Solid-state NMR molecular snapshots of Aspergillus fumigatus cell wall architecture during a conidial morphotype transition

Autor: Gaëlle Lamon, Alons Lends, Isabel Valsecchi, Sarah Sze Wah Wong, Vincent Duprès, Frank Lafont, James Tolchard, Christine Schmitt, Adeline Mallet, Axelle Grélard, Estelle Morvan, Erick J. Dufourc, Birgit Habenstein, J. Iñaki Guijarro, Vishukumar Aimanianda, Antoine Loquet
Přispěvatelé: Chimie et Biologie des Membranes et des Nanoobjets (CBMN), Université de Bordeaux (UB)-École Nationale d'Ingénieurs des Travaux Agricoles - Bordeaux (ENITAB)-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS), Institut Européen de Chimie et Biologie (IECB), Université de Bordeaux (UB)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Plateforme Technologique de RMN Biologique et HDX-MS - Biological NMR and HDX-MS Technological Platform, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité), Mycologie moléculaire - Molecular Mycology, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Centre d’Infection et d’Immunité de Lille - INSERM U 1019 - UMR 9017 - UMR 8204 (CIIL), Institut Pasteur de Lille, Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Lille-Centre Hospitalier Régional Universitaire [Lille] (CHRU Lille)-Centre National de la Recherche Scientifique (CNRS), CHU Lille, Plate-forme de bioimagerie ultrastructurale - Ultrastructural BioImaging Core Facility, Institut Pasteur [Paris] (IP)-Université Paris Cité (UPCité), We are grateful for the support for equipment from the French Government Programme Investissements d’Avenir France BioImaging (FBI, Agence Nationale de la Recherche, N° ANR-10-INSB-04-01) and the French Government Investissement d’Avenir programme, Laboratoire d’Excellence 'Integrative Biology of Emerging Infectious Diseases' (ANR-10-LABX-62-IBEID). We thank the ANR grants ANR-16-CE11-0020-02 to I.G., A.L., and V.A., ANR-21-CE17-0032-01 to V.A.), as well as the Swiss National Science Foundation (for early postdoc mobility project P2EZP2_184258 to A. Lends. This work has benefited from the Biophysical and Structural Chemistry Platform at Institut Européen de Chimie et Biologie IECB, Centre National de la Recherche Scientifique CNRS Unité d'Appui et de Recherche UAR 3033, INSERM US001, and the CNRS (IR‐RMN FR3050 and Infranalytics FR2054). We also acknowledge the access to the confocal microscope of the Ultrastructural BioImaging core facility of the Institut Pasteur, ANR-10-LABX-0062,IBEID,Integrative Biology of Emerging Infectious Diseases(2010), ANR-16-CE11-0020,FUNHYDRO,Amyloïdes fonctionnels formés par les hydrophobines du pathogène fongique Aspergillus fumigatus(2016), ANR-21-CE17-0032,FUNPOLYVAC,Explorer les polysaccharides fongiques de la paroi cellulaire pour les immunothérapies(2021)
Rok vydání: 2023
Předmět:
Zdroj: Proceedings of the National Academy of Sciences of the United States of America
Proceedings of the National Academy of Sciences of the United States of America, 2023, 120 (6), ⟨10.1073/pnas.2212003120⟩
ISSN: 1091-6490
0027-8424
DOI: 10.1073/pnas.2212003120
Popis: While establishing an invasive infection, the dormant conidia of Aspergillus fumigatus transit through swollen and germinating stages, to form hyphae. During this morphotype transition, the conidial cell wall undergoes dynamic remodeling, which poses challenges to the host immune system and antifungal drugs. However, such cell wall reorganization during conidial germination has not been studied so far. Here, we explored the molecular rearrangement of Aspergillus fumigatus cell wall polysaccharides during different stages of germination. We took advantage of magic-angle spinning NMR to investigate the cell wall polysaccharides, without employing any destructive method for sample preparation. The breaking of dormancy was associated with a significant change in the molar ratio between the major polysaccharides β-1,3-glucan and α-1,3-glucan, while chitin remained equally abundant. The use of various polarization transfers allowed the detection of rigid and mobile polysaccharides; the appearance of mobile galactosaminogalactan was a molecular hallmark of germinating conidia. We also report for the first time highly abundant triglyceride lipids in the mobile matrix of conidial cell walls. Water to polysaccharides polarization transfers revealed an increased surface exposure of glucans during germination, while chitin remained embedded deeper in the cell wall, suggesting a molecular compensation mechanism to keep the cell wall rigidity. We complement the NMR analysis with confocal and atomic force microscopies to explore the role of melanin and RodA hydrophobin on the dormant conidial surface. Exemplified here using Aspergillus fumigatus as a model, our approach provides a powerful tool to decipher the molecular remodeling of fungal cell walls during their morphotype switching.
Databáze: OpenAIRE
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