Shifts among Eukaryota, Bacteria, and Archaea define the vertical organization of a lake sediment

Abstract

BackgroundLake sediments harbor diverse microbial communities that cycle carbon and nutrients while being constantly colonized and potentially buried by organic matter sinking from the water column. The interaction of activity and burial remained largely unexplored in aquatic sediments. We aimed to relate taxonomic composition to sediment biogeochemical parameters, test whether community turnover with depth resulted from taxonomic replacement or from richness effects, and to provide a basic model for the vertical community structure in sediments.MethodsWe analyzed four replicate sediment cores taken from 30-m depth in oligo-mesotrophic Lake Stechlin in northern Germany. Each 30-cm core spanned ca. 170 years of sediment accumulation according to 137Cs dating and was sectioned into layers 1–4 cm thick. We examined a full suite of biogeochemical parameters and used DNA metabarcoding to examine community composition of microbial Archaea, Bacteria, and Eukaryota.ResultsCommunity β-diversity indicated nearly complete turnover within the uppermost 30 cm. We observed a pronounced shift from Eukaryota- and Bacteria-dominated upper layers (<5 cm) to Bacteria-dominated intermediate layers (5–14 cm) and to deep layers (>14 cm) dominated by enigmatic Archaea that typically occur in deep-sea sediments. Taxonomic replacement was the prevalent mechanism in structuring the community composition and was linked to parameters indicative of microbial activity (e.g., CO2 and CH4 concentration, bacterial protein production). Richness loss played a lesser role but was linked to conservative parameters (e.g., C, N, P) indicative of past conditions.ConclusionsBy including all three domains, we were able to directly link the exponential decay of eukaryotes with the active sediment microbial community. The dominance of Archaea in deeper layers confirms earlier findings from marine systems and establishes freshwater sediments as a potential low-energy environment, similar to deep sea sediments. We propose a general model of sediment structure and function based on microbial characteristics and burial processes. An upper “replacement horizon” is dominated by rapid taxonomic turnover with depth, high microbial activity, and biotic interactions. A lower “depauperate horizon” is characterized by low taxonomic richness, more stable “low-energy” conditions, and a dominance of enigmatic Archaea.Electronic supplementary materialThe online version of this article (doi:10.1186/s40168-017-0255-9) contains supplementary material, which is available to authorized users.

Archaea in boreal Swedish lakes are diverse, dominated by Woesearchaeota and follow deterministic community assembly

“…The detected Bathyarchaeia were highly diverse, represented by more than 7761 ASVs that were collectively abundant across the lakes. Bathyarchaeia are among the most abundant organisms reported in marine and freshwater sediments globally (Biddle et al, 2006;Lloyd et al, 2013;Fillol et al, 2015;Lazar et al, 2015, Wurzbacher et al, 2017. Verstraetearchaeia, occurring as a minor archaeal class in our dataset, appear to be capable of fermentation utilizing sugars as a carbon source and generating acetyl-CoA via the Embden-Meyerhof-Parnas pathway and pyruvate-ferredoxin oxidoreductase (Vanwonterghem A B Fig 5. Taxonomic composition of the archaeal methanogenic genera (following SILVA 132 taxonomy) (A) and their number of reads (relative abundance in percentage) in relation to environmental variables as inferred by redundancy analysis (B) with the 15 most abundant genera represented.…”

Weak Influence of Paleoenvironmental Conditions on the Subsurface Biosphere of Lake Ohrid over the Last 515 ka

“…However, these studies are still scarce, and more analyses from other lakes are required to validate and potentially generalize the hypothesis of retained sensitivity of the lake subsurface biosphere to paleoclimatic conditions. Indeed, models and studies from other lakes, generally in shallower sediments, have emphasized the strong dominance of taxa adapted to low energy environments, similar to those found in ocean sediments [32]. A second hypothesis is therefore that eventually conditions become too exclusive (i.e., poor in nutrients and in labile organic matter) and result in the takeover of energy conservative slow-growing organisms such as Bathyarchaeota, Atribacteria, Dehalococcoidia or other poorly understood microorganisms likely better adapted to the specificity of deep sedimentary environments [32,33].…”

“…Their metabolic abilities cannot be easily constrained using our method, but their occurrence has often been acknowledged in the deep subsurface [33]. Potential association with sugar fermentation coupled with Mn and Fe reduction was hypothesized for Bacteroidetes members [32] but is not expressed in the METAGENassist simulation (Figure 8). However, they likely have energy conservative metabolisms allowing them to remain present in extreme deep lacustrine sediments [26].…”

“…The two other most significant phyla observed in Ohrid sediments belong to the archaeal candidate division Bathyarchaeia and the bacterial division Atribacteria. These are both common phyla in sedimentary environments at depth [54], and particularly in the marine realm (e.g., [32]), where their occurrence has been associated with strong adaptations to low energy environments and varied fermentative abilities. Atribacteria have been suggested to perform primary fermentation of carbohydrates and secondary fermentation of organic acids (propionate among others), leading to the production of H 2 [33,55].…”

Bacteria‐sediment associations in an alpine, freshwater environment and their effects on particle size, density and settling velocity

“…Alpine, glacial meltwater at the source differs in temperature, if not nutrient concentration and availability, from the increasingly distal and/or lowland sites into which that meltwater flows. Glaciers support microbially‐dominated food webs that thrive in the presence of liquid water and sediment (Hodson et al ) and bacteria are widely reported from glacier‐fed environments, including fjords (Jankowska ; Syvitski et al ), subglacial meltwater (Sharp et al ), glacier‐fed lakes (Mindl et al ), supraglacial lakes (Liu et al ), cryoconite holes (Hodson et al ), lake sediment cores (Wurzbacher et al ) and channel beds (Battin et al ; Fegel et al ). Alpine glaciers are sensitive to hydroclimatic conditions (Hodder et al ), and seasonal shifts in the availability of liquid water and suspended sediment, especially during snow‐ and ice‐melt and the associated release of meltwater, are likely linked with corresponding shifts in bacterial abundance.…”