Metagenomic insights into strategies of carbon conservation and unusual sulfur biogeochemistry in a hypersaline Antarctic lake

Abstract

Organic Lake is a shallow, marine-derived hypersaline lake in the Vestfold Hills, Antarctica that has the highest reported concentration of dimethylsulfide (DMS) in a natural body of water. To determine the composition and functional potential of the microbial community and learn about the unusual sulfur chemistry in Organic Lake, shotgun metagenomics was performed on size-fractionated samples collected along a depth profile. Eucaryal phytoflagellates were the main photosynthetic organisms. Bacteria were dominated by the globally distributed heterotrophic taxa Marinobacter, Roseovarius and Psychroflexus. The dominance of heterotrophic degradation, coupled with low fixation potential, indicates possible net carbon loss. However, abundant marker genes for aerobic anoxygenic phototrophy, sulfur oxidation, rhodopsins and CO oxidation were also linked to the dominant heterotrophic bacteria, and indicate the use of photo-and lithoheterotrophy as mechanisms for conserving organic carbon. Similarly, a high genetic potential for the recycling of nitrogen compounds likely functions to retain fixed nitrogen in the lake. Dimethylsulfoniopropionate (DMSP) lyase genes were abundant, indicating that DMSP is a significant carbon and energy source. Unlike marine environments, DMSP demethylases were less abundant, indicating that DMSP cleavage is the likely source of high DMS concentration. DMSP cleavage, carbon mixotrophy (photoheterotrophy and lithoheterotrophy) and nitrogen remineralization by dominant Organic Lake bacteria are potentially important adaptations to nutrient constraints. In particular, carbon mixotrophy relieves the extent of carbon oxidation for energy production, allowing more carbon to be used for biosynthetic processes. The study sheds light on how the microbial community has adapted to this unique Antarctic lake environment.

Contrasting taxonomic stratification of microbial communities in two hypersaline meromictic lakes

“…Ammonium reached the highest concentrations in the deep anoxic layers of the lakes, indicating a higher rate of mineralization than assimilation, coupled with a higher stability in the acidic pH range. The depth profiles of ammonium concentration were comparable for both Ursu and Fara Fund lakes, and similar to the ones described in other stratified lakes (Auguet et al, 2012;La Cono et al, 2013;Yau et al, 2013). The vertical profiles of nutrients (sulfate, sulfide, nitrite, nitrate and phosphate) were found to be a result of sedimentation, biogeochemical cycling or conservative mixing (Pasche et al, 2009), and were also comparable with those found in other studied lakes (Lepère et al, 2010;La Cono et al, 2013;Marteinsson et al, 2013).…”

“…The relative abundance of Archaea in the 0.5 (~2%) and 2 m (1.2%) depth assemblages was minor, and could be attributed to the lower salinity levels found at these depths (that is,~70 g l − 1 ). Similar findings were reported in other saline lakes (Yau et al, 2013;Baricz et al, 2014) or shallow ponds (Ghai et al, 2011), and are supported by the fact that most haloarchaeal species lyse at salt concentrations of o100 g l − 1 (Andrei et al, 2012). As the salinity increased over 240 g l − 1 (at 3.5 m depth) the proportion of the Archaea in the communities was higher, ranging between~20% (at 3.5 m depth) and~40% (at 9 m depth), but nonetheless lower than the bacterial one.…”

“…Furthermore, these findings are corroborated with other studies that detected disparate communities in the mixolimnion versus monimolimnion of other meromictic lakes (Barberán and Casamayor, 2011;Lauro et al, 2011;Comeau et al, 2012). In addition, the overall organization of the prokaryotic communities was found to be typical for stratified lakes with regard to depth distribution of photosynthetic and redox conditions (Lauro et al, 2011;Comeau et al, 2012;Edberg et al, 2012;Lentini et al, 2012;Yau et al, 2013).…”

Relationships between protein-encoding gene abundance and corresponding process are commonly assumed yet rarely observed

“…For example, reactant pools may frequently be assimilated, leached or re-routed through other biochemical pathways independent of the pathway that corresponds to the gene of interest. The advent of relatively new technologies like gene microarrays (He et al, 2007) and metagenomics (Tyson et al, 2004;Mackelprang et al, 2011;Fierer et al, 2012;Yau et al, 2013) has allowed researchers to rapidly assess more genes compared with qPCR techniques. However, the use of enticing new technologies for assessing gene abundance is also susceptible to many of the same biases that obscure the links between molecular information and biogeochemical processes illustrated by the meta-analysis presented here.…”

“…To evaluate these linkages, many studies use molecular techniques, including quantitative PCR (qPCR), reversetranscription qPCR (Liu et al, 2010;Shannon et al, 2011), microarrays (Taroncher-Oldenburg et al, 2003;Kang et al, 2013) and, most recently, metagenomics (Tyson et al, 2004;Mackelprang et al, 2011;Fierer et al, 2012;Yau et al, 2013). These techniques measure the relative abundances of nucleic acids encoding proteins that catalyze biogeochemical reactions, which we refer to as protein-encoding genes and transcripts (or henceforth as gene or transcript).…”