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.

Keywords: Antarctica; biogeochemical cycling; chemosynthetic ecosystem; subglacial lake; subsurface microbiology.

FIGURE 1

Non-metric multidimensional scaling plot based on OTUs classified from the 16S rRNA and rRNA gene sequences obtained from samples of the drilling water, SLW water column, sediments, and experimental controls. Circles represent rDNA-based sample libraries and triangles represent rRNA-based libraries. Lake water is denoted by black symbols, sediments are gray, and controls are white. Inset contains the 3.0, 0.8, and 0.2 μm samples from each water cast outlined with a black box.

FIGURE 2

The most abundant OTUs in the bulk SLW water column and sediments (>1%). All of the OTUs are listed with their nearest taxonomic neighbor and total relative abundance in the overall SLW community. Brackets 1, 2, and 3 represent putative taxa that are involved in sulfur/iron, nitrogen, and methane cycling, respectively.

FIGURE 3

The ratio of 16S rRNA to rDNA sequences obtained from the SLW molecular data. (A) The relative abundance of individual OTUs in rRNA versus the rDNA sequence data. The black line denotes those OTUs in the top 1% (ratio of 5.8) while those above the hashed line represent outliers (ratio >10.7). (B) The rank abundance of OTUs (gray), based on 16S rDNA data, and their rRNA:rDNA ratios denoted as black dots. The horizontal black line denotes an rRNA:rDNA ratio of 1. (C) List of the top 1% of OTUs with rRNA:rDNA ratios ≥5.8, identified by their nearest taxonomic neighbor. Bracket designations are the same as Figure 2.

FIGURE 4

Heat plot showing the occurrence of various putative metabolic functions in SLW inferred from 16S rRNA phylogenetic associations and sequence abundances of important community members.