Groundwaterelusimicrobiaare Metabolically Diverse Compared To Gut Microbiomeelusimicrobiaand Some Have A Novel Nitrogenase Paralog

Currently described members ofElusimicrobia, a relatively recently defined phylum, are animal-associated and rely on fermentation. However, free-livingElusimicrobiahave been detected in sediments, soils and groundwater, raising questions regarding their metabolic capacities and evolutionary relationship to animal-associated species. Here, we analyzed 94 draft-quality, non-redundant genomes, including 30 newly reconstructed genomes, from diverse animal-associated and natural environments. Genomes group into 12 clades, 10 of which previously lacked reference genomes. Groundwater-associatedElusimicrobiaare predicted to be capable of heterotrophic or autotrophic lifestyles, reliant on oxygen or nitrate/nitrite-dependent respiration, or a variety of organic compounds andRhodobacternitrogen fixation (Rnf) complex-dependent acetogenesis with hydrogen and carbon dioxide as the substrates. Genomes from two clades of groundwater-associatedElusimicrobiaoften encode a new group of nitrogenase paralogs that co-occur with an extensive suite of radical S-Adenosylmethionine (SAM) proteins. We identified similar genomic loci in genomes of bacteria from the Gracilibacteria phylum and theMyxococcalesorder and predict that the gene clusters reduce a tetrapyrrole, possibly to form a novel cofactor. The animal-associatedElusimicrobiaclades nest phylogenetically within two free-living-associated clades. Thus, we propose an evolutionary trajectory in which someElusimicrobiaadapted to animal-associated lifestyles from free-living species via genome reduction.