Krumholzibacteriota and Deltaproteobacteria contain rare genetic potential to liberate carbon from monoaromatic compounds in subsurface coal seams

Biogenic methane in subsurface coal seam environments is produced by diverse consortia of microbes. Although this methane is useful for global energy security, it remains unclear which microbes can liberate carbon from the coal. Most of this carbon is relatively resistant to biodegradation, as it is contained within aromatic rings. Thus, to explore for coal-degrading taxa in the subsurface, this study used coal seam metagenomes to reconstruct important metagenome-assembled genomes (MAGs) using a key genomic marker for the anaerobic degradation of monoaromatic compounds as a guide: the benzoyl-CoA reductase gene (bcrABCD). Three taxa were identified with this genetic potential. The first was a novel taxon from the Krumholzibacteriota phylum, which this study is the first to describe. This Krumholzibacteriota sp. contained a full set of genes for benzoyl-CoA dearomatisation, in addition to other genes for anaerobic catabolism of monoaromatics. Analysis of Krumholzibacteriota MAGs from other environments revealed that this genetic potential may be common within this phylum, and thus they may be important organisms for the liberation of recalcitrant carbon on a global scale. Further, two taxa from the Deltaproteobacteria class were also implicated in monoaromatic degradation; two geographically unrelated Syntrophorhabdus aromaticivorans MAGs, and a Syntrophaceae sp. MAG. Each of these three taxa are potential rate-limiting organisms for subsurface coal-to-methane biodegradation. Their description here provides an understanding of their function within the coal seam microbiome, and will help inform future efforts in coal bed methane stimulation, anoxic bioremediation of organic pollutants, and assessments of anoxic carbon cycling and emissions. ImportanceSubsurface coal seams are highly anoxic and oligotrophic environments, where the main source of carbon is "locked away" within aromatic rings. Despite these challenges, biogenic methane accumulates within many of these coal seams, which implies that the coal seam microbiome can "unlock" this carbon source in situ. For over two decades, researchers have been working to understand which organisms are responsible for these processes. This study provides the first descriptions of these organisms. Here, we report metagenomic insights into the liberation of carbon from aromatic molecules typically found within coal, the degradation pathways involved, and descriptions of the Krumholzibacteriota sp., Syntrophorhabdus aromaticivorans, and Syntrophaceae sp. that contain this genetic potential. Additionally, this is the first time that the Krumholzibacteriota phylum has been implicated in anaerobic dearomatisation of aromatic hydrocarbons. This potential is identified here in numerous taxa within the phylum from other subsurface environments, implicating Krumholzibacteriota in global-scale carbon-cycling processes.