Intron-dominated genomes of early ancestors of eukaryotes

Abstract

Evolutionary reconstructions using maximum likelihood methods point to unexpectedly high densities of introns in protein-coding genes of ancestral eukaryotic forms including the last common ancestor of all extant eukaryotes. Combined with the evidence of the origin of spliceosomal introns from invading Group II self-splicing introns, these results suggest that early ancestral eukaryotic genomes consisted of up to 80% sequences derived from Group II introns, a much greater contribution of introns than that seen in any extant genome. An organism with such an unusual genome architecture could survive only under conditions of a severe population bottleneck.

Figure 1

Intron densities in selected extant eukaryotic genomes and inferred intron densities in ancestral genomes. The data are from Carmel et al. (2007). Intron density is the number of introns per kilobase of protein-coding DNA. Color code: blue, extant eukaryotic genomes; gray, ancestral forms; and red, LECA. For the ancestral forms, the low bound of intron density is indicated. Species names: Anoga, Anopheles gambiae; Arath, Arabidopsis thaliana; Aspfu, Aspergillus fumigates; Caeel, Caenorhabditis elegans; Cioin, Ciona intestinalis; Cryne, Cryptococcus neoformis; Danre, Danio rerio; Dicdi, Dictyostelium discoideum; Drome, Drosophila melanogaster; Homsa, Homo sapiens; Neucr, Neurospora crassa; Plafa, Plasmodium falciparum; Schpo, Schizosaccharomyces pombae; Strpu, Strongylocentrotus purpuratum; and Thepa, Theileria parva. (This figure appears in color in the online version of Journal of Heredity.)

Figure 2

Mean and median intron lengths in extant eukaryotic genomes and inferred mean and median lengths of introns in a hypothetical pre-LECA eukaryote. For each taxon, the genome with the highest values of mean and median lengths was chosen. The data are from the National Center for Biotechnology Information genome division (http://www.ncbi.nlm.nih.gov/Genomes/). (This figure appears in color in the online version of Journal of Heredity.)

Figure 3

Approximate fraction of the genome occupied by introns in selected extant eukaryotic taxa and in a hypothetical pre-LECA eukaryote. For each taxon, the genome with the highest intron content (as in Figure 2) was chosen. The data are from the National Center for Biotechnology Information genome division (http://www.ncbi.nlm.nih.gov/Genomes/). (This figure appears in color in the online version of Journal of Heredity.)

Figure 4

A putative major population bottleneck on the path of evolution from mitochondrial endosymbiosis to LECA. (This figure appears in color in the online version of Journal of Heredity.)