Group II Introns in Archaeal Genomes and the Evolutionary Origin of Eukaryotic Spliceosomal Introns

Abstract

A key attribute of eukaryotic genomes is the presence of abundant spliceosomal introns that break up many protein-coding genes into multiple exons and must be spliced out during the process of gene expression. These introns are believed to be evolutionarily derived from group II introns, which are known to be widespread in bacteria. One prominent hypothesis is that the spliceosomal intron arose after the endosymbiotic origin of the mitochondrion, as a consequence of transfer of genes containing group II introns from the organelle to nuclear genome; in this model, transfer of group II introns into the ancestral eukaryotic genome set the stage for evolution of the spliceosomal form. However, the recent discovery and sequencing of asgard archaea -- the closest archaeal relatives of extant eukaryotes -- has shed significant light on the composition of the early eukaryotic genome and calls that model into question. Using sequence analysis and structural modeling, we show here the presence of group II intron maturases in the genomes of Heimdallarchaeia and other asgard archaea, and demonstrate by phylogenetic inference that these are closely related to both eukaryotic mitochondrial group II intron maturases and the spliceosome protein PRP8. This suggests that the first intron-containing eukaryotic common ancestor (FIECA) inherited selfish group II introns from its ancestral archaeal genome - the progenitor of the nuclear genome - rather than from the mitochondrial endosymbiont. These observations suggest that the spread and diversification of introns may have occurred independently of the acquisition of the mitochondrion. To better understand the context for intron evolution, we investigate the broader occurrence of group II introns in archaea, identify archaeal clades enriched in group II introns, and perform structural modeling to examine the relationship between the archaeal group II intron maturase and the eukaryotic spliceosome. We propose a model of intron acquisition and expansion during early eukaryotic evolution that places the spread of introns prior to the acquisition of mitochondria, possibly facilitated by the separation of transcription and translation afforded by the nucleus.