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.
Highlights
Freshwater lakes are biologically complex ecosystems that contribute several economic and societal services and provide habitats for a wide range of micro- and macro-organisms [1]
A significant increase in total suspended solids throughout the water column, with turbidity values increasing from 0.7 ±0.1–1.5±0.64 NTU in Microbial lake community prior to stratification/eutrophication (March) to 9.8±3.5–13.5±4.75 NTU in June (Wilcoxon ranked sum test coefficient (W) = 2, p-value = 2.2x10-16)
The transition from an oxygenated, completely mixed, water column in March with dissolved oxygen concentrations ranging from 102.9±5.28%–122.4±6.18% throughout the water column (Fig 2E) into a stratified water column in June, where the dissolved O2 levels decreased with depth from highly oxic (90.1±37.2%–99.9±4.1%) in the epilimnion to moderately hypoxic (27.2 ±6.3%–29.4±4.8%) in the metalimnion (6–24 m deep) to highly hypoxic (3.48±1.3%–6.25 ±0.78%) in the hypolimnion (24–28 m)
Summary
Freshwater lakes are biologically complex ecosystems that contribute several economic and societal services and provide habitats for a wide range of micro- and macro-organisms [1]. Microbial community characterization in freshwater lakes has been the subject of a wide range of studies using culturing approaches [2,3,4,5,6,7,8,9,10,11,12,13,14,15,16,17], culture-independent diversity surveys [2, 7, 8, 13, 14, 18,19,20,21,22,23,24,25,26,27,28,29], and–omics based investigations [8, 30,31,32,33,34,35,36,37,38,39,40,41,42,43]. Autochthonous deposition is often associated with the development of algal blooms, of which frequency and intensity are expected to increase in the future due to global patterns of increased nitrogen and phosphorous deposition from agricultural runoff and the expected rise in mean atmospheric temperature associated with global climate change [50]
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