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Solid-state NMR molecular snapshots of Aspergillus fumigatus cell wall architecture during a conidial morphotype
Gaëlle Lamon1, Alons Lends1, Isabel Valsecchi2
1Univ. Bordeaux, Centre National de la Recherche Scientifique (CNRS), Bordeaux Institut National Polytechnique, Chemistry and Biology of Membranes and Nanoobjects (CBMN), Unité Mixte de Recherche (UMR) 5248, Institut Européen de Chimie et Biologie (IECB), Pessac F-33607, France.
Abstract:
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.
Insights
Dormant Aspergillus fumigatus conidia undergo cell wall remodeling during germination. Mobile galactosaminogalactan and lipids appear, while glucans become more exposed, aiding morphotype transition.
Area of Science:
- Medical Mycology
- Biochemistry
- Microbial Pathogenesis
Background:
- Aspergillus fumigatus conidia transition from dormant to germinating forms during infection.
- This morphotype transition involves dynamic cell wall remodeling, impacting host immunity and antifungal drug efficacy.
- Understanding fungal cell wall changes during germination is crucial for developing new therapeutic strategies.
Purpose of the Study:
- To investigate the molecular rearrangement of Aspergillus fumigatus cell wall polysaccharides during conidial germination.
- To characterize the changes in cell wall composition and structure associated with the switch from dormant conidia to hyphae.
- To establish a non-destructive method for analyzing fungal cell wall dynamics.
Main Methods:
- Magic-angle spinning Nuclear Magnetic Resonance (NMR) spectroscopy was employed to analyze cell wall polysaccharides without destructive sample preparation.
- Various polarization transfer techniques were used to differentiate between rigid and mobile polysaccharide components.
- Confocal and atomic force microscopy were utilized to study surface components like melanin and hydrophobins.
Main Results:
- A significant shift in the molar ratio of β-1,3-glucan and α-1,3-glucan was observed upon dormancy breaking, with chitin levels remaining constant.
- Mobile galactosaminogalactan emerged as a key marker of germinating conidia.
- Highly abundant triglyceride lipids were detected in the mobile matrix of conidial cell walls, and increased surface exposure of glucans was noted during germination.
Conclusions:
- Fungal cell wall remodeling during Aspergillus fumigatus germination involves significant changes in polysaccharide composition and organization.
- The appearance of mobile galactosaminogalactan and lipids, along with altered glucan exposure, are critical molecular events during morphotype switching.
- The developed NMR approach offers a powerful tool for deciphering fungal cell wall dynamics during critical developmental transitions.
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