Novel Asgard archaea phylum Hermodarchaeota degrade alkanes and aromatics via alkyl/benzyl-succinate synthase and benzoyl-CoA pathway

Abstract

Asgard superphylum is composed of a group of uncultivated archaea that are deemed the closest relatives of eukaryotes. These archaea are widely distributed in anaerobic environments and suggested to be important players in carbon cycling of sediments. Alkanes and aromatics are refractory organic compounds and abundant in sediments. However, little is known about degradation of these compounds by Asgard archaea to date. Here, we describe a previously unrecognized archaeal phylum, Hermodarchaeota, affiliated with the Asgard superphylum. The genomes of these archaea were recovered in metagenomes from mangrove sediments, and were found to encode alkyl/benzyl-succinate synthases and their activating enzymes that are similar to those found in alkanes-degrading sulfate-reducing bacteria. Hermodarchaeota also encode enzymes for alkyl-coenzyme A and benzoyl-coenzyme A oxidation, and the Wood-Ljungdahl pathway, as well as nitrate reductases. Furthermore, transcripts for these enzymes have been frequently detected in metatranscriptomes from mangrove sediments. This indicates that members of this phylum are able to anaerobically oxidize alkanes and aromatic compounds, coupling the reduction of nitrate. Genes encoding 16S rRNA and alkyl/benzyl-succinate synthases analogous to those in Hermodarchaeota were identified in a range of marine and freshwater sediments. These findings suggest that Asgard archaea capable of degrading alkanes and aromatics via formation of alkyl/benzyl-substituted succinates are ubiquitous in sediments.