Evidence for the anaerobic biodegradation of higher molecular weight hydrocarbons in the Guaymas Basin

The hydrothermal sediments of the Guaymas Basin are rich in chemically complex petroleum components, including gaseous hydrocarbons, higher molecular weight n-alkanes and aromatic compounds. Studies of indigenous deep-sea microorganisms obtained from these sediments led to novel insights on the fundamental mechanisms for the anaerobic biodegradation of gaseous hydrocarbons. However, the metabolic fate of other hydrocarbons and the requisite organisms involved in the cycling of petroleum components remain largely unexplored. Metagenomic sequencing and laboratory enrichments were used to garner evidence for the anaerobic biodegradation of liquid hydrocarbons in hydrothermal sediments and mineral concretions from three sites in the Guaymas Basin (“Megamat II”, Rebecca's Roost and Octopus Mound). Elevated sulfate consumption by microbial enrichments from the Megamat II and Rebecca's Roost sites was observed at 55 °C when sediment incubations were amended with liquid n-alkanes (C6–C12; C16–C18) or with crude oil as potential electron donors. The biodegradation of the same hydrocarbons, linked to sulfate reduction, was also evident at 31 °C by microbial consortia enriched from the “Megamat II” and Octopus Mound sites. Notably, methane was concurrently produced in enrichments from the Octopus Mound site that was covered by Ampharetid methane-oxidizing worm mats. Metagenomic sequencing revealed that Deltaproteobacteria were predominant at the three sites (up to 47.48% of the microbial community). Moreover, the genes responsible for the activation of alkanes (Ass, alkylsuccinate synthase) and aromatic hydrocarbons (Bss, benzylsuccinate synthase) were identified from all three sites. The reconstruction of high-quality draft genomes from the Desulfobacterales further confirmed their metabolic potential to degrade alkanes via fumarate addition in Guaymas Basin sediments. Collectively, our findings demonstrate that mesophilic and thermophilic microbial consortia from hydrothermal sediments and mineral concretions in different regions of the Guaymas Basin are capable of anaerobically biodegrading C6–C12- and C16–C18 n-alkanes as well as crude oil under the ambient temperature regimes. Our findings highlight the importance of integrating multiple approaches to better understand the ecological functioning of microbial communities in hydrocarbon-rich hydrothermal systems.