Genetic exchange drives relatedness of large linear and circular extrachromosomal elements of archaea

Archaeal extra-chromosomal elements (ECEs) play key roles in archaeal host biology and evolution, yet little is known about their diversity and interactions with each other. Here, we report 42 complete 66 - 165 kbp genomes: 23 "Klingons", 8 "Romulans" and "Romulan-like elements", and 11 "Ferengi", three new families of archaeal ECEs from diverse terrestrial environments. Methylation patterns, phylogenetics and gene sharing analyses suggest that Klingons and Romulans associate with Candidatus Methanoperedens and Ferengi are likely hosted by Candidatus Bathyarchaeaota. Like known archaeal viruses and plasmids, these ECEs both have circular genomes and replicate bi-directionally, unlike the linear Borg and mini-Borg ECEs that also replicate in Methanoperedens. The new ECE genomes all encode genes for methylation, glycosylation, protein degradation, and novel TnpB-like enzymes, which may interact with novel CRISPR-like arrays. All genomes also encode proteins with strong structural similarity to archaeal viral capsid proteins, and some are predicted to multimerize into pentameric or hexameric subunit capsid-like arrays and thus may encapsulate themselves. The three new ECE families share gene content with each other and with Borgs and mini-Borgs, often concentrated in specific genomic regions. Discordance among single gene and genomic phylogenies suggests that apparent relatedness of the five distinct ECE types stems from extensive horizontal gene transfer, rather than evolution from a common ancestor. The three new families of ECEs broaden our understanding of the diversity of archaeal ECEs and highlight the role of horizontal gene transfer in modulating the archaeal and archaeal ECE gene pools.