The biological darkening of the Greenland Ice Sheet: impacts of visible and UV light on the photosynthetic performance, metabolome and transcriptome of glacier algae

Large blooms of purple-brownish pigmented glacier algae cover the ablation zones of the Greenland Ice Sheet (GrIS) and amplify its melt by lowering the ice surface albedo and increasing its solar radiation absorption. The darkening effect of these Zygnematophycean algae can be mainly attributed to their phenolic pigments, which absorb in the visible (VIS) and UV light ranges. Currently, a mechanistic understanding of the factors regulating the production of these pigments and their implications for the large-scale biologically-driven albedo reduction on the GrIS is missing. Here, we reveal how light (VIS vs. UV range) controls the phenolic pigment production, endo- and exometabolome, gene expression and photosynthetic performance of glacier algae. Two different algal communities (a mixed natural microbial community collected from snow-free ice and a laboratory-grown community of the ice algae Mesotaenium berggrenii without its original dark pigmentation) were used for a set of in situ incubations on Mittivakkat glacier in SE-Greenland. Pulse-amplitude-modulated (PAM) fluorometry revealed an overall higher photosynthetic performance (electron transport rate) at higher irradiances for the field population containing purpurogallin-like pigments compared to the lab community without dark pigmentation. The lab population showed a low maximum quantum efficiency of photosystem II under in situ light conditions, indicating a photo-damaging effect from high intensities of UV light in the absence of purpurogallin-derived phenolic pigments. Our study highlights the intracellular shading effect by purpurogallin-derived pigments, which are key for the survival of glacier algae on the ice and forms a cornerstone of understanding the large-scale variability in the biological darkening of the GrIS.