Background Microbes play an active role in oil spill remediation, but little is known about the baseline hydrocarbon-degrading communities that exist before a spill occurs, or the diversity of metabolic mechanisms responsible for degradation. The Faroe Shetland Channel (FSC) is a region of the North Atlantic Ocean with prominent oil production and a diverse microbial community associated with the degradation of petroleum compounds. We characterized the baseline hydrocarbon-degrading communities of the FSC and identified potential novel molecular mechanisms for petrochemical degradation. Results We obtained 42 metagenome assembled genomes (MAGs) from bacteria actively utilizing a major compound in oil, n-hexadecane, via stable isotope probing (SIP) from the FSC. Phylogenomics revealed that they belong to 19 genera, including two not previously shown to degrade hydrocarbons: Lentibacter(Alphaproteobacteria) and Dokdonia(Bacteroidetes). Diversity surveys indicated Lentibacter were dominant members of the FSC, constituting up to 17% of these communities. 42% of the SIP-enriched MAGs encoded a complete alkane oxidation pathway containing alkane monooxygenase (AlkB), rubredoxin reductase (AlkT), and rubredoxin-2 (AlkG). However, 40% of the Alphaproteobacteria lacked AlkG for electron transfer in alkane hydroxylation. Instead, they encoded novel disulfide isomerases with iron-binding cysteine motifs conserved across rubredoxins. Dokdonialacked AlkT and AlkG, however, their central alkane-degradation catabolic pathways were complete. Conclusion This study describes new bacteria capable of hydrocarbon degradation including the dominant genera Lentibacter, along with novel putative hydrocarbon degradation enzymes. These bacteria may be continuously purging hydrocarbons released from industrial activities in the FSC. This study advances our understanding of the diversity and physiologies of alkane degradation in the North Atlantic and provides evidence of new mechanisms used to metabolize alkanes.