The deep archaeal roots of eukaryotes

Abstract

The set of conserved eukaryotic protein-coding genes includes distinct subsets one of which appears to be most closely related to and, by inference, derived from archaea, whereas another one appears to be of bacterial, possibly, endosymbiotic origin. The "archaeal" genes of eukaryotes, primarily, encode components of information-processing systems, whereas the "bacterial" genes are predominantly operational. The precise nature of the archaeo-eukaryotic relationship remains uncertain, and it has been variously argued that eukaryotic informational genes evolved from the homologous genes of Euryarchaeota or Crenarchaeota (the major branches of extant archaea) or that the origin of eukaryotes lies outside the known diversity of archaea. We describe a comprehensive set of 355 eukaryotic genes of apparent archaeal origin identified through ortholog detection and phylogenetic analysis. Phylogenetic hypothesis testing using constrained trees, combined with a systematic search for shared derived characters in the form of homologous inserts in conserved proteins, indicate that, for the majority of these genes, the preferred tree topology is one with the eukaryotic branch placed outside the extant diversity of archaea although small subsets of genes show crenarchaeal and euryarchaeal affinities. Thus, the archaeal genes in eukaryotes appear to descend from a distinct, ancient, and otherwise uncharacterized archaeal lineage that acquired some euryarchaeal and crenarchaeal genes via early horizontal gene transfer.

FIG. 1.—

Phylogenetic classification of the archaeal–eukaryotic orthologs. (a) Flowchart of the procedure. (b) Breakdown of orthologous clusters by inferred origin A, archaea; B, bacteria; CA, Crenarchaeota; E, eukaryotes; and EA, Euryarchaeota. For further details, see text.

FIG. 2.—

Functional classification of ancestral eukaryotic genes of different probable origins. (a) Distribution of ancestral eukaryotic genes of different inferred origins by functional categories. The functional classes are as in the COG database: C, energy production and conversion; D, cell division; E, amino acid metabolism and transport; F, nucleotide metabolism and transport; G, carbohydrate metabolism and transport; H, coenzyme metabolism; I, lipid metabolism; J, translation; K, transcription; L, replication and repair; O, posttranslational modification, protein turnover, and chaperone functions; Q, secondary metabolism; T, signal transduction; U, intracellular trafficking and secretion; V, defense and resistance; R, general functional prediction only (typically, prediction of biochemical activity); and S, function unknown. (b) Fractions of arCOGs belonging to different functional classes in the set of 975 A–E pairs and in the set of 351 eukaryotic genes of inferred archaeal origin. (c) Log-odds ratio of the fraction of arCOGs belonging to different functional classes relative to the fraction of arCOGs that belong to the A–E set and the set of eukaryotic genes of inferred archaeal origin (1,008/7,538 and 286/7,538, respectively). The log base is 2.

FIG. 3.—

The evolutionary relationship between archaea and eukaryotes assessed by phylogenetic analysis of 136 A–E–B clusters. The ELW values are plotted on a simplex surface.

FIG. 4.—

Distribution of the deep, crenarchaeal, and euryarchaeal topologies depending on the ELW value cutoff.

FIG. 5.—

A cartoon representation of the deep, crenarchaeal, and euryarchaeal inferred origins of the archaeal genes in eukaryotes.