Chaotropic Ions Reshape the Cell Wall of the Obligate Halophile Aspergillus atacamensis: Insight from Solid-State NMR

Fungal survival in hypersaline environments requires exceptional adaptation of polysaccharide-based cell walls, yet the molecular principles underlying these adaptations remain largely unknown due to the extreme rarity of obligate halophilic fungi. Aspergillus atacamensis is an obligate halophile and chaotolerant fungus capable of growth at saturating NaCl concentrations and unusually high levels of MgCl2. Here, we used multidimensional solid-state NMR spectroscopy to investigate the molecular organization, hydration, and dynamics of cell wall polysaccharides in intact, uniformly 13C-labeled A. atacamensis cells grown under kosmotropic NaCl and chaotropic MgCl2 conditions. Under NaCl conditions, the rigid cell wall core was dominated by {beta}-1,3-glucan and chitin across all salinities. Hyperosmotic NaCl induced thinner, dehydrated walls with increased polysaccharide mobility. In contrast, MgCl2 exposure resulted in marked remodeling of wall carbohydrates, including the emergence of chitosan, incorporation of mannan into the rigid phase, increased wall thickness, and enhanced hydration and dynamics. Together, these findings reveal fundamentally distinct polysaccharide remodeling strategies in response to kosmotropic versus chaotropic stress and establish a molecular framework for understanding fungal survival in extreme ionic environments. GRAPHICAL ABSTRACT O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=80 SRC="FIGDIR/small/700186v1_ufig1.gif" ALT="Figure 1"> View larger version (27K): org.highwire.dtl.DTLVardef@a38e89org.highwire.dtl.DTLVardef@1e2f7fdorg.highwire.dtl.DTLVardef@71a94org.highwire.dtl.DTLVardef@61f2c4_HPS_FORMAT_FIGEXP M_FIG C_FIG HIGHLIGHTSO_LISolid-state NMR reveals salt-dependent remodeling of fungal cell wall polysaccharides C_LIO_LIKosmotropic and chaotropic salts drive distinct cell wall adaptation strategies C_LIO_LINaCl stress promotes dehydration and compaction of the {beta}-1,3-glucan-chitin framework C_LIO_LIMgCl2 induces chitosan emergence and alters mannan organization in the rigid phase C_LIO_LIPolysaccharide hydration and dynamics encode fungal adaptation to extreme environments C_LI