Borgs are giant genetic elements with potential to expand metabolic capacity

Anaerobic methane oxidation exerts a key control on greenhouse gas emissions, yet factors that modulate the activity of microorganisms performing this function remain little explored. In studying groundwater, sediments, and wetland soil where methane production and oxidation occur, we discovered extraordinarily large, diverse DNA sequences that primarily encode hypothetical proteins. Four curated, complete genomes are linear, up to 1 Mbp in length and share genome organization, including replichore structure, long inverted terminal repeats, and genome-wide unique perfect tandem direct repeats that are intergenic or generate amino acid repeats. We infer that these are highly divergent archaeal extrachromosomal elements with a distinct evolutionary origin. Gene sequence similarity, phylogeny, and local divergence of sequence composition indicate that many of their genes were assimilated from methane-oxidizing Methanoperedens archaea. We refer to these elements as Borgs. We identified at least 19 different Borg types coexisting with Methanoperedens spp. in four distinct ecosystems. Borgs provide methane-oxidizing Methanoperedens archaea access to genes coding for proteins involved in redox reactions and energy conservation (e.g., clusters of multiheme cytochromes, methyl coenzyme M reductase) and response to changing environmental conditions. Thus, Borgs could play previously unrecognized roles in the metabolism of a group of archaea known to modulate greenhouse gas emissions.