Lower viral evolutionary pressure under stable versus fluctuating conditions in subzero Arctic brines

Abstract

Background: Climate change threatens Earth’s ice-based ecosystems which currently offer archives and eco-evolutionary experiments in the extreme. Arctic cryopeg brine (marine-derived, within permafrost) and sea-ice brine, similar in subzero temperature and high salinity but different in temporal stability, are inhabited by microbes adapted to these extreme conditions. However, little is known about their viruses (community composition, diversity, interaction with hosts, or evolution) or how they might respond to geologically stable cryopeg versus fluctuating sea-ice conditions. Results: We used long- and short-read viromics and metatranscriptomics to study viruses in Arctic cryopeg brine, sea-ice brine, and underlying seawater, recovering 11,088 vOTUs (~species-level taxonomic unit), a 4.4-fold increase of known viruses in these brines. More specifically, the long-read-powered viromes doubled the number of longer (≥25 kb) vOTUs generated and recovered more hypervariable regions by >5-fold compared to short-read viromes. Distribution assessment, by comparing to known viruses in public databases, supported that cryopeg-brine viruses were of marine origin yet distinct from either sea-ice-brine or seawater viruses, while 94% of sea-ice-brine viruses also presented in seawater. A virus-encoded, ecologically important exopolysaccharide biosynthesis gene was identified, and many viruses (~half of metatranscriptome-inferred ‘active’ vOTUs) were predicted as actively infecting the dominant microbial genera Marinobacter and Polaribacterin cryopeg and sea-ice brines, respectively. Evolutionarily, microdiversity (intra-species genetic variations) analyses suggested that viruses within the stable cryopeg brine were under significantly lower evolutionary pressures than those in the fluctuating sea-ice environment, while many sea-ice-brine virus-tail genes were under positive selection, indicating virus-host co-evolutionary arms races. Conclusions: Our results confirmed the benefits of long-read-powered viromics in understanding the environmental virosphere through significantly improved genomic recovery, expanding viral discovery and the potential for biological inference. Evidence of viruses actively infecting the dominant microbes in subzero brines and modulating host metabolism underscored the potential impact of viruses on these remote and underexplored extreme ecosystems. Microdiversity results shed light on the different strategies viruses use to evolve and adapt when extreme conditions are stable versus fluctuating. Together, these findings verify the value of long-read-powered viromics and provide foundational data on viral evolution and virus-microbe interactions in Earth’s destabilized and rapidly disappearing cryosphere.

Temporal turnover of viral biodiversity and functional potential in intertidal wetlands

“…In this study, significant correlations and similar temporal patterns were observed for viral macro-and micro-diversity. This finding is consistent with a recent study of ocean viruses at the regional scale 16 . This suggested that the viral compositional heterogeneity at large spatial scales may have hampered the association between macro-and micro-diversity 15 .…”

“…Besides macro-diversity, the temporal patterns of viral micro-diversity were also investigated. Micro-diversity (i.e., intra-population diversity) is represented by nucleotide diversity and offers insights into population-level selection pressures 16,29 . For large organisms, the macro-and micro-diversity are often correlated across habitats sharing similar species pools 17,30 .…”

“…As a result, the taxonomic diversity 12,13 and functional potential 14,15 of viruses in various ecosystems can be systematically investigated. Notably, several studies have directed their attention from examining viral macrodiversity variations to delving into micro-diversity variations, which can provide in-depth information for understanding how genetic drift and environmental selection shape viral communities 16,17 .…”

Breaking the Ice: A Review of Phages in Polar Ecosystems

“…Phylogenetic clustering of viral with microbial FAD genes revealed origin of these genes from Bacteroidetes and proteobacterial hosts at least for sea ice suggesting phage-host transfer for these AMGs, whereas cryopeg-derived viral FAD gene origin was less traceable. In addition to more FAD encoding viruses, a recent preprint identified a new AMG in Arctic brine viruses, namely epsG, having a role in biofilm formation Phages in polar ecosystems 10 and extracellular polysaccharide (EPS) production [56]. In subzero brines, microbes were previously shown to use EPS as cryo-and osmoprotectant [57,58] [60].…”

Viruses in deep-sea cold seep sediments harbor diverse survival mechanisms and remain genetically conserved within species

“…For example, depth-dependent evolutionary strategies of viruses were observed in the Mediterranean Sea 9 and grassland soil in northern California 10 . Large viral microdiversity was observed for perhaps the most abundant ocean virus in temperate and tropical waters infecting Pelagibacter 23 , whereas viruses were under significantly low evolutionary pressures in stable subzero Arctic brines 24 . The principles governing the viral evolution likely differ depending on environmental conditions, such as host dynamics, physicochemical properties, and population sizes [25][26][27] .…”