Synergistic Photoprotection: Enhanced Stability of Vulpinic Acid through Interaction with Exocellular Polysaccharides

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Lichens have been of great interest in exobiological studies due to their remarkable tolerance to ultraviolet (UV) radiation. These organisms employ extracellular pigments for screening high-energy solar radiation, allowing the photosynthetically active radiation to pass through and be utilized by the photosymbiont. These pigments are found co-occurring within polysaccharide scaffolds in the lichen cortex. Despite extensive studies on isolated lichen pigments, the potential role of exopolysaccharides (EPS) in the photoprotective system of lichens has remained unclear. We report detailed photophysical studies on the wolf lichen pigment vulpinic acid in pullulan, a polysaccharide that mimics lichen EPS. Solid phase studies demonstrate that the pigment’s photostability is greatly enhanced in the pullulan polysaccharide matrix. Analysis of ultrafast transient absorption infrared spectroscopy indicates potential interactions of the polysaccharide inhibiting the relaxation pathway of vulpinic acid upon UV photoexcitation. These polysaccharides interrupt an intramolecular proton transfer that traditionally leads to photodecomposition of the isolated vulpinic acid compound. These results suggest a crucial role of EPS in the photoprotective systems of lichens. The interaction between vulpinic acid and pullulan exemplifies a non-spectator role of polysaccharides in photoprotection, potentially contributing to the extraordinary resilience of lichens and cyanobacteria. This polysaccharide-pigment interaction may represent a general strategy among extremophiles to mitigate UV-induced damage, highlighting the importance of interdisciplinary approaches in unraveling complex biological systems.

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