The common ancestor of archaea and eukarya was not an archaeon

Abstract

It is often assumed that eukarya originated from archaea. This view has been recently supported by phylogenetic analyses in which eukarya are nested within archaea. Here, I argue that these analyses are not reliable, and I critically discuss archaeal ancestor scenarios, as well as fusion scenarios for the origin of eukaryotes. Based on recognized evolutionary trends toward reduction in archaea and toward complexity in eukarya, I suggest that their last common ancestor was more complex than modern archaea but simpler than modern eukaryotes (the bug in-between scenario). I propose that the ancestors of archaea (and bacteria) escaped protoeukaryotic predators by invading high temperature biotopes, triggering their reductive evolution toward the "prokaryotic" phenotype (the thermoreduction hypothesis). Intriguingly, whereas archaea and eukarya share many basic features at the molecular level, the archaeal mobilome resembles more the bacterial than the eukaryotic one. I suggest that selection of different parts of the ancestral virosphere at the onset of the three domains played a critical role in shaping their respective biology. Eukarya probably evolved toward complexity with the help of retroviruses and large DNA viruses, whereas similar selection pressure (thermoreduction) could explain why the archaeal and bacterial mobilomes somehow resemble each other.

Figure 1

The Aristotle scenarios. (a) The traditional ladder-like evolutionary scenario, in which organisms increased in complexity from the origin of life to prokaryotes and eukaryotes, with archaea being intermediate organisms on the way to become eukaryotes; (b) the classical universal tree of life of Woese et al. [53] in red, combined with the fusion hypothesis (blue line). The LECA is the last eukaryotic common ancestor and FME the first eukaryote harbouring mitochondria; the dotted line refers to the hypothesis in which eukaryotes originated by the association of an archaeon with the mitochondrial bacterial ancestor [49]. Thick arrows indicate the emergence of eukaryotic specific features (ESFs).

Figure 2

Two contrasting phylogenies of the same universal protein. Schematic representation of two published phylogenies of a universal protein known under different names (YgjD, YeaZ, Kae1/OSGEP, and Qri7/OSGEP L) which is involved in the biosynthesis of the universal tRNA modified base t6A [54]. These simplified phylogenies are adapted from Figure S46 in [55] (left panel) and from Figure S1 in [56] (right panel). Squares indicate unresolved nodes, whereas triangles indicate resolve nodes. The tree on the right is congruent with firmly established biological knowledge such as the monophyly of bacteria and eukarya, the bacterial origin of mitochondria. It favours the classical three-domain tree of Woese and colleagues. The tree on the left, which is not resolved, with aberrant paraphyly of archaea (see for instance the position of Nanoarchaeum equitans) was nevertheless used by the authors to support the “eocyte tree”. Comparison of these trees clearly reveals that the methodology (data sampling and/or algorithm for tree reconstruction) used by Cox and co-workers [55] for phylogenetic analyses cannot recover correct phylogenies for universal proteins.

Figure 3

A scenario based on divergent evolutionary trends for “prokaryotes” (archaea and bacteria) and eukaryotes. This scheme is based on the assumption that the universal tree is rooted in the bacterial branch [53]. Complexity increased from the origin of life to LUCA to eukaryotes, via the last archaeal-eukaryal common ancestor (LAECA). Reductive evolution occurred from LAECA to LACA and modern archaea, possibly triggered by thermoreduction [77] indicated by large red triangles and/or as a way to escape protoeukaryotic predators [50]. Bacteria experienced independently a similar evolutionary path. The blue arrow indicates the mitochondrial endosymbiosis.

Figure 4

Schematic evolution of cellular membranes. Distribution of proteins involved in phospholipid biosynthesis in the three domains, LUCA, and LACA are depicted according to Lombard et al., [18, 22], but my evolutionary interpretation is different from those proposed by these authors [22]. Bacterial/eukaryal type membranes are in green and archaeal type membrane in red. Green circles correspond to universal enzymes involved in phospholipid biosynthesis (glycerol phosphate dehydrogenases, enzymes linking polar head groups to glycerol). Pink circles correspond to the classical mevalonate pathway for isoprenoid biosynthesis that was probably present in LUCA and lost in bacteria. Red circle represents enzymes of the alternative mevalonate pathway, which are specific of archaea, and involves a mixture of eukaryotic-like and archaeal specific enzymes. Blue circles correspond to the nonhomologous methylerythritol pathway for isoprenoid biosynthesis present in bacteria. Black circles represent the fatty acid biosynthetic pathway, which is no longer used for membrane phospholipid biosynthesis in archaea. Circles corresponding to proteins involved in the biosynthesis of membrane phospholipids are encircled.

Figure 5

Schematic phylogenies of RNA polymerases. The RNA polymerase tree has been drawn combining and interpreting results from several papers [54, 60, 78, 79]. The position of the Nudivirus RNA polymerase is extrapolated from its high divergence with other homologous RNA polymerases (indicated by dotted lines). An update phylogeny would be welcome but would not change the take-home message, the puzzling mixture of cellular and viral enzymes, suggesting several ancient transfers between viruses and cells.