The two-domain tree of life is linked to a new root for the Archaea

Abstract

One of the most fundamental questions in evolutionary biology is the origin of the lineage leading to eukaryotes. Recent phylogenomic analyses have indicated an emergence of eukaryotes from within the radiation of modern Archaea and specifically from a group comprising Thaumarchaeota/"Aigarchaeota" (candidate phylum)/Crenarchaeota/Korarchaeota (TACK). Despite their major implications, these studies were all based on the reconstruction of universal trees and left the exact placement of eukaryotes with respect to the TACK lineage unclear. Here we have applied an original two-step approach that involves the separate analysis of markers shared between Archaea and eukaryotes and between Archaea and Bacteria. This strategy allowed us to use a larger number of markers and greater taxonomic coverage, obtain high-quality alignments, and alleviate tree reconstruction artifacts potentially introduced when analyzing the three domains simultaneously. Our results robustly indicate a sister relationship of eukaryotes with the TACK superphylum that is strongly associated with a distinct root of the Archaea that lies within the Euryarchaeota, challenging the traditional topology of the archaeal tree. Therefore, if we are to embrace an archaeal origin for eukaryotes, our view of the evolution of the third domain of life will have to be profoundly reconsidered, as will many areas of investigation aimed at inferring ancestral characteristics of early life and Earth.

Keywords: Tree of Life; ancient evolution; archaeal phylogeny; methanogenesis; site-heterogeneous model.

Fig. 1.

Unrooted Bayesian phylogeny of the A/E supermatrix. The tree was calculated by Phylobayes (CAT+GTR+Γ4). Values at nodes represent posterior probabilities. For clarity, the branch leading to eukaryotes has been shortened, and the real length is indicated. KOR, Korarchaeota; CREN, Crenarchaeota; ‘AIG’, Aigarchaeota; THAUM, Thaumarchaeota; EURY, Euryarchaeota. (Scale bar: average number of substitutions per site.)

Fig. 2.

The three alternative scenarios for the origin of eukaryotes depending on the root of the Archaea. Euka, Eukaryotes; Eury, Euryarchaeota; TACK, Thaumarchaeota, Aigarchaeota, Crenarchaeota, and Korarchaeota.

Fig. 3.

Unrooted Bayesian phylogeny of the A/B supermatrix. The tree was calculated by Phylobayes (CAT+GTR+Γ4). Values at nodes represent posterior probabilities. For clarity, the branch leading to Bacteria has been shortened, and the real length is indicated. The root within Euryarchaeota leading to Cluster I and Cluster II Archaea is indicated as root 1, with respect to the traditional root between Euryarchaeota and the TACK superphylum (root 2) obtained by the LG+Γ4 model (SI Appendix, Fig. S6). (Scale bar: average number of substitutions per site.)

Fig. 4.

Effect of removal of fast-evolving positions from the A/B supermatrix with the site-homogeneous LG+Γ4 model (A) and with the site-heterogeneous CAT+GTR+Γ4 model (B). The x axis shows the name of the supermatrix and its number of positions, where removal of fastest-evolving sites proceeds from left to right (from the original supermatrix to progressively less noisy and smaller supermatrices). The y axis represents support of each matrix for either root 1 (indicated by the combined support for the monophyly of Cluster I and for the monophyly of Cluster II) or for root 2 (indicated by the combined support for the monophyly of Euryarchaeota and for the monophyly of the TACK superphylum). The trees corresponding to each of these supermatrices are provided as SI Appendix, Supplementary Datasets.

Fig. 5.

Bayesian phylogeny of the A/B/E supermatrix. The tree was calculated by Phylobayes (CAT+GTR+Γ4). Values at nodes represent posterior probabilities. For clarity, the branch leading to Bacteria has been shortened, and the real length is indicated. The emergence of eukaryotes within Archaea is associated with support for the newly inferred archaeal root 1 (Fig. 3). The sister relationship of eukaryotes with korarchaeon is poorly supported and likely is an artifact of tree reconstruction (see text for discussion). Removal of korarchaeon from the dataset did not change the resulting topology (SI Appendix, Fig. S8). (Scale bar: average number of substitutions per site.)