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Ecogenomics and Adaptation Strategies of Southern Ocean Viral Communities.

ABSTRACT: 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.

SUBMITTER: Alarcon-Schumacher T

PROVIDER: S-EPMC8407431 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:Viruses directly affect the most important biological processes in the ocean via their regulation of prokaryotic and eukaryotic populations. Marine sponges form stable symbiotic partnerships with a wide diversity of microorganisms and this high symbiont complexity makes them an ideal model for studying viral ecology. Here, we used morphological and molecular approaches to illuminate the diversity and function of viruses inhabiting nine sponge species from the Great Barrier Reef and seven from the Red Sea. RESULTS:Viromic sequencing revealed host-specific and site-specific patterns in the viral assemblages, with all sponge species dominated by the bacteriophage order Caudovirales but also containing variable representation from the nucleocytoplasmic large DNA virus families Mimiviridae, Marseilleviridae, Phycodnaviridae, Ascoviridae, Iridoviridae, Asfarviridae and Poxviridae. Whilst core viral functions related to replication, infection and structure were largely consistent across the sponge viromes, functional profiles varied significantly between species and sites largely due to differential representation of putative auxiliary metabolic genes (AMGs) and accessory genes, including those associated with herbicide resistance, heavy metal resistance and nylon degradation. Furthermore, putative AMGs varied with the composition and abundance of the sponge-associated microbiome. For instance, genes associated with antimicrobial activity were enriched in low microbial abundance sponges, genes associated with nitrogen metabolism were enriched in high microbial abundance sponges and genes related to cellulose biosynthesis were enriched in species that host photosynthetic symbionts. CONCLUSIONS:Our results highlight the diverse functional roles that viruses can play in marine sponges and are consistent with our current understanding of sponge ecology. Differential representation of putative viral AMGs and accessory genes across sponge species illustrate the diverse suite of beneficial roles viruses can play in the functional ecology of these complex reef holobionts. Video Abstract.

Project description:Arctic regions, which are changing rapidly as they warm 2 to 3 times faster than the global average, still retain microbial habitats that serve as natural laboratories for understanding mechanisms of microbial adaptation to extreme conditions. Seawater-derived brines within both sea ice (sea-ice brine) and ancient layers of permafrost (cryopeg brine) support diverse microbes adapted to subzero temperatures and high salinities, yet little is known about viruses in these extreme environments, which, if analogous to other systems, could play important evolutionary and ecosystem roles. Here, we characterized viral communities and their functions in samples of cryopeg brine, sea-ice brine, and melted sea ice. Viral abundance was high in cryopeg brine (1.2 × 108 ml-1) and much lower in sea-ice brine (1.3 × 105 to 2.1 × 105 ml-1), which roughly paralleled the differences in cell concentrations in these samples. Five low-input, quantitative viral metagenomes were sequenced to yield 476 viral populations (i.e., species level; ≥10 kb), only 12% of which could be assigned taxonomy by traditional database approaches, indicating a high degree of novelty. Additional analyses revealed that these viruses: (i) formed communities that differed between sample type and vertically with sea-ice depth; (ii) infected hosts that dominated these extreme ecosystems, including Marinobacter, Glaciecola, and Colwellia; and (iii) encoded fatty acid desaturase (FAD) genes that likely helped their hosts overcome cold and salt stress during infection, as well as mediated horizontal gene transfer of FAD genes between microbes. Together, these findings contribute to understanding viral abundances and communities and how viruses impact their microbial hosts in subzero brines and sea ice.IMPORTANCE This study explores viral community structure and function in remote and extreme Arctic environments, including subzero brines within marine layers of permafrost and sea ice, using a modern viral ecogenomics toolkit for the first time. In addition to providing foundational data sets for these climate-threatened habitats, we found evidence that the viruses had habitat specificity, infected dominant microbial hosts, encoded host-derived metabolic genes, and mediated horizontal gene transfer among hosts. These results advance our understanding of the virosphere and how viruses influence extreme ecosystems. More broadly, the evidence that virally mediated gene transfers may be limited by host range in these extreme habitats contributes to a mechanistic understanding of genetic exchange among microbes under stressful conditions in other systems.

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Ecogenomics and Adaptation Strategies of Southern Ocean Viral Communities.

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