Sedimentary DNA records long-term changes in a lake bacterial community in response to varying nutrient availability

Microbial communities play important roles in lake ecosystems and are sensitive to environmental change. However, our understanding of their responses to long-term change such as eutrophication is limited, as long-term lake monitoring is rare, and traditional paleolimnological techniques (pigments and microfossils) are restricted to a low taxonomic resolution, or organisms with well-preserved structures. Sedimentary DNA (sedDNA) is a promising technique to reconstruct past microbial communities in sediments, but taphonomic processes and the ability of sedDNA to record bacterial pelagic history accurately are largely unknown. Here, we sequenced the 16S rRNA gene in triplicate sediment cores from Esthwaite Water (English Lake District) which has concurrent long-term monitoring and observational data. The sediment record spanned 113 years and included an episode of increased nutrient availability from the 1970s, followed by a more recent decline. Trends in bacterial community composition were broadly similar among the three sediment cores. Cyanobacterial richness in the sediment cores correlated significantly with that of cyanobacteria in a 65-year microscopy-based monitoring record, and some known pelagic bacterial taxa were detected in the sediment. sedDNA revealed distinct shifts in community composition in response to changing lake physicochemical conditions. The relative abundance of cyanobacteria closely reflected nutrient enrichment, and Proteobacteria, Bacteroidetes, and Verrucomicrobia were relatively more abundant in recent sediments, while Chloroflexi, Firmicutes, Acidobacteria, Nitrospirae, Spirochaetes, and Planctomycetes declined in more recent sediments. Following lake restoration efforts to reduce nutrient enrichment, the relative abundance of cyanobacteria returned to pre-1970 levels, but the bacterial community did not fully recover from the period of intense eutrophication within the time scale of our study. These results suggest that sedDNA is a valuable approach to reconstruct lake microbial community composition over the 100-year time scale studied, but an improved understanding of DNA deposition and degradation is required to further the application of sedDNA in paleolimnology.