Genome beginnings: rooting the tree of life

Abstract

A rooted tree of life provides a framework to answer central questions about the evolution of life. Here we review progress on rooting the tree of life and introduce a new root of life obtained through the analysis of indels, insertions and deletions, found within paralogous gene sets. Through the analysis of indels in eight paralogous gene sets, the root is localized to the branch between the clade consisting of the Actinobacteria and the double-membrane (Gram-negative) prokaryotes and one consisting of the archaebacteria and the firmicutes. This root provides a new perspective on the habitats of early life, including the evolution of methanogenesis, membranes and hyperthermophily, and the speciation of major prokaryotic taxa. Our analyses exclude methanogenesis as a primitive metabolism, in contrast to previous findings. They parsimoniously imply that the ether archaebacterial lipids are not primitive and that the cenancestral prokaryotic population consisted of organisms enclosed by a single, ester-linked lipid membrane, covered by a peptidoglycan layer. These results explain the similarities previously noted by others between the lipid synthesis pathways in eubacteria and archaebacteria. The new root also implies that the last common ancestor was not hyperthermophilic, although moderate thermophily cannot be excluded.

An archaeal origin of eukaryotes supports only two primary domains of life

“…These results imply that the mitochondrion was acquired before the radiation of known eukaryotes; therefore, the observation that the mitochondrion descends from an endosymbiotic member of the alphaproteobacteria 64,88 provides strong evidence that the origin of eukaryotes postdates the origin of that bacterial group 2,89 . A relatively late origin of eukaryotes compared to Bacteria is consistent with the best evidence from the geological record and with either the three-domains or eocyte tree rooted on the bacterial stem or within the Bacteria [5][6][7][8][9][10][11] . Moreover, if all eukaryotes have both mitochondria and a nucleus, then we can no longer be sure which structure arose first during evolution: in other words, the host cell that acquired the mitochondrion need not have already possessed a nucleus.…”

“…However, this record is very incomplete and subject to deep and sometimes heated controversy. The first fossil that is indisputably eukaryotic is of a bangiophyte red alga dated to between 1.2 billion and 720 million years ago 75 , but earlier microfossils with a possible eukaryotic origin are found in rocks dated to approximately 1.8 billion depicting the relationships between Archaea and the eukaryotic nuclear lineage, consistent with recent analyses of core genes using new methods [47][48][49] and rooted using the Bacteria as the outgroup [5][6][7][8][9][10][11] . The phylogenetic position of Korarchaeum was not consistently resolved in these different analyses and hence is depicted as part of a polytomy.…”

“…Evolutionary biologists now have access to more data and better phylogenetic methods than ever before, although there is still much room for improvement and many uncertainties remain. These caveats apply equally to all attempts to infer ancient relationships, affecting not only the debate over whether the three-domains or eocyte tree best depicts the history of core eukaryotic genes, but also the placement of the universal root 5,[9][10][11][12]21 and the relationships among major eukaryotic phyla 26,102,103 . The pioneering analyses of molecular sequence data led by Carl Woese and his coworkers culminated in the three-domains tree recognizing the Archaea, Bacteria and Eukaryota as the three primary domains of cellular life.…”

“…Although similar to Bacteria in terms of cell structure, molecular phylogenies for ribosomal RNA and a small core of genes, that mainly have essential roles in protein translation 3 , suggested that the Archaea were more closely related to the eukaryotic nuclear lineage; that is, to the host cell that acquired the mitochondrion 4 . The idea that Archaea and eukaryotes are more closely related to each other than either is to Bacteria depends on analyses suggesting that the root of the tree should be placed on the bacterial stem, or within the Bacteria [5][6][7][8][9][10][11][12] , implying that the prokaryotes-cells that lack a nucleus-are a paraphyletic group 13 . The main question now debated is whether core components of the eukaryotic nuclear lineage descend from a common ancestor shared with Archaea, as in the three-domains tree 14 (Fig.…”

Integrative modeling of gene and genome evolution roots the archaeal tree of life

“…Recently published analyses (9, 10) used a bacterial outgroup to root the archaeal tree, based on the assumption that the root of the universal tree lies between the two prokaryotic domains or within the Bacteria (11)(12)(13)(14)(15). Although outgroup rooting is a widely used approach, it has at least two major difficulties in this context.…”