Ecogenomics and Adaptation Strategies of Southern Ocean Viral Communities

The Southern Ocean (SO) represents up to one-fifth of the total carbon drawdown worldwide. Intense selective pressures (low temperature, high UV radiation, and strong seasonality) and physical isolation characterize the SO, serving as a "natural" laboratory for the study of ecogenomics and unique adaptations of endemic viral populations. Here, we report 2,416 novel viral genomes from the SO, obtained from newly sequenced viral metagenomes in combination with mining of publicly available data sets, which represents a 25% increase in the SO viral genomes reported to date. They comprised 567 viral clusters (defined as approximately genus-level groups), with 186 genera endemic to the SO, demonstrating that the SO viral community is predominantly constituted by a large pool of genetically divergent viral species from widespread viral families. The predicted proteome from SO viruses revealed that several protein clusters related to cold-shock-event responses and quorum-sensing mechanisms involved in the lysogenic-lytic cycle shift decision were under positive selection, which is ultimately important for fine adaptation of viral populations in response to the strong selective pressures of the SO. Finally, changes in the hydrophobicity patterns and amino acid frequencies suggested marked temperature-driven genetic selection of the SO viral proteome. Our data provide valuable insights into how viruses adapt and remain successful in this extreme polar marine environment. IMPORTANCE Viruses are the most abundant biologic entities in marine systems and strongly influence the microbial community composition and diversity. However, little is known about viral communities' adaptation and diversification in the ocean. In this work, we take advantage of the geographical isolation and the intense selective pressures of the SO, to which viruses are exposed, to identify potential viral adaptations due to positive environmental selection and dispersal limitation. To that end, we recovered more than two thousand novel viral genomes, revealing a high degree of divergence in these SO endemic communities. Furthermore, we describe remarkable viral adaptations in amino acid frequencies and accessory proteins related to cold shock response and quorum sensing that allow them to thrive at lower temperatures. Consequently, our work greatly expands the understanding of the diversification of the viral communities of the SO and their particular adaptations to low temperatures.