Paleometagenomics reveals environmental microbiome response to vegetation changes in northern Siberia over the millennia

Abstract

The study of environmental ancient DNA provides us with the unique opportunity to link environmental with ecosystem change over a millennial timescale. Paleorecords such as lake sediments contain genetic pools of past living organisms that are a valuable source of information to reconstruct how ecosystems were and how they changed in response to climate in the past. Here, we report on paleometagenomics of a sedimentary record in northern Siberia covering the past 6700 years. We integrated taxonomic with functional gene analysis, which enabled to shed light not only on community compositions but also on eco-physiological adaptations and ecosystem functioning. We reconstructed the presence of an open boreal forest 6700 years ago that over time was gradually replaced by tundra. This vegetation change had major consequences on the environmental microbiome, primarily enriching bacterial and archaeal ammonia oxidizers (e.g., Nitrospira, Nitrosopumilus, and Ca. Nitrosocosmicus) in the tundra ecosystem. We identified a core microbiome conserved through time and largely consisting of heterotrophic bacteria of the Bacteroidetes phylum (e.g., Mucilaginibacter) harboring numerous functional genes for degradation of plant-biomass and abiotic and biotic stress resistance. Archaea were also a key functional guild, involved in nitrogen and carbon cycling, not only methanogenesis but possibly also degradation of plant material via enzymes such as cellulases and amylases. Overall, the paleo-perspective offered by our study can have a profound impact on modern climate change biology, by helping to explain and predict the ecological interplay among multiple ecosystem levels based on past experiences.