Marine Sediments Harbor Diverse Archaea and Bacteria With Potentials for Anaerobic Hydrocarbon Degradation via Fumarate Addition

Abstract Background: Marine sediments can contain large amounts of alkanes and methylated aromatic hydrocarbons that are introduced by natural processes or anthropogenic activities. These compounds can be biodegraded by anaerobic microorganisms via enzymatic addition of fumarate. Previous gene- and genome-based surveys have detected ubiquitous and novel fumarate-adding enzymes (FAE), but these were neither confirmed as occurring within full degradation pathways nor affiliated with known organisms. The identity and ecological roles of a significant fraction of anaerobic hydrocarbon degraders in marine sediments therefore remains unknown.Results: By combining phylogenetic reconstructions, protein homolog modelling, and functional profiling of publicly available and newly sequenced metagenomes and genomes, 61 draft bacterial and archaeal genomes encoding anaerobic hydrocarbon degradation via fumarate addition were obtained. Besides Deltaproteobacteria that are well-known to catalyze these reactions, Chloroflexi are dominant FAE-encoding bacteria in hydrocarbon-impacted sediments, potentially coupling sulfate reduction or fermentation to anaerobic hydrocarbon degradation. Among Archaea, besides Archaeoglobi previously shown to have this capability, genomes of Heimdallarchaeota, Lokiarchaeota, Thorarchaeota and Thermoplasmata also suggest fermentative hydrocarbon degradation using archaea-type FAE. The biogeography survey reveals these bacterial and archaeal hydrocarbon degraders occur in a wide range of marine sediments, including high abundances of FAE-encoding Asgard archaea associated with natural seeps and subseafloor ecosystems.Conclusions: Our results expand the knowledge of novel microbial lineages engaged in anaerobic degradation of alkanes and methylated aromatic hydrocarbons, and shed new light on the importance of marine sedimentary archaea in hydrocarbon degradation.