The hydrocarbon-enriched environments, such as oil reservoirs and oil sands tailings ponds, contain a broad diversity of uncultured microorganisms. Despite being one of the few prokaryotic lineages that is consistently detected in both production water from oil reservoirs and stable hydrocarbon-degrading enrichment cultures originated from oil reservoirs, the physiological and ecological roles of candidate phylum “Atribacteria” (OP9/JS1) are not known in deep subsurface environments. Here, we report the expanded metabolic capabilities of Atribacteria as inferred from genomic reconstructions. Seventeen newly assembled medium-to-high-quality metagenomic assembly genomes (MAGs) were obtained either from co-assembly of two metagenomes from an Alaska North Slope oil reservoir or from previous studies of metagenomes coming from different environments. These MAGs comprise three currently known genus-level lineages and four novel genus-level groups of OP9 and JS1, which expands the genomic coverage of the major lineages within the candidate phylum Atribacteria. Genes involved in anaerobic hydrocarbon degradation were found in seven MAGs associated with hydrocarbon-enriched environments, and suggest that some Atribacteria could ferment short-chain n-alkanes into fatty acid while conserving energy. This study expands predicted metabolic capabilities of Atribacteria (JS1) and suggests that they are mediating a key role in subsurface carbon cycling.