Genetic elements and defense systems drive diversification and evolution in Asgard archaea

Asgard Archaea are of great interest as the progenitors of Eukaryotes, but little is known about the mobile genetic elements (MGEs) that may shape their ongoing evolution. Here, we describe MGEs that replicate in Atabeyarchaeia, wetland Asgard archaea phylum represented by two complete genomes. We used soil depth-resolved population metagenomic datasets to track 18 MGEs for which genome structures were defined and precise chromosome integration sites could be identified for confident host linkage. Additionally, we identified a complete 20.67 kilobase pair (kbp) circular plasmid (the first reported for Asgard archaea) and two groups of viruses linked to Atabeyarchaeia, via CRISPR spacer targeting. Closely related 40 kbp viruses possess a hypervariable genomic region encoding combinations of specific genes for small cysteine-rich proteins structurally similar to restriction-homing endonucleases. One 10.9 kbp circularizable plasmid-like MGE integrates genomically into an Atabeyarchaeia chromosome and has a 2.5 kbp circularizable element integrated within it. The 10.9 kbp MGE encodes a highly expressed methylase with a sequence specificity matching an active methylation motif identified by PacBio sequencing. Restriction-modification of Atabeyarchaeia differs from that of another coexisting Asgard archaea Freyarchaeia which has few identified MGEs but possesses diverse defense mechanisms, including DISARM and Hachiman not found in Atabeyarchaeia. Overall, defense systems and methylation mechanisms of Asgard archaea likely modulate their interactions with MGEs, and integration/excision and copy number variation of MGEs in turn enable host genetic versatility.