Syntrophy among Archaea and Bacteria facilitates the anaerobic degradation of organic compounds to CH4 and CO2. Particularly during aliphatic and aromatic hydrocarbon mineralization, as in crude oil reservoirs and petroleum contaminated sediments, metabolic interactions between obligate mutualistic microbial partners are of central importance1. Using micromanipulation combined with shotgun metagenomic approaches, we disentangled the genomes of complex consortia inside a short chain alkane degrading cultures operating under methanogenic conditions. Metabolic reconstruction revealed that only a small fraction of genes in the metagenome assembled genomes of this study, encode the capacity for fermentation of alkanes facilitated by energy conservation linked to H2 metabolism. Instead, inferred lifestyles based on scavenging anabolic products and intermediate fermentation products derived from detrital biomass was a common feature in the consortia. Additionally, inferred auxotrophy for vitamins and amino acids suggests that the hydrocarbon degrading microbial assemblages are structured and maintained by multiple interactions beyond the canonical H2 producing and syntrophic alkane degrader methanogen partnership2. Our study uncovers the complexity of interactomes within microbial consortia mediating hydrocarbon transformation under anaerobic conditions.