Viral dynamics at the Central Arctic air-water interface

In polar environments, aquatic viruses are challenged with low host availability and harsh environmental conditions. Due to restricted ecosystem accessibility, knowledge about viruses from near-atmosphere aquatic ecosystems around the North Pole is lacking. Here, our aim was to investigate viral diversity, adaptations, and host interactions at the air-water interface in the Central Arctic. Aquatic samples were collected from ~60 cm depth and the submillimeter surface microlayer (SML) during the Synoptic Arctic Survey expedition on icebreaker Oden in summer 2021. Samples were taken from a melt pond in the ice and the ocean before undergoing size-fractioned filtration. Genome-resolved metagenomics and cultivation were applied to investigate prokaryotes and viruses. Diversity of the melt pond was lower compared to open water and dominated by Aquiluna sp. (phylum Actinobacteriota) whose reconstructed small genome encoded for a limited metabolic potential. From 1154 viral operational taxonomic units (vOTUs), two-thirds were predicted bacteriophages. Auxiliary metabolic genes (AMGs) were detected in 17.2% of all vOTUs, of which 26.6% carried more than one AMG. Abundant AMGs with functions in amino acid, porphyrin, and glycan polymer metabolism were detected. Glycerol-3-phosphate cytidylyltransferase with a potential role in the host"s cryoprotection was encoded by 16 vOTUs. The presence of vOTUs at several stations was more strongly correlated to vOTU abundance in the SML than in the underlying water, suggesting dispersal to be mediated by the air-sea boundary layer. More prophages occurred in SML-derived genomes, and a prophage of the bacterial strain Leeuwenhoekiella aequorea Arc30 was inducible with mitomycin C. Electron microscopy revealed that the induced phage vB_LaeS_Arctus_1 was a siphovirus. Arctus_1 had a 42.7 kb circular genome, shared little protein similarities with known phages, placing it in a novel genus. The results demonstrate that Arctic viruses have elaborate strategies to endure in remote, inhospitable, and host-limited environments.