Shotgun metagenomics reveals the flexibility and diversity of Arctic marine microbiomes

Polar oceanographic regions are exposed to rapid changes in temperature, salinity, and light fields that determine microbial species distributions, but resilience to an increasingly unstable climate is unknown. To unravel microbial genomic potential of the Northern Baffin Bay's polynya, we constructed eight metagenomes from the same latitude but targeting two sides of Pikialasorsuaq (The North Water) that differ by current systems, stratification, and temperature regimes. Samples from the surface and subsurface chlorophyll maximum (SCM) of both sides were collected 13 months apart. Details of metabolic pathways were determined for 18 bacteria and 10 microbial eukaryote metagenome-assembled genomes (MAGs). The microbial eukaryotic MAGs were associated with the dominant green algae in the Mamiellales and diatoms in the Mediophyceae, which tended to respectively dominate the eastern and western sides of Pikialasorsuaq. We show that microbial community taxonomic and functional signatures were ca. 80% similar at the latitude sampled with only 20% of genes associated with local conditions. From the metagenomes we found genes involved in osmotic regulation, antifreeze proteins, and photosystem protection, with hydrocarbon biodegradation and methane oxidation potential detected. The shared genomic compliment was consistent with adaptation to the Arctic's extreme fluctuating conditions, with implications for their evolutionary history and the long-term survival of a pan-arctic microbiome. In particular, previously unrecognized genetic capabilities for methane bio-attenuation and hydrocarbon metabolism in eukaryotic phytoplankton suggest adaptation to dark conditions that will remain, despite climate warming, in the high latitude offshore waters of a future Arctic.