DeepH: Horizontal evolution of uncultivated archaea in the deep biosphere

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The deep subsurface houses approximately 70% of Earth’s Prokaryotes, yet there is little information on major modes of prokaryotic evolution in its ecosystems that are mainly characterized by the absence of sunlight, little to no oxygen availability, and little amounts of nutrients. Recent investigations demonstrated that some genomes from different subsurface sites can be of extremely high similarity, suggesting low evolutionary processes of deep subsurface microbes. However, only conserved core genes were used for these analyses. At the same time, previous attempts at resolving genomes from deep subsurface archaea showed that transposon propagation can result in diversification of strains. Consequently, a conclusive analysis on the extent and dynamics of genome evolution in the continental subsurface is missing. In the project DeepH, we propose to tackle the question of how transposable elements (TEs) impact archaeal genome evolution and genome plasticity in the continental subsurface by performing long-read genome-resolved metagenomics, coupled to proximity-ligation (Hi-C) metagenomics and methylation base calling to reconstruct (near) complete genomes of Candidatus Altiarchaea from various subsurface ecosystems across the globe. These archaea have been selected as model organisms since they can be abundant in their ecosystem (up to ~70% in relative abundance), show a very strict biogeography, and have many genes of bacterial origin besides their conserved core genomes as we recently demonstrated. After resolving complete genomes (existing genomes are extremely fragmented), we will investigate the mode of gene transfer by focusing on TEs in the host genome underpinning their origin (some are carried by viruses) and investigating TE distribution across sampling sites (from US over Europe to Japan). We will also investigate genome rearrangements, transposition, and the general genome architecture of these microbes. Finally, presence and diversity of TEs in Ca. Altiarchaea strains will be detected at single cell level using single molecule fluorescence microscopy. We anticipate the detection of bacterial cargo genes on TEs as well as site-specific TEs that drive the short-term evolution of these archaea without spoilage of the core genome. Overall, we propose that the DeepH project will substantially contribute to a better understanding of genome evolution and genome (re)organization of archaea, particularly Ca. Altiarchaea, in the deep biosphere and reveal a major mode of evolution in these ecosystems.