduardo R. deAzevedo & Ray Dupree & Paul Dupree, 2016. "Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR," Nature Communications, Nature, vol. 7(1), pages 1-9, December.
    6. Charles R. Harris & K. Jarrod Millman & Stéfan J. Walt & Ralf Gommers & Pauli Virtanen & David Cournapeau & Eric Wieser & Julian Taylor & Sebastian Berg & Nathaniel J. Smith & Robert Kern & Matti Picu, 2020. "Array programming with NumPy," Nature, Nature, vol. 585(7825), pages 357-362, September.
    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. Liyanage D. Fernando & Yordanis Pérez-Llano & Malitha C. Dickwella Widanage & Anand Jacob & Liliana Martínez-Ávila & Andrew S. Lipton & Nina Gunde-Cimerman & Jean-Paul Latgé & Ramón Alberto Batista-Ga, 2023. "Structural adaptation of fungal cell wall in hypersaline environment," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Tan Wang & L. Jeff Hong, 2023. "Large-Scale Inventory Optimization: A Recurrent Neural Networks–Inspired Simulation Approach," INFORMS Journal on Computing, INFORMS, vol. 35(1), pages 196-215, January.
    3. Léon Faure & Bastien Mollet & Wolfram Liebermeister & Jean-Loup Faulon, 2023. "A neural-mechanistic hybrid approach improving the predictive power of genome-scale metabolic models," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Claudia Quinteros-Cartaya & Guillermo Solorio-Magaña & Francisco Javier Núñez-Cornú & Felipe de Jesús Escalona-Alcázar & Diana Núñez, 2023. "Microearthquakes in the Guadalajara Metropolitan Zone, Mexico: evidence from buried active faults in Tesistán Valley, Zapopan," Natural Hazards: Journal of the International Society for the Prevention and Mitigation of Natural Hazards, Springer;International Society for the Prevention and Mitigation of Natural Hazards, vol. 116(3), pages 2797-2818, April.
    5. Furqan Dar & Samuel R. Cohen & Diana M. Mitrea & Aaron H. Phillips & Gergely Nagy & Wellington C. Leite & Christopher B. Stanley & Jeong-Mo Choi & Richard W. Kriwacki & Rohit V. Pappu, 2024. "Biomolecular condensates form spatially inhomogeneous network fluids," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Nina Tiel & Fabian Fopp & Philipp Brun & Johan Hoogen & Dirk Nikolaus Karger & Cecilia M. Casadei & Lisha Lyu & Devis Tuia & Niklaus E. Zimmermann & Thomas W. Crowther & Loïc Pellissier, 2024. "Regional uniqueness of tree species composition and response to forest loss and climate change," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    7. López Pérez, Mario & Mansilla Corona, Ricardo, 2022. "Ordinal synchronization and typical states in high-frequency digital markets," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 598(C).
    8. Jessica M. Vanslambrouck & Sean B. Wilson & Ker Sin Tan & Ella Groenewegen & Rajeev Rudraraju & Jessica Neil & Kynan T. Lawlor & Sophia Mah & Michelle Scurr & Sara E. Howden & Kanta Subbarao & Melissa, 2022. "Enhanced metanephric specification to functional proximal tubule enables toxicity screening and infectious disease modelling in kidney organoids," Nature Communications, Nature, vol. 13(1), pages 1-23, December.
    9. Kiran Krishnamachari & Dylan Lu & Alexander Swift-Scott & Anuar Yeraliyev & Kayla Lee & Weitai Huang & Sim Ngak Leng & Anders Jacobsen Skanderup, 2022. "Accurate somatic variant detection using weakly supervised deep learning," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    10. Larissa Samaan & Leonie Klock & Sandra Weber & Mirjam Reidick & Leonie Ascone & Simone Kühn, 2024. "Low-Level Visual Features of Window Views Contribute to Perceived Naturalness and Mental Health Outcomes," IJERPH, MDPI, vol. 21(5), pages 1-35, May.
    11. Dennis Bontempi & Leonard Nuernberg & Suraj Pai & Deepa Krishnaswamy & Vamsi Thiriveedhi & Ahmed Hosny & Raymond H. Mak & Keyvan Farahani & Ron Kikinis & Andrey Fedorov & Hugo J. W. L. Aerts, 2024. "End-to-end reproducible AI pipelines in radiology using the cloud," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    12. Lauren L. Porter & Allen K. Kim & Swechha Rimal & Loren L. Looger & Ananya Majumdar & Brett D. Mensh & Mary R. Starich & Marie-Paule Strub, 2022. "Many dissimilar NusG protein domains switch between α-helix and β-sheet folds," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    13. Qaseem, Mirza Faisal & Shaheen, Humaira & Wu, Ai-Min, 2021. "Cell wall hemicellulose for sustainable industrial utilization," Renewable and Sustainable Energy Reviews, Elsevier, vol. 144(C).
    14. Oren Amsalem & Hidehiko Inagaki & Jianing Yu & Karel Svoboda & Ran Darshan, 2024. "Sub-threshold neuronal activity and the dynamical regime of cerebral cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    15. Matthew Rosenblatt & Link Tejavibulya & Rongtao Jiang & Stephanie Noble & Dustin Scheinost, 2024. "Data leakage inflates prediction performance in connectome-based machine learning models," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    16. Jackie Grant & Mark Hindmarsh & Sergey E. Koposov, 2022. "The distribution of loss to future USS pensions due to the UUK cuts of April 2022," Papers 2206.06201, arXiv.org.
    17. Sayedali Shetab Boushehri & Katharina Essig & Nikolaos-Kosmas Chlis & Sylvia Herter & Marina Bacac & Fabian J. Theis & Elke Glasmacher & Carsten Marr & Fabian Schmich, 2023. "Explainable machine learning for profiling the immunological synapse and functional characterization of therapeutic antibodies," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    18. Henry Webel & Lili Niu & Annelaura Bach Nielsen & Marie Locard-Paulet & Matthias Mann & Lars Juhl Jensen & Simon Rasmussen, 2024. "Imputation of label-free quantitative mass spectrometry-based proteomics data using self-supervised deep learning," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    19. Shukla, Mohak & Thakur, Ajay D., 2022. "An Enquiry on similarities between Renormalization Group and Auto-Encoders using Transfer Learning," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 608(P1).
    20. Borofsky, Talia & Feldman, Marcus W. & Ram, Yoav, 2024. "Cultural transmission, competition for prey, and the evolution of cooperative hunting," Theoretical Population Biology, Elsevier, vol. 156(C), pages 12-21.

    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_s41467-024-50799-8. 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.