Genome-resolved metagenomics extends the environmental distribution of the Verrucomicrobia phylum to the deep terrestrial subsurface

Bacteria of the phylum Verrucomicrobia are prevalent and are particularly common in soil and freshwater environments. Their cosmopolitan distribution
and reported capacity for polysaccharide degradation suggests members of Verrucomicrobia are important contributors to carbon cycling across Earth’s ecosystems. Despite their prevalence, the Verrucomicrobia are underrepresented in isolate collections and genome databases; consequently, their ecophysiological roles may not be
fully realized. Here, we expand genomic sampling of the Verrucomicrobia phylum by
describing a novel genus, “Candidatus Marcellius,” belonging to the order Opitutales.
“Ca. Marcellius” was recovered from a shale-derived produced fluid metagenome
collected 313 days after hydraulic fracturing, the deepest environment from which a
member of the Verrucomicrobia has been recovered to date. We uncover genomic
attributes that may explain the capacity of this organism to inhabit a shale gas well,
including the potential for utilization of organic polymers common in hydraulic fracturing fluids, nitrogen fixation, adaptation to high salinities, and adaptive immunity
via CRISPR-Cas. To illuminate the phylogenetic and environmental distribution of
these metabolic and adaptive traits across the Verrucomicrobia phylum, we performed a comparative genomic analysis of 31 publicly available, nearly complete
Verrucomicrobia genomes. Our genomic findings extend the environmental distribution of the Verrucomicrobia 2.3 kilometers into the terrestrial subsurface. Moreover,
we reveal traits widely encoded across members of the Verrucomicrobia, including
the capacity to degrade hemicellulose and to adapt to physical and biological environmental perturbations, thereby contributing to the expansive habitat range reported for this phylum.