Microbial sulfur transformations in sediments from Subglacial Lake Whillans

Abstract

Diverse microbial assemblages inhabit subglacial aquatic environments. While few of these environments have been sampled, data reveal that subglacial organisms gain energy for growth from reduced minerals containing nitrogen, iron, and sulfur. Here we investigate the role of microbially mediated sulfur transformations in sediments from Subglacial Lake Whillans (SLW), Antarctica, by examining key genes involved in dissimilatory sulfur oxidation and reduction. The presence of sulfur transformation genes throughout the top 34 cm of SLW sediments changes with depth. SLW surficial sediments were dominated by genes related to known sulfur-oxidizing chemoautotrophs. Sequences encoding the adenosine-5'-phosphosulfate (APS) reductase gene, involved in both dissimilatory sulfate reduction and sulfur oxidation, were present in all samples and clustered into 16 distinct operational taxonomic units. The majority of APS reductase sequences (74%) clustered with known sulfur oxidizers including those within the "Sideroxydans" and Thiobacillus genera. Reverse-acting dissimilatory sulfite reductase (rDSR) and 16S rRNA gene sequences further support dominance of "Sideroxydans" and Thiobacillus phylotypes in the top 2 cm of SLW sediments. The SLW microbial community has the genetic potential for sulfate reduction which is supported by experimentally measured low rates (1.4 pmol cm(-3)d(-1)) of biologically mediated sulfate reduction and the presence of APS reductase and DSR gene sequences related to Desulfobacteraceae and Desulfotomaculum. Our results also infer the presence of sulfur oxidation, which can be a significant energetic pathway for chemosynthetic biosynthesis in SLW sediments. The water in SLW ultimately flows into the Ross Sea where intermediates from subglacial sulfur transformations can influence the flux of solutes to the Southern Ocean.

Keywords: Antarctic subglacial aquatic environments; chemosynthesis; geomicrobiology; sulfate reduction; sulfur oxidation.

FIGURE 1

Location of Subglacial Lake Whillans (SLW) and schematic of the Whillans Ice Stream (WIS). (A) Satellite image of the Siple Coast with SLW labeled (after Fricker and Scambos, 2009); the blue line indicates the proposed subglacial water flow path toward the grounding line (Carter and Fricker, 2012). Background satellite image from MODIS Mosaic of Antarctica (Haran et al., 2005). (B) Cross-sectional cartoon of the WIS indicating the borehole created through 801 m of ice. Sediment cores were collected through ∼2.2 m of water. Black arrows indicate the direction of ice movement; green arrow indicates predicted dispersal of subglacial water into the marine cavity beneath the Ross Ice Shelf. Cross-sectional cartoon of the WIS adapted from Fricker et al. (2011).

FIGURE 2

Sulfate reduction rates (SRR) in SLW sediment samples. (A) SRR for killed controls was subtracted from each sample replicate. Black bars represent sediment incubations with no carbon addition; Gray bars represent sediment incubations with 50 mM formate addition (± SD of triplicates). (B) Image of SLW sediment core MC-2B.

FIGURE 3

Q-PCR quantification of bacterial and archaeal 16S rRNA and aprA gene copies. Total bacterial (black bars) and archaeal (white bars) 16S rRNA and aprA (gray bars) gene copies from all sediment depths from SLW MC-2B and MC-3C (± SD of technical replicates).

FIGURE 4

Phylogenetic tree of SLW sediments aprA OTUs. Neighbor-joining reconstruction of 16 aprA sequences from SLW sediments and the most identical aprA-containing cultured organisms and environmental sequences. Values at nodes indicate bootstrap support from 1000 replicates. One representative aprA sequence from each of the 16 operational taxonomic units (OTUs) was randomly selected and included. SLW aprA OTUs are in bold and the total number of sequences obtained within that OTU are in parentheses. Lineage designations on the right are from Meyer and Kuever (2007c). Pyrobaculum aerophilum was used as an outgroup reference. Scale bar indicates the branch length corresponding to 0.1 substitutions per amino acid position.

FIGURE 5

Distribution of aprA sequences from SLW sediment cores MC-2B and MC-3C among putative sulfur-cycling lineages. Sulfur cycling lineages as functional categories defined by Meyer and Kuever (2007a). Blue represents sulfur-oxidizing prokaryote lineages I and II, black represents sulfate-reducing lineages, and gray represents sequences of uncertain function. Percentages represent the number of sequences within the designated lineage out of the total aprA sequences obtained from each depth. The total number of sequences obtained for each depth are listed in Table 3.

FIGURE 6

Rarefaction curves of aprA in SLW sediments. (A) Individual depths from sediment cores MC-2B and MC-3C. (B) Total aprA sequences from all depths and cores.