Spatiotemporal analysis of microbial community dynamics during seasonal stratification events in a freshwater lake (Grand Lake, OK, USA)

Abstract

Many freshwater lakes undergo seasonal stratification, where the formation of phototrophic blooms in the epilimnion and subsequent sedimentation induces hypoxia/anoxia in the thermocline and hypolimnion. This autochthonously produced biomass represents a major seasonal organic input that impacts the entire ecosystem. While the limnological aspects of this process are fairly well documented, relatively little is known regarding the microbial community response to such events, especially in the deeper anoxic layers of the water column. Here, we conducted a spatiotemporal survey of the particle-associated and free-living microbial communities in a warm monomictic freshwater reservoir (Grand Lake O’ the Cherokees) in northeastern Oklahoma, USA. Pre-stratification samples (March) harbored a homogeneous community throughout the oxygenated water column dominated by typical oligotrophic aquatic lineages (acl clade within Actinobacteria, and Flavobacterium within the Bacteroidetes). The onset of phototrophic blooming in June induced the progression of this baseline community into two distinct trajectories. Within the oxic epilimnion, samples were characterized by the propagation of phototrophic (Prochlorococcus), and heterotrophic (Planctomycetes, Verrucomicrobia, and Beta-Proteobacteria) lineages. Within the oxygen-deficient thermocline and hypolimnion, the sedimentation of surface biomass induced the development of a highly diverse community, with the enrichment of Chloroflexi, “Latescibacteria”, Armatimonadetes, and Delta-Proteobacteria in the particle-associated fraction, and Gemmatimonadetes and “Omnitrophica” in the free-living fraction. Our work documents the development of multiple spatially and temporally distinct niches during lake stratification, and supports the enrichment of multiple yet-uncultured and poorly characterized lineages in the lake’s deeper oxygen-deficient layers, an ecologically relevant microbial niche that is often overlooked in lakes diversity surveys.

Temporal variability of bacterioplankton is habitat driven

“…() also found that DO was important in deep layers but not at the surface. Surprisingly, in the hypolimnion, the phylum Actinobacteria was among the most abundant; this phylum is usually tied to epilimnetic sites (Barberán & Casamayor, ; Morrison et al., ) and less so to the hypolimnion (Newton et al., and references therein). We suggest that the lack of anoxia (DO ≥ 19%), among other factors, can explain the strong presence of Actinobacteria in this deep habitat.…”

“…Thus, variations in bacterial community (BC) composition should reflect the effects of stable, lake‐specific characteristics as well as the effects of factors that fluctuate according to seasonal cycles (Yannarell et al., ). Most studies are short term (<1 year) with BC composition showing a distinct seasonal pattern (e.g., Eiler, Heinrich, & Bertilsson, ; Morrison et al., ; Woodhouse et al., ). However in multiyear studies, BC composition displays a huge temporal variability showing repetitive seasonal patterns (Kent et al., ; Nelson, ; Shade et al., ) with high bacterial abundance in summer and low abundance in winter (Nelson, ; Rösel, Allgaier, & Grossart, ), high interannual variability (Linz et al., ), absence of any seasonality (Berdjeb et al., ; Jones, Cadkin, Newton, & McMahon, ) or shifts indicating ecosystem transitions depending on the year under scrutiny (Thaler, Vincent, Lionard, Hamilton, & Lovejoy, ).…”

Parallel and non-parallel changes of the gut microbiota during trophic diversification in repeated young adaptive radiations of sympatric cichlid fish

“…2). Thus, caution should be taken when drawing conclusions about the extent to which the gut microbiota of Midas cichlids is derived from bacteria present in the water based on our data, particularly since microbial communities of lakes are known to show temporal variation [e.g., 55,56,57]. Future studies need to systematically investigate the temporal dynamics of microbial communities for the Nicaraguan lakes in more detail.…”

Geographical patterns of denitrifying bacterial communities associated with different urban lakes

“…Firmicutes can be frequently found in other environmental ecosystems, which can survive in extreme conditions. 7,12,13,31 The largest proportion of the OTUs in PZ with 28% was unclassied. At family level, the majority of sequence reads were affiliated with known members of Rhodocyclaceae.…”

“…6 To date, most studies have focused on exploring microbial community diversity in drinking water reservoirs, 7,8 polluted rivers, 9,10 drinking water pipes, 11 and entropic lakes. 12,13 In lake ecosystems, it has long been of signicant interest to study the relationships between water quality and sediment bacterial, 13 archaeal, 14 and fungal 15 communities. Numerous water physical-chemical factors, such as the pH, total nitrogen (TN) and organic carbon levels, have been evaluated to understand their effect on the distribution of the microbial community.…”