Metabolome-mediated biocryomorphic evolution promotes carbon fixation in Greenlandic cryoconite holes

Microbial photoautotrophs on glaciers engineer the formation of granular microbial-mineral aggregates termed cryoconite which accelerate ice melt, creating quasi-cylindrical pits called ‘cryoconite holes’. These act as biogeochemical reactors on the ice surface and provide habitats for remarkably active and diverse microbiota. Evolution of cryoconite holes towards an equilibrium depth is well known, yet interactions between microbial activity and hole morphology are currently weakly addressed. Here, we experimentally perturbed the depths and diameters of cryoconite holes on the Greenland Ice Sheet. Cryoconite holes responded by sensitively adjusting their shapes in three dimensions (‘biocryomorphic evolution’) thus maintaining favourable conditions for net autotrophy at the hole floors. Non-targeted metabolomics reveals concomitant shifts in cyclic AMP and fucose metabolism consistent with phototaxis and extracellular polymer synthesis indicating metabolomic-level granular changes in response to perturbation. We present a conceptual model explaining this process and suggest that it results in remarkably robust net autotrophy on the Greenland Ice Sheet. We also describe observations of cryoconite migrating away from shade, implying a degree of self-regulation of carbon budgets over mesoscales. Since cryoconite is a microbe-mineral aggregate, it appears that microbial processes themselves form and maintain stable autotrophic habitats on the surface of the Greenland ice sheet.