The Aspergillus fumigatus Extracellular Polysaccharide Galactosaminogalactan Displays Context-Dependent Cooperative and Competitive Social Traits in Mixed Biofilms

Biofilm-dwelling cells construct communities by secreting extracellular polysaccharide (EPS). In bacteria, EPS can act as cooperative public goods or competitive traits, yet the social nature of EPS in fungi remains poorly understood. Galactosaminogalactan (GAG) is an EPS produced by the human-pathogenic fungus <i>Aspergillus fumigatus</i>. The study of social characteristics of GAG revealed that under basal conditions, GAG can be shared between GAG production strain (GAG⁺) and non-production strain (GAG^-) in mixed biofilms. This led to significant competitive advantages for GAG^-, with fitness outcomes dependent on initial inoculum ratios, cultivation duration, and nutrient availability. Conversely, under cell wall stress induced by antifungal drug caspofungin, GAG confers a competitive advantage for GAG⁺ in the mixed biofilms. Further investigation revealed that GAG⁺ cells are able to retain higher levels of GAG on the hyphal surface compared to GAG^- in the mixed biofilms. This hyphal surface-associated GAG layer might protect GAG⁺ from caspofungin-mediated damage, creating a lineage-specific competitive advantage. Overall, GAG has a dual-trait social nature in biofilms, functioning as a public good at the population level and as a competitive trait for the producing lineage, switching according to environmental conditions.