Borg extrachromosomal elements of methane-oxidizing archaea have conserved and expressed genetic repertoires

Abstract

AbstractBorgs are huge extrachromosomal elements (ECE) of anaerobic methane-consuming “CandidatusMethanoperedens” archaea. Here, we used nanopore sequencing to validate published complete genomes curated from short reads and to reconstruct new genomes. 13 complete and four near-complete linear genomes share 40 genes that define a largely syntenous genome backbone. We use these conserved genes to identify new Borgs from peatland soil and to delineate Borg phylogeny, revealing two major clades. Remarkably, Borg genes encoding OmcZ nanowire-like electron-exporting cytochromes and cell surface proteins are more highly expressed than those of hostMethanoperedens, indicating that Borgs augment theMethanoperedensactivityin situ. We reconstructed the first complete 4.00 Mbp genome for aMethanoperedensthat is inferred to be a Borg host and predicted its methylation motifs, which differ from pervasive TC and CC methylation motifs of the Borgs. Thus, methylation may enableMethanoperedensto distinguish their genomes from those of Borgs. Very high Borg toMethanoperedensratios and structural predictions suggest that Borgs may be capable of encapsulation. The findings clearly define Borgs as a distinct class of ECE with shared genomic signatures, establish their diversification from a common ancestor with genetic inheritance, and raise the possibility of periodic existence outside of host cells.