Abstract
Subzero hypersaline brines are liquid microbial habitats within otherwise frozen environments, where concentrated dissolved salts prevent freezing. Such extreme conditions presumably require unique microbial adaptations, and possibly altered ecologies, but specific strategies remain largely unknown. 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. Overall, both taxonomic composition and functional potential were starkly different. Taxonomically, sea-ice brine communities (∼105 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 (∼108 cells mL–1) lacked these genera and instead were dominated by Marinobacter. 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. 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. Such cryopeg genomic traits provide insight into how long-term environmental stability may enable life to survive extreme conditions.
Highlights
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)
For comparative analyses of the functional potential encoded in the microbial communities in cryopeg brines and sea ice, we focused on molecular functions represented in the KEGG Orthology (KO) database (Kanehisa et al, 2016)
The strongest drivers of the taxonomic variance from cryopeg brines were members of Bacteroidetes, mainly Polaribacter and unclassified Flavobacteriaceae, as well as the gammaproteobacterial genera Paraglaciecola, Glaciecola and Colwellia, and the alphaproteobacterial genus Octadecabacter and SAR11 clade (Figure 1C)—all were dominant in sea ice and near- (
Summary
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). 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, for Arctic sea ice, are pronounced (Overland and Wang, 2013; Stroeve and Notz, 2018). 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). The challenges are many, including safe accessibility, sampling without altering (melting) the habitat, and accounting for the complexities and heterogeneity of the microscale living spaces within ice, especially in sea ice (Junge et al, 2001), which is subject to seasonal extremes in temperature and salinity (Ewert and Deming, 2013, 2014) and fluctuating porosity (Golden et al, 2007; Petrich and Eicken, 2017)
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