A metagenomic view of novel microbial and metabolic diversity found within the deep terrestrial biosphere at DeMMO: A microbial observatory in South Dakota,USA

The deep terrestrial subsurface is a large and diverse microbial habitat and vast repository of biomass. However, in relation to its size and physical heterogeneity we have limited understanding of taxonomic and metabolic diversity in this realm. Here we present a detailed metagenomic analysis of samples from the Deep Mine Microbial Observatory (DeMMO) spanning depths from the surface to 1.5 km into the crust. From eight geochemically and spatially distinct fluid samples we reconstructed ~600 partial to near-complete metagenome-assembled genomes (MAGs), representing 50 distinct phyla and including 18 candidate phyla. These novel clades include members of the candidate phyla radiation, two new MAGs from OLB16, a phylum originally identified in DeMMO fluids and for which only one other MAG is currently available, and new MAGs from the Eisenbacteria, Omnitrophota, and Edwardsbacteria. We find that microbes spanning this expansive phylogenetic diversity and physical subsurface space gain a competitive edge by maintaining a wide variety of functional pathways, are often capable of numerous dissimilatory energy metabolisms and poised to take advantage of nutrients as they become available in isolated fracture fluids. Our results support and expand on emerging themes of tight nutrient cycling and genomic plasticity in deep subsurface biosphere taxa.