Characterization of active microbial communities in extreme High Arctic cold saline spring systems with meta’omics

Cryoenvironments, or environments with continuously sub-zero temperatures, present unique challenges to microbial life, including freezing temperatures and high solute concentrations. Study of inhabitant microbes informs our understanding of the cold and saline limits of life on Earth and extraterrestrial bodies. Lost Hammer and Gypsum Hill springs, located on Axel Heiberg Island, Nunavut, in the Canadian High Arctic, are rare examples of perennial cold springs arising in an area of thick permafrost. These springs are perennially sub- or near-zero (-5 to 7°C), hypersaline (7-24%), and anoxic (<1 ppm O2). Lost Hammer is also the coldest known terrestrial methane seep on Earth. Multi-omics methods were used to characterize the metabolic activities and adaptations sustaining microbial life in situ in these extreme environments. In Lost Hammer, a combination of metagenomics, single-amplified genomics, and metatranscriptomics identified a predominantly lithotrophic active microbial community in the sediment utilizing inorganic compounds (hydrogen sulfide, hydrogen, carbon dioxide) as energy and carbon sources, driven in part by sulfide-oxidizing Gammaproteobacteria scavenging trace oxygen. Genomes from active methane-oxidizing archaea (ANME-1), the first identified under ambient sub-zero and hypersaline conditions, showed evidence of putative metabolic flexibility and cold and saline adaptations. Evidence of anaerobic heterotrophic and fermentative lifestyles were identified in candidate phyla DPANN archaea and CG03 bacteria. In Gypsum Hill, metagenomic and metatranscriptomic sequencing and isotopic analysis identified an active microbial community in the spring sediment dominated by sulfur cycling Desulfobacterota and Gammaproteobacteria. Sulfate reduction was dominated by hydrogen-oxidizing chemolithoautotrophic Desulfovibrionaceae sp. and was identified in phyla not typically associated with sulfate reduction in novel lineages of Spirochaetota and Bacteroidota. Highly abundant and active sulfur-reducing Desulfuromusa sp. expressed non-coding RNAs associated with transcriptional regulation, showing potential evidence of putative metabolic flexibility in response to substrate availability. Despite low oxygen availability, sulfide oxidation was primarily attributed to aerobic chemolithoautotrophic Halothiobacillaceae. In the Gypsum Hill spring outflow channels, seasonal microbial streamers were formed by a novel chemolithoautotrophic Thiomicrorhabdus sp. oxidizing sulfide to elemental sulfur. The Thiomicrorhabdus sp. genome contained osmotic and cold stress adaptations, including for the production of extracellular polymeric substances suggested to promote streamer formation and provide cold stress protection. This study identified active, predominantly chemolithoautotrophic microbial communities in extreme cold and hypersaline Arctic springs, providing insights into how microbial life is sustained in Earth’s cryosphere and what types of microbial life could exist in analogous environments on Mars and other astrobiology targets

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