Methanotrophic Methanoperedens archaea host diverse and interacting extrachromosomal elements

Methane emissions that contribute to climate change can be mitigated by anaerobic methane-oxidizing archaea such as Methanoperedens. Some Methanoperedens have huge extrachromosomal genetic elements (ECEs) called Borgs that may modulate their activity, yet the broader diversity of Methanoperedens ECEs is little studied. Here, we report small enigmatic linear ECEs, circular viruses and unclassified ECEs, that we predict replicate within Methanoperedens. 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 and Methanoperedens. 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 of Methanoperedens viruses, 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 other Methanoperedens ECEs including previously reported plasmids. The diverse groups of ECEs exchange genetic information with each other and with Methanoperedens, likely impacting the activity and evolution of these environmentally important archaea.