Microbial characterization of a subzero, hypersaline methane seep in the Canadian High Arctic

Abstract

We report the first microbiological characterization of a terrestrial methane seep in a cryoenvironment in the form of an Arctic hypersaline (B24% salinity), subzero (À5 1C), perennial spring, arising through thick permafrost in an area with an average annual air temperature of À15 1C. Bacterial and archaeal 16S rRNA gene clone libraries indicated a relatively low diversity of phylotypes within the spring sediment (Shannon index values of 1.65 and 1.39, respectively). Bacterial phylotypes were related to microorganisms such as Loktanella, Gillisia, Halomonas and Marinobacter spp. previously recovered from cold, saline habitats. A proportion of the bacterial phylotypes were cultured, including Marinobacter and Halomonas, with all isolates capable of growth at the in situ temperature (À5 1C). Archaeal phylotypes were related to signatures from hypersaline deep-sea methane-seep sediments and were dominated by the anaerobic methane group 1a (ANME-1a) clade of anaerobic methane oxidizing archaea. CARD-FISH analyses indicated that cells within the spring sediment consisted of B84.0% bacterial and 3.8% archaeal cells with ANME-1 cells accounting for most of the archaeal cells. The major gas discharging from the spring was methane (B50%) with the low CH 4 /C 2 þ ratio and hydrogen and carbon isotope signatures consistent with a thermogenic origin of the methane. Overall, this hypersaline, subzero environment supports a viable microbial community capable of activity at in situ temperature and where methane may behave as an energy and carbon source for sustaining anaerobic oxidation of methane-based microbial metabolism. This site also provides a model of how a methane seep can form in a cryoenvironment as well as a mechanism for the hypothesized Martian methane plumes.

Microbial diversity and activity in hypersaline high Arctic spring channels

“…Molecular analyses (bacterial and archaeal 16S rRNA gene clone libraries, CARD-FISH) detected bacterial phylotypes related to microorganisms previously recovered from cold, saline habitats. Archaeal phylotypes were related to those found in hypersaline deepsea methane-seep sediments and were dominated by the ANaerobic MEthane group 1a (ANME-1a) clade of anaerobic methane oxidizing archaea indicating that the thermogenic methane exsolving from the LH spring source may act as an energy and carbon source for sustaining anaerobic oxidation of methane-based microbial metabolism under ambient hypersaline, subzero conditions (Niederberger et al 2010).…”

“…In addition to prolonged exposure to subzero temperatures, microbial communities existing in such cryoenvironments must overcome extremely low rates of nutrient and metabolite transfer, high solute concentrations, low water activity, and potentially high background radiation (Ayala-del-Rio et al 2010;Bakermans 2008;Steven et al 2006). Nevertheless, microbial diversity, ecology and activity have been recently described in numerous cryoenvironment habitats and generally indicate that viable microbial communities consisting of bacteria, archaea, viruses, and eukaryotes exist in these extreme habitats (Bakermans 2008(Bakermans , 2012Priscu and Christner 2004;Steven et al 2006;Wells and Deming 2006;and reviewed in Margesin and Miteva 2011) and are capable of both growth and metabolic activity at ambient subzero temperatures (Anesio et al 2007;Bakermans 2012;Bottos et al 2008;D'Amico et al 2006;Niederberger et al 2010;Steven et al 2008). Cold-adapted microorganisms inhabiting such environments exhibit a variety of modifications to their proteins, nucleic acids, and membranes, which allow them to maintain their fluidity, flexibility and associated activity at low temperatures, as well as other adaptations including cryoprotectant production, and highly efficient regulation of growth (Ayala-del-Rio et al 2010;Bakermans 2008).…”

“…We recently described the microbial communities inhabiting Lost Hammer (LH) spring source, a hypersaline (24% salinity), subzero (-5°C) perennial spring that is the only known terrestrial hypersaline CH 4 seep in a cryoenvironment on Earth arising through thick permafrost (Niederberger et al 2010). Numerous sources of methane seeps including deep-sea marine margins where methane hydrates occur (Valentine 2002;Valentine and Reeburgh 2000) and terrestrial thermokarst lakes (Anthony et al 2010;Isaksen et al 2011;Matveeva et al 2003) are known to exist and have been described in both Arctic and sub-Arctic regions, however, the microbial communities have rarely been explored.…”

Microbial life at −13 °C in the brine of an ice-sealed Antarctic lake

“…The understanding of ecosystems based on energy sources other than the Sun comes mainly from realms where hydrothermal processes have provided reduced compounds necessary to fuel chemosynthetically driven ecosystems. Methane derived from thermogenic or biogenic sources can also support microbial communities in deep sea (7) and high arctic cold saline seeps (8). More recently, discoveries of life and associated processes in deep terrestrial subsurface ecosystems (9) provide compelling evidence of subsurface life that in some cases is fueled by nonphotosynthetic processes.…”

Diversity of Arctic pelagic <i>Bacteria</i> with an emphasis on photoheterotrophs: a review

“…4). Two of them (phylogroups E and F) belonged to the Rhodobacterales that is one of the most common alphaproteobacterial order in polar and subpolar oceans (Fu et al, 2010;Ghiglione and Murray, 2012;Niederberger et al, 2010;Prabagaran et al, 2007;Salka et al, 2008;Selje et al, 2004). Loktanella-like puf M clones (phylotype F) dominated the libraries at both seasons, whereas proportions of Sulfitobacter-related sequences (phylogroup E) increased in winter.…”