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

Kasie Raymann, Céline Brochier-Armanet, and Simonetta Gribaldo
PNAS May 26, 2015 112 (21) 6670-6675; published ahead of print May 11, 2015 https://doi.org/10.1073/pnas.1420858112

  1. Edited by W. Ford Doolittle, Dalhousie University, Halifax, NS, Canada, and approved April 17, 2015 (received for review November 02, 2014)

Significance

An archaeal origin for eukaryotes is an exciting recent finding. Nevertheless, it has been based largely on the reconstruction of universal trees. The use of an alternative strategy based on markers shared between Archaea and eukaryotes and Archaea and Bacteria bypasses potential problems linked to the analysis of the three domains simultaneously. Comparison of the phylogenies obtained by these two complementary sets of markers supports a sister relationship between eukaryotes and the Thaumarchaeota/“Aigarchaeota” (candidate phylum)/Crenarchaeota/Korarchaeota lineage but also robustly indicates a root of the tree of Archaea that challenges the traditional topology of this domain. This sensibly changes our perspective of the ancient evolution of the Archaea, early life, and Earth.

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.

Footnotes

  • ↵1To whom correspondence should be addressed. Email: simonetta.gribaldo{at}pasteur.fr.

  • Author contributions: C.B.-A. and S.G. designed research; K.R. performed research; K.R., C.B.-A., and S.G. analyzed data; and K.R., C.B.-A., and S.G. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1420858112/-/DCSupplemental.

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Eukaryotic origins and the roots of Archaea
Kasie Raymann, Céline Brochier-Armanet, Simonetta Gribaldo
Proceedings of the National Academy of Sciences May 2015, 112 (21) 6670-6675; DOI: 10.1073/pnas.1420858112
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