Contrasting taxonomic stratification of microbial communities in two hypersaline meromictic lakes

Abstract

Hypersaline meromictic lakes are extreme environments in which water stratification is associated with powerful physicochemical gradients and high salt concentrations. Furthermore, their physical stability coupled with vertical water column partitioning makes them important research model systems in microbial niche differentiation and biogeochemical cycling. Here, we compare the prokaryotic assemblages from Ursu and Fara Fund hypersaline meromictic lakes (Transylvanian Basin, Romania) in relation to their limnological factors and infer their role in elemental cycling by matching taxa to known taxon-specific biogeochemical functions. To assess the composition and structure of prokaryotic communities and the environmental factors that structure them, deep-coverage small subunit (SSU) ribosomal RNA (rDNA) amplicon sequencing, community domain-specific quantitative PCR and physicochemical analyses were performed on samples collected along depth profiles. The analyses showed that the lakes harbored multiple and diverse prokaryotic communities whose distribution mirrored the water stratification patterns. Ursu Lake was found to be dominated by Bacteria and to have a greater prokaryotic diversity than Fara Fund Lake that harbored an increased cell density and was populated mostly by Archaea within oxic strata. In spite of their contrasting diversity, the microbial populations indigenous to each lake pointed to similar physiological functions within carbon degradation and sulfate reduction. Furthermore, the taxonomy results coupled with methane detection and its stable C isotope composition indicated the presence of a yet-undescribed methanogenic group in the lakes' hypersaline monimolimnion. In addition, ultrasmall uncultivated archaeal lineages were detected in the chemocline of Fara Fund Lake, where the recently proposed Nanohaloarchaeota phylum was found to thrive.

Figure 1

Ursu Lake and Fara Fund Lake sampling sites. (a) Map showing the location of the lakes within Transylvanian Basin (Romania). The symbol size is not proportional with the sizes of the lakes. (b) Topo-bathymetric profile of Ursu and (c) Fara Fund lakes' basins. The circles indicate the sampling points.

Figure 2

Vertical distribution of physicochemical parameters (salinity, dissolved oxygen, pH, temperature and reduction potential) measured in situ along the water columns of Ursu (a) and Fara Fund (b) lakes during October 2013. The three water layers resulted from physicochemical partitioning were separated by dashed lines. Sampling points for DNA and chemical analyses are indicated by circles. Ch, chemocline; DO, dissolved oxygen; Mi, mixolimnion; Mo, monimolimnion; ORP, oxidoreduction potential.

Figure 3

Prokaryotic cell numbers per ml as estimated by quantitative PCR (black and gray columns) and DAPI counts (white columns) for the Ursu (a) and Fara Fund (b) lakes. The sampling depths from each lake are represented on the abscissa. The columns represent means, and the error bars represent their s.d. values. TC, total cell counts.

Figure 4

Class-level taxonomic profiles of the prokaryotic communities using 16S rRNA gene sequences.