Microbial functional potential of Arctic freshwater ponds and the environmental origin of their diversity

The Arctic holds more surface water than any other region on Earth. Yet its freshwater microbial communities remain largely understudied owing to their remoteness and challenging access. Arctic freshwater systems are regarded as sinks for algal-derived carbon. The structure of their microbial communities critically determines whether biogeochemical cycling is dominated by carbon autotrophy or heterotrophy. Hydrological runoff from the terrestrial environment can influence the microbial community structure of these freshwater systems, both through colonization and the input of allochthonous organic matter. In Greenland, climate change has shortened the ice-covered period of inland freshwater systems and increased precipitation. Consequently, Arctic lakes and ponds face greater inputs of dissolved organic matter and nutrients from both the underlying thawing permafrost and from the washed-out surrounding soil. The shorter ice-covered period, coupled with elevated nutrient input, is likely to increase microbial breakdown of organic matter and the release of carbon dioxide and methane. This raises the concern that Arctic freshwater systems will shift to net heterotrophy. Here, we show the differences in prokaryotic community structures between High-Arctic ponds and tundra soils at the species level, while highlighting the relative abundance of heterotrophs and autotrophs. To determine the structure and functional potential of prokaryotic communities, we conducted a genome-resolved metagenomic analysis of permanent and ephemeral ponds, including their upslope tundra soil, in a deglaciated High-Arctic desert. Our study location on the Princess Ingeborg Peninsula (81°36' N, 16°40' W) in Greenland provides a unique opportunity to compare the metagenomes of two habitats exposed to minimal anthropogenic interference. We investigated whether these habitats have the potential to act as carbon sinks or sources and whether tundra soil serves as a potential reservoir for the microbial colonization of newly emerging freshwater systems in the Arctic. Our work provides new insights into Arctic microbial communities, thereby contributing to a better understanding of how climate change could affect biogeochemical cycles in the Arctic region.