Survival strategies of supraglacial algae-dominated communities in the transition from high light to continual darkness on the Greenland Ice Sheet

Glacier ice algae of the streptophyte genus Ancylonema live on glaciers globally, including the Greenland Ice Sheet, and bloom despite low temperatures, low nutrient availability, and very high light intensities. In polar regions, the long polar night also imposes additional abiotic stressors. However, the cellular mechanisms responsible for Ancylonema’s resistance and adaptation to high light stress or to prolonged darkness during the polar winter are not known. We addressed this knowledge gap by evaluating the functional responses of a Greenland Ice Sheet Ancylonema-dominated microbiome to in-situ light conditions and continual darkness during a 12-day period using amplicon sequencing, metatranscriptomics, and metaproteomics. The microbial community did not substantially change during the 12 days of dark incubation; however, heterotrophs became more transcriptionally active in the dark. Metatranscriptomic and metaproteomic analyses showed that Ancylonema cells underwent high oxidative stress in the light. However, after 12 days in darkness, the algal cells retained functional photosynthetic machinery but downregulated their expression of early shikimate pathway enzyme transcripts. Transcriptional reprogramming linked to sugar uptake and phytohormone signalling was also identified in the dark, providing an insight into the first steps towards algal cell survival through the polar night. These results give us a novel understanding of the gene expression dynamics of glacier ice algae under changing light conditions, providing important clues regarding their adaptation to a harsh and extremely variable environment.