MethanotrophicMethanoperedensarchaea host diverse and interacting extrachromosomal elements

Abstract

AbstractMethane emissions that contribute to climate change can be mitigated by anaerobic methane-oxidizing archaea such asMethanoperedens. SomeMethanoperedenshave huge extrachromosomal genetic elements (ECEs) called Borgs that may modulate their activity, yet the broader diversity ofMethanoperedensECEs is little studied. Here, we report small enigmatic linear ECEs, circular viruses and unclassified ECEs, that we predict replicate withinMethanoperedens. The linear ECEs have features such as inverted terminal repeats, pervasive tandem repeats, and coding patterns that are strongly reminiscent of Borgs, but they are only 52 kb to 145 kb in length. They share proteins with Borgs andMethanoperedens. Thus, we refer to them as mini-Borgs. Mini-Borgs are genetically diverse and we assign them to at least five family-level groups. We also identify eight novel families ofMethanoperedensviruses, some of which encode multiheme cytochromes, and unclassified circular ECEs that encode TnpB genes. A population-heterogeneous CRISPR array is in close proximity to the TnpB and has spacers that target otherMethanoperedensECEs including previously reported plasmids. The diverse groups of ECEs exchange genetic information with each other and withMethanoperedens, likely impacting the activity and evolution of these environmentally important archaea.