Microbial Community Structure of Subglacial Lake Whillans, West Antarctica

Abstract

Subglacial Lake Whillans (SLW) is located beneath ∼800 m of ice on the Whillans Ice Stream in West Antarctica and was sampled in January of 2013, providing the first opportunity to directly examine water and sediments from an Antarctic subglacial lake. To minimize the introduction of surface contaminants to SLW during its exploration, an access borehole was created using a microbiologically clean hot water drill designed to reduce the number and viability of microorganisms in the drilling water. Analysis of 16S rRNA genes (rDNA) amplified from samples of the drilling and borehole water allowed an evaluation of the efficacy of this approach and enabled a confident assessment of the SLW ecosystem inhabitants. Based on an analysis of 16S rDNA and rRNA (i.e., reverse-transcribed rRNA molecules) data, the SLW community was found to be bacterially dominated and compositionally distinct from the assemblages identified in the drill system. The abundance of bacteria (e.g., Candidatus Nitrotoga, Sideroxydans, Thiobacillus, and Albidiferax) and archaea (Candidatus Nitrosoarchaeum) related to chemolithoautotrophs was consistent with the oxidation of reduced iron, sulfur, and nitrogen compounds having important roles as pathways for primary production in this permanently dark ecosystem. Further, the prevalence of Methylobacter in surficial lake sediments combined with the detection of methanogenic taxa in the deepest sediment horizons analyzed (34–36 cm) supported the hypothesis that methane cycling occurs beneath the West Antarctic Ice Sheet. Large ratios of rRNA to rDNA were observed for several operational taxonomic units abundant in the water column and sediments (e.g., Albidiferax, Methylobacter, Candidatus Nitrotoga, Sideroxydans, and Smithella), suggesting a potentially active role for these taxa in the SLW ecosystem. Our findings are consistent with chemosynthetic microorganisms serving as the ecological foundation in this dark subsurface environment, providing new organic matter that sustains a microbial ecosystem beneath the West Antarctic Ice Sheet.

Physiological Ecology of Microorganisms in Subglacial Lake Whillans

“…Similarly, some studies suggest that maintaining high concentrations of rRNA transcripts relative to rRNA genes also allows microorganisms to adapt to changing conditions (reviewed in Blazewicz et al, 2013). High ratios of amplified 16S rRNA transcripts to genes have been associated with certain taxa in SLW (Achberger et al, 2016). In SLW, low growth efficiency and high rRNA transcript-to-gene ratios suggest that heterotrophic microorganisms in the lake maintain metabolic flexibility that may be important in dealing with changing physicochemical conditions.…”

“…SLW is relatively isolated from anthropogenic inputs, and a metagenomic analysis of the microbial community does not indicate that N-fixation as an important process in the lake (Achberger, 2016). The nitrate in SLW is microbially, rather than atmospherically, derived (Christner et al, 2014), implying that nitrification and biological recycling of organic N in the water column and/or sediment porewaters, are the major sources of N to the water column.…”

“…This is shorter than the ~4 year depletion time modeled for oxygen in the SLW water column. It is clear that if nitrification is an important process in SLW, as geochemical, isotopic, and molecular data suggest (Christner et al, 2014; Achberger, 2016; Achberger et al, 2016), then unaccounted for sources (such as overlying ice) and the internal cycling of N also play important roles.…”

“…The scenarios focused on redox couples that were geochemically plausible, as well as those indicated by potential metabolisms derived from microbial community data, which included aerobic organisms in addition to facultative aerobes, and strict anaerobes (Christner et al, 2014; Purcell et al, 2014; Achberger et al, 2016). Scenario A used the observed physicochemical measurements from the SLW water column: temperature, pH, redox (pE), and concentrations of acetate, formate, DIC, O 2 (aq), CH 4 (aq), SO${}_4^{2-}$, NO${}_3^{-}$, NO${}_2^{-}$, NH${}_4^{+}$, Cl − and F − , Total dissolved Fe, Ca, Mg, Na, K, and P (Table S1).…”

“…Outflow from SLW flows beneath the Whillans Ice Stream and drains into the ocean beneath the Ross Ice Shelf, and the lake is refilled by periodic inflow from upstream (Siegfried et al, 2014); the ice surface rises and falls with the lake level (Fricker et al, 2007). Microbiological analyses of water and sediment samples from SLW revealed the presence of active microbial communities and evidence for an ecosystem driven by chemosynthetic production (Christner et al, 2014; Mikucki et al, 2015; Achberger et al, 2016) and by organic matter and nutrients contained in relict marine sediments beneath the West Antarctic Ice Sheet (Scherer et al, 1998; Wadham et al, 2012; Michaud et al, 2016). This evidence, coupled with the connectivity of SLW to the hydrological network of this region (Fricker et al, 2007), suggests microbial life is widespread beneath the ice sheet.…”