What Are the Functions of Chitin Deacetylases in Aspergillus fumigatus?

Mouyna, Isabelle; Dellière, Sarah; Beauvais, Anne; Gravelat, Fabrice N.; Snarr, Brendan D.; Lehoux, Mélanie; Zacharias, Caitlin; Sun, Yan; Carrion, Steven de Jesus; Pearlman, Eric; Sheppard, Donald C.; Latgé, Jean‐Paul

doi:10.3389/fcimb.2020.00028

Cited by 34 publications

(20 citation statements)

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“…No chitosan signal was observed in these fresh A. fumigatus samples. This is in agreement with a recent genomic study which indicates that the deletion of all deacetylase genes in A. fumigatus does not lead to any significant growth phenotype (Mouyna et al, 2020). Interestingly, the occurrence of a significant amount of chitosan in xerophilic Aspergillus species may indicate that the fungus synthesizes chitosan to make the cell wall more flexible to fight against the increase in osmotic pressure.…”

Section: Spectroscopic and Structural Features Of Fungal Chitosansupporting

confidence: 92%

Structural Polymorphism of Chitin and Chitosan in Fungal Cell Walls From Solid-State NMR and Principal Component Analysis

Fernando

Widanage

Penfield

et al. 2021

Front. Mol. Biosci.

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Chitin is a major carbohydrate component of the fungal cell wall and a promising target for novel antifungal agents. However, it is technically challenging to characterize the structure of this polymer in native cell walls. Here, we recorded and compared 13C chemical shifts of chitin using isotopically enriched cells of six Aspergillus, Rhizopus, and Candida strains, with data interpretation assisted by principal component analysis (PCA) and linear discriminant analysis (LDA) methods. The structure of chitin is found to be intrinsically heterogeneous, with peak multiplicity detected in each sample and distinct fingerprints observed across fungal species. Fungal chitin exhibits partial similarity to the model structures of α- and γ-allomorphs; therefore, chitin structure is not significantly affected by interactions with other cell wall components. Addition of antifungal drugs and salts did not significantly perturb the chemical shifts, revealing the structural resistance of chitin to external stress. In addition, the structure of the deacetylated form, chitosan, was found to resemble a relaxed two-fold helix conformation. This study provides high-resolution information on the structure of chitin and chitosan in their cellular contexts. The method is applicable to the analysis of other complex carbohydrates and polymer composites.

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Section: Spectroscopic and Structural Features Of Fungal Chitosansupporting

confidence: 92%

Structural Polymorphism of Chitin and Chitosan in Fungal Cell Walls From Solid-State NMR and Principal Component Analysis

Fernando

Widanage

Penfield

et al. 2021

Front. Mol. Biosci.

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“…A number of hydrolases required for the breakdown of β-glucan chains and other cell-wall components— i.e., carboxylic ester hydrolyses (CF317_004653-T1, CF317_008040-T1, CF317_002308-T1, CF317_005799-T1), feruloyl esterase (CF317_002949-T1), alongside glucan 1,3-beta-glucosidase (CF317_002004-T1), murein transglycosylase (CF317_006383-T1) and cutinase (CF317_007621-T1) which were downregulated in the mutant proteome—were present in the secretome at levels comprised between 1.5- and 4-folds higher than in the wild type ( Supplementary Table 11 ). The same for mannan endo-1,6-alpha-mannosidase (CF317_001276-T1) and chitin deacetylase (CF317_003258-T1), which play multiple roles in the function of the fungal cell wall ( Spreghini et al, 2003 ; Mouyna et al, 2020 ). In the category transport, the multicopper oxidase (CF317_009669-T1; 1.9-fold), the chloride channel protein (CF317_004136-T; 1.7-folds) and the nitrate/nitrite transporter (CF317_004846-T1; 1.6-fold) represented the most upregulated proteins.…”

Section: Resultsmentioning

confidence: 99%

Effects of Simulated Microgravity on the Proteome and Secretome of the Polyextremotolerant Black Fungus Knufia chersonesos

et al. 2021

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Black fungi are a group of melanotic microfungi characterized by remarkable polyextremotolerance. Due to a broad ecological plasticity and adaptations at the cellular level, it is predicted that they may survive in a variety of extreme environments, including harsh niches on Earth and Mars, and in outer space. However, the molecular mechanisms aiding survival, especially in space, are yet to be fully elucidated. Based on these premises, the rock-inhabiting black fungus Knufia chersonesos (Wt) and its non-melanized mutant (Mut) were exposed to simulated microgravity—one of the prevalent features characterizing space conditions—by growing the cultures in high-aspect-ratio vessels (HARVs). Qualitative and quantitative proteomic analyses were performed on the mycelia and supernatant of culture medium (secretome) to assess alterations in cell physiology in response to low-shear simulated microgravity (LSSMG) and to ultimately evaluate the role of cell-wall melanization in stress survival. Differential expression was observed for proteins involved in carbohydrate and lipid metabolic processes, transport, and ribosome biogenesis and translation via ribosomal translational machinery. However, no evidence of significant activation of stress components or starvation response was detected, except for the scytalone dehydratase, enzyme involved in the synthesis of dihydroxynaphthalene (DNH) melanin, which was found to be upregulated in the secretome of the wild type and downregulated in the mutant. Differences in protein modulation were observed between K. chersonesos Wt and Mut, with several proteins being downregulated under LSSMG in the Mut when compared to the Wt. Lastly, no major morphological alterations were observed following exposure to LSSMG. Similarly, the strains’ survivability was not negatively affected. This study is the first to characterize the response to simulated microgravity in black fungi, which might have implications on future astrobiological missions.

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“…Until now, the full set of cda genes has been deleted in Schizosaccharomyces pombe ( 38 ), Saccharomyces cerevisiae ( 39 , 40 ), C. neoformans ( 41 ), and Aspergillus fumigatus ( 42 ). In all of these species, the mutants were viable and showed defects only under stress conditions.…”

Section: Discussionmentioning

confidence: 99%

Chitosan and Chitin Deacetylase Activity Are Necessary for Development and Virulence of Ustilago maydis

Rizzi

Happel

Lenz

et al. 2021

mBio

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The biotrophic fungus Ustilago maydis harbors a chitin deacetylase (CDA) family of six active genes as well as one pseudogene which are differentially expressed during colonization. This includes one secreted soluble CDA (Cda4) and five putatively glycosylphosphatidylinositol (GPI)-anchored CDAs, of which Cda7 belongs to a new class of fungal CDAs. Here, we provide a comprehensive functional study of the entire family. While budding cells of U. maydis showed a discrete pattern of chitosan staining, biotrophic hyphae appeared surrounded by a chitosan layer. We purified all six active CDAs and show their activity on different chitin substrates. Single as well as multiple cda mutants were generated and revealed a virulence defect for mutants lacking cda7. We implicated cda4 in production of the chitosan layer surrounding biotrophic hyphae and demonstrated that the loss of this layer does not reduce virulence. By combining different cda mutations, we detected redundancy as well as specific functions for certain CDAs. Specifically, certain combinations of mutations significantly affected virulence concomitantly with reduced adherence, appressorium formation, penetration, and activation of plant defenses. Attempts to inactivate all seven cda genes simultaneously were unsuccessful, and induced depletion of cda2 in a background lacking the other six cda genes illustrated an essential role of chitosan for cell wall integrity. IMPORTANCE The basidiomycete Ustilago maydis causes smut disease in maize, causing substantial losses in world corn production. This nonobligate pathogen penetrates the plant cell wall with the help of appressoria and then establishes an extensive biotrophic interaction, where the hyphae are tightly encased by the plant plasma membrane. For successful invasion and development in plant tissue, recognition of conserved fungal cell wall components such as chitin by the plant immune system needs to be avoided or suppressed. One strategy to achieve this lies in the modification of chitin to chitosan by chitin deacetylases (CDAs). U. maydis has seven cda genes. This study reveals discrete as well as redundant contributions of these genes to virulence as well as to cell wall integrity. Unexpectedly, the inactivation of all seven genes is not tolerated, revealing an essential role of chitosan for viability.

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What Are the Functions of Chitin Deacetylases in Aspergillus fumigatus?

Cited by 34 publications

References 50 publications

Structural Polymorphism of Chitin and Chitosan in Fungal Cell Walls From Solid-State NMR and Principal Component Analysis

Structural Polymorphism of Chitin and Chitosan in Fungal Cell Walls From Solid-State NMR and Principal Component Analysis

Effects of Simulated Microgravity on the Proteome and Secretome of the Polyextremotolerant Black Fungus Knufia chersonesos

Chitosan and Chitin Deacetylase Activity Are Necessary for Development and Virulence of Ustilago maydis

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