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

Dickwella Widanage, Malitha C.; Gautam, Isha; Sarkar, Daipayan; Mentink-Vigier, Frederic; Vermaas, Josh V.; Ding, Shi-You; Lipton, Andrew S.; Fontaine, Thierry; Latgé, Jean-Paul; Wang, Ping; Wang, Tuo

doi:10.1038/s41467-024-50799-8

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

Journal Article · Wed Jul 31 00:00:00 EDT 2024 · Nature Communications

DOI:https://doi.org/10.1038/s41467-024-50799-8· OSTI ID:2480834

Dickwella Widanage, Malitha C. ^[1]; Gautam, Isha ^[2]; Sarkar, Daipayan ^[2]; ^[3]; ^[2]; ^[2]; ^[4]; Fontaine, Thierry ^[5]; Latgé, Jean-Paul ^[6]; ^[7]; ^[2]

Michigan State Univ., East Lansing, MI (United States); Florida State Univ., Tallahassee, FL (United States). National High Magnetic Field Lab. (MagLab)
Michigan State Univ., East Lansing, MI (United States)
Tallahassee, FL (United States). National High Magnetic Field Lab. (MagLab)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
Univ. of Paris (France); French National Research Institute for Agriculture, Food and Environment (INRAE), Champenoux (France)
Univ. of Crete, Heraklion (Greece)
Louisiana State University Health Sciences Center, New Orleans, LA (United States)

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.

View Accepted Manuscript (DOE)

Research Organization:: Michigan State Univ., East Lansing, MI (United States); Michigan State University; Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)

Sponsoring Organization:: National Institutes of Health (NIH); National Science Foundation (NSF); USDOE Office of Science (SC); USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-76RL01830; FG02-91ER20021; SC0019072

OSTI ID:: 2480834

Alternate ID(s):: OSTI ID: 2471969
OSTI ID: 2403466

Report Number(s):: PNNL-SA--197650

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 15; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Molecular architecture of fungal cell walls revealed by solid-state NMR

Journal Article · Sun Jul 15 20:00:00 EDT 2018 · Nature Communications · OSTI ID:1511439

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

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