Viral challenges and adaptations between Central Arctic Ocean and atmosphere

Aquatic viruses act as key players in shaping microbial communities. In polar environments, they face significant challenges like limited host availability and harsh conditions. However, due to restricted ecosystem accessibility, our understanding of viral diversity, abundance, adaptations, and host interactions remains limited. To fill this knowledge gap, we studied viruses from atmosphere-close aquatic ecosystems in the Central Arctic and Northern Greenland. Aquatic samples for virus-host analysis were collected from ~60 cm depth and the submillimeter surface microlayer (SML) during the Synoptic Arctic Survey 2021 on icebreaker Oden in Arctic summer. Water was sampled from a melt pond and open water before undergoing size-fractioned filtration and followed by genome-resolved metagenomic and cultivation investigations. The prokaryotic diversity in the melt pond was considerably lower compared to open water. The melt pond was dominated by a Flavobacterium sp. and Aquiluna sp., the latter having a relatively small genome size of 1.2 Mb and the metabolic potential to generate ATP using the phosphate acetyltransferase-acetate kinase pathway. Viral diversity on the host fraction (0.2 – 5 µm) of the melt pond was strikingly limited compared to open water. From 1154 dereplicated viral operational taxonomic units (vOTUs), of which two-thirds were predicted bacteriophages, 17.2% encoded for auxiliary metabolic genes (AMGs) with metabolic functions. Some AMGs like glycerol-3-phosphate cytidylyltransferase and ice-binding like proteins might serve cryoprotection of the host. Prophages were often associated with SML genomes, and two active prophages of a new viral genera from the Arctic SML strain Leeuwenhoekiella aequorea Arc30 were induced. We found evidence that vOTU abundance in the SML compared to ~60 cm depth was more positively correlated to the distribution of a vOTU across five different Arctic stations. The results indicate that viruses employ elaborated strategies to endure in extreme and host-limited environments. Moreover, our observations suggest that the immediate air-sea interface serves as a platform for viral distribution in the Central Arctic.