Sediment Metagenomes as Time Capsules of Lake Microbiomes

ABSTRACT The reconstruction of ecological time series from lake sediment archives can retrace the environmental impact of human activities. Molecular genetic approaches in paleolimnology have provided unprecedented access to DNA time series, which record evidence of the microbial ecologies that underlaid historical lake ecosystems. Such studies often rely on single-gene surveys, and consequently, the full diversity of preserved microorganisms remains unexplored. In this study, we probed the diversity archived in contemporary and preindustrial sediments by comparative shotgun metagenomic analysis of surface water and sediment samples from three eastern Canadian lakes. In a strategy that was aimed at disentangling historical DNA from the indigenous sediment background, microbial preservation signals were captured by mapping sequence similarities between sediment metagenome reads and reference surface water metagenome assemblies. We detected preserved Cyanobacteria, diverse bacterioplankton, microeukaryotes, and viruses in sediment metagenomes. Among the preserved microorganisms were important groups never before reported in paleolimnological reconstructions, including bacteriophages (Caudovirales) and ubiquitous freshwater Betaproteobacteria (Polynucleobacter and Limnohabitans). In contrast, ultramicroscopic Actinobacteria (“Candidatus Nanopelagicales”) and Alphaproteobacteria (Pelagibacterales) were apparently not well preserved in sediment metagenomes even though they were numerically dominant in surface water metagenomes. Overall, our study explored a novel application of whole-metagenome shotgun sequencing for discovering the DNA remains of a broad diversity of microorganisms preserved in lake sediments. The recovery of diverse microbial time series supports the taxonomic expansion of microbiome reconstructions and the development of novel microbial paleoindicators. IMPORTANCE Lakes are critical freshwater resources under mounting pressure from climate change and other anthropogenic stressors. The reconstruction of ecological time series from sediment archives with paleolimnological techniques has been shown to be an effective means of understanding how humans are modifying lake ecosystems over extended timescales. In this study, we combined shotgun DNA sequencing with a novel comparative analysis of surface water and sediment metagenomes to expose the diversity of microorganisms preserved in lake sediments. The detection of DNA from a broad diversity of preserved microbes serves to more fully reconstruct historical microbiomes and describe preimpact lake conditions