Microbial Communities in Subpermafrost Saline Fracture Water at the Lupin Au Mine, Nunavut, Canada

Abstract

We report the first investigation of a deep subpermafrost microbial ecosystem, a terrestrial analog for the Martian subsurface. Our multidisciplinary team analyzed fracture water collected at 890 and 1,130 m depths beneath a 540-m-thick permafrost layer at the Lupin Au mine (Nunavut, Canada). 14C, 3H, and noble gas isotope analyses suggest that the Na-Ca-Cl, suboxic, fracture water represents a mixture of geologically ancient brine, approximately25-kyr-old, meteoric water and a minor modern talik-water component. Microbial planktonic concentrations were approximately10(3) cells mL(-1). Analysis of the 16S rRNA gene from extracted DNA and enrichment cultures revealed 42 unique operational taxonomic units in 11 genera with Desulfosporosinus, Halothiobacillus, and Pseudomonas representing the most prominent phylotypes and failed to detect Archaea. The abundance of terminally branched and midchain-branched saturated fatty acids (5 to 15 mol%) was consistent with the abundance of Gram-positive bacteria in the clone libraries. Geochemical data, the ubiquinone (UQ) abundance (3 to 11 mol%), and the presence of both aerobic and anaerobic bacteria indicated that the environment was suboxic, not anoxic. Stable sulfur isotope analyses of the fracture water detected the presence of microbial sulfate reduction, and analyses of the vein-filling pyrite indicated that it was in isotopic equilibrium with the dissolved sulfide. Free energy calculations revealed that sulfate reduction and sulfide oxidation via denitrification and not methanogenesis were the most thermodynamically viable consistent with the principal metabolisms inferred from the 16S rRNA community composition and with CH4 isotopic compositions. The sulfate-reducing bacteria most likely colonized the subsurface during the Pleistocene or earlier, whereas aerobic bacteria may have entered the fracture water networks either during deglaciation prior to permafrost formation 9,000 years ago or from the nearby talik through the hydrologic gradient created during mine dewatering. Although the absence of methanogens from this subsurface ecosystem is somewhat surprising, it may be attributable to an energy bottleneck that restricts their migration from surface permafrost deposits where they are frequently reported. These results have implications for the biological origin of CH4 on Mars.

Taxonomically and functionally diverse microbial communities in deep crystalline rocks of the Fennoscandian shield

“…Previous studies using 16S rRNA gene cloning have reported up to 42 bacterial OTUs in continental crystalline rocks (Gihring et al, 2006;Sahl et al, 2008;Onstott et al, 2009), whereas analysis of rarefied pyrotag data obtained from Outokumpu in this study inferred 48-110 bacterial OTUs per sample (Supplementary Table S4). Archaeal OTU richness also greatly exceeded expectations based on earlier studies, with up to 112 OTUs detected in samples recovered above 1500 m (Takai et al, 2001;Sahl et al, 2008).…”

“…Yet, studies conducted in mines and deep drill holes have documented that microbial life extends several kilometers into the Earth's crystalline crust with diverse microbial communities detected in a variety of continental areas (Havemann et al, 1999;Zhang et al, 2005;Gihring et al, 2006;Sahl et al, 2008;Onstott et al, 2009;Itävaara et al, 2011a;Nyyssö nen et al, 2012). Culture-based studies under laboratory conditions show that these microbial communities include both autotrophic and heterotrophic members with variable modes of metabolism including sulfate and iron reduction, methanogenesis and acetogenesis (Haveman et al, 1999;Haveman and Pedersen, 2002).…”

Microbial diversity and activity in hypersaline high Arctic spring channels

“…Most of the closest relatives for these identified phylotypes were found in cold and/saline environments including Desulfuromonas sp. identified in subpermafrost saline fracture water at the Lupin mine in the Canadian Arctic (Onstott et al 2009). …”

The interglacial–glacial cycle and geochemical evolution of Canadian and Fennoscandian Shield groundwaters

“…Gas hydrates or clathrates, form in certain low temperature and high pressure conditions, in areas with high methane concentrations, including permafrost and deep sea environments (Kvenvolden and Lorenson, 2001). Recently, groundwater and gases were characterized at the Lupin Mine, Canada, within a part of the Canadian Shield affected by 540 m of permafrost (Ruskeeniemi et al, 2002Stotler et al, 2003Stotler et al, , 2006Stotler et al, , 2008Stotler et al, , 2009Stotler et al, , 2010bLambie et al, 2004;Négrel et al, 2004;Casanova et al, 2005;Ahonen et al, 2008;Stotler, 2008;Onstott et al, 2009). At this site, the maximum salinity was 42 g L À1 , and methane hydrate was inferred to be present and stable during the last 120 ky (Stotler et al, , 2010b.…”