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The cold saline springs at Gypsum Hill (GH) and Colour Peak (CP) in the Canadian high Arctic are rare examples of perennial flows in thick continuous permafrost. We surveyed the microbial diversity of the springs by analyzing clone libraries of the small subunit rRNA gene. Half of the bacterial clones from the GH library classified as Delta- and Gammaproteobacteria. Clones related to Proteobacteria (82%), Firmicutes (9%) and Bacteroidetes (6%) constituted 97% of the bacterial library from CP. At least 56 and 76% of the bacterial clones from GH and CP, respectively, were from putative sulfur-metabolizers, and clones related to the sulfur-oxidizing bacterium Thiomicrospira psychrophila dominated in both springs. Archaeal clones were affiliated with uncultured Crenarchaeota, methanogens and haloarchaea. The eukaryotic clones were related to known Fungi, Viridiplantae (green algae), Strametopila (e.g. diatoms), Cercozoa and Alveolata in the CP sediment. Eukaryotic rRNA genes could not be amplified from the GH sediments. Forty-nine phylotypes of heterotrophic and sulfur-oxidizing bacteria (Thiomicrospira, Halothiobacillus ) were isolated from the GH springs. The strains were predominantly psychrotrophic and halotolerant, and were most related to bacteria also isolated from permanently cold environments. Some heterotrophic strains possessed genes for photosynthesis and thiosulfate oxidation, possibly enabling them to better compete in these sulfur-rich ecosystems exposed to continuous light in the summer. Assays of leucine and CO2 incorporation showed a low heterotrophic activity in the GH spring water, but significant autotrophic activity in complete darkness (chemoautotrophy). Microbial sulfur metabolism was demonstrated in microcosms of the GH sediment. Sulfur oxidation and chemoautotrophy were also demonstrated in microbial filaments that thrive in the GH spring channels. Fluorescence in situ hybridization (FISH) showed that the filaments were almost exclusively composed of rod-shaped Gammaproteobacteria that were further identified as Thiomicrospira. This work describes active microbial communities capable of sustainability in extreme environments that combine low temperature, moderate salinity, and prolonged periods of continuous light or darkness. Sulfur oxidation seems to be a major energetic process and chemolithoautotrophy appears to contribute significantly to primary production. Similar hydrosystems, formed by brines in the cold permafrost, are hypothesized to exist on Mars.

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