Direct comparisons between subzero brines that differ in age or stability are rare ( Cooper et al., 2019), and have not yet included an exploration of genomic adaptations to long-term vs.
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With continued warming, opportunities to study these microbes and their current roles in situ dwindle, yet the molecular microbial ecology of the cryosphere remains underexplored compared to other areas of environmental microbiology (reviewed by Deming and Collins, 2017). Though largely frozen, these at-risk environments contain subzero hypersaline brines that provide interior liquid habitat for diverse microbial life of both ecological relevance and inherent curiosity for their unique adaptations to extreme conditions ( Boetius et al., 2015).
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Others, like sea ice, are inherently short-lived, with formation and melting occurring annually ( Vaughan et al., 2013), yet recent losses in areal extent and volume, particularly for Arctic sea ice, are pronounced ( Overland and Wang, 2013 Stroeve and Notz, 2018). Cryosphere components like permafrost, relatively stable features that have remained frozen for thousands or even millions of years ( Froese et al., 2008), are warming now ( Biskaborn et al., 2019 Nitzbon et al., 2020). These frozen regions are incurring significant losses due to climate change ( Fountain et al., 2012). The cryosphere, that portion of the planet where most of the water is frozen, includes more than half of land surfaces and 7% of the surface ocean globally ( Vaughan et al., 2013). Such cryopeg genomic traits provide insight into how long-term environmental stability may enable life to survive extreme conditions. Together these genomic features suggest adaptations and capabilities of sea-ice communities manifesting at the community level through seasonal ecological succession, whereas the denser cryopeg communities appear adapted to intense bacterial competition, leaving fewer genera to dominate with brine-specific adaptations and social interactions that sacrifice some members for the benefit of others. Functionally, however, sea ice encoded fewer accessory traits and lower average genomic copy numbers for shared traits, though DNA replication and repair were elevated in contrast, microbes in cryopeg brines had greater genetic versatility with elevated abundances of accessory traits involved in sensing, responding to environmental cues, transport, mobile elements (transposases and plasmids), toxin-antitoxin systems, and type VI secretion systems. Taxonomically, sea-ice brine communities (∼10 5 cells mL –1) had greater richness, more diversity and were dominated by bacterial genera, including Polaribacter, Paraglaciecola, Colwellia, and Glaciecola, whereas the more densely inhabited cryopeg brines (∼10 8 cells mL –1) lacked these genera and instead were dominated by Marinobacter.
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Overall, both taxonomic composition and functional potential were starkly different. Here we examined prokaryotic taxonomic and functional diversity in two seawater-derived subzero hypersaline brines: first-year sea ice, subject to seasonally fluctuating conditions and ancient cryopeg, under relatively stable conditions geophysically isolated in permafrost. Such extreme conditions presumably require unique microbial adaptations, and possibly altered ecologies, but specific strategies remain largely unknown. Subzero hypersaline brines are liquid microbial habitats within otherwise frozen environments, where concentrated dissolved salts prevent freezing.