Study of fungal cell wall evolution through its monosaccharide composition: An insight into fungal species interacting with plants

Abstract

Every fungal cell is encapsulated in a cell wall, essential for cell viability, morphogenesis, and pathogenesis. Most knowledge of the cell wall composition in fungi has focused on ascomycetes, especially human pathogens, but considerably less is known about early divergent fungal groups, such as species in the Zoopagomycota and Mucoromycota phyla. To shed light on evolutionary changes in the fungal cell wall, we studied the monosaccharide composition of the cell wall of 18 species including early diverging fungi and species in the Basidiomycota and Ascomycota phyla with a focus on those with pathogenic lifestyles and interactions with plants. Our data revealed that chitin is the most characteristic component of the fungal cell wall, and was found to be in a higher proportion in the early divergent groups. The Mucoromycota species possess few glucans, but instead have other monosaccharides such as fucose and glucuronic acid that are almost exclusively found in their cell walls. Additionally, we observed that hexoses (glucose, mannose and galactose) accumulate in much higher proportions in species belonging to Dikarya. Our data demonstrate a clear relationship between phylogenetic position and fungal cell wall carbohydrate composition and lay the foundation for a better understanding of their evolution and their role in plant interactions.

Keywords: Cell wall; Chitin; Fungi; Glucan; Monosaccharide; Mucoran.

Fig. 1

Scheme of the preparation and analysis of fungal cell wall carbohydrates. Discarded fractions are shown in red.

Fig. 2

Phylogenetic relations between fungal species from the Zoopagomycota, Mucoromycota, Basidiomycota and Ascomycota phyla analysed in this study.

Fig. 3

Accumulative analysis of different types of monosaccharides and proteins in fungal cell walls. Absolute amounts (µg/mg cell wall dry weight) of amino sugars, neutral sugars, uronic acids and proteins in 18 fungal species are plotted. Data represent mean ± S.D. of 4 independent measurements.

Fig. 4

Amount of glucosamine, galactosamine and glucose in the cell wall of selected fungal species. Data (µg/mg cell wall dry weight) represent mean ± S.D. of (A) glucosamine and galactosamine and (B) glucose from 4 independent measurements.

Fig. 5

Amount of mannose and galactose in the cell wall of selected fungal species. Data (µg/mg cell wall dry weight) represent mean ± S.D. of (A) mannose and (B) galactose from 4 independent measurements.

Fig. 6

Amount of fucose and glucuronic acid in the cell wall of selected fungal species. Data (µg/mg cell wall dry weight) represent mean ± S.D. of (A) fucose and (B) glucuronic acid from 4 independent measurements.

Fig. 7

Qualitative comparison of the presence of different monosaccharides in several fungal species. A phylogenetic tree including the species analysed is shown on the left-hand side. The size of the coloured circles is scaled from 1 to 10 and refer to the relative concentration for each monosaccharide, according to the concentrations obtained in each species. The symbol “+” means that the respective monosaccharide was detected only in trace amounts (less than 5 µg/mg cell wall dry weight), therefore, it was not scaled. Abbreviations: GlcN (Glucosamine), GalN (Galactosamine), Glc (Glucose), Man (Mannose), Gal (Galactose), Fuc (Fucose), Rha (Rhamnose), GlcA (Glucuronic acid).