What is an archaeon and are the Archaea really unique?

Abstract

The recognition of the group Archaea as a major branch of the tree of life (ToL) prompted a new view of the evolution of biodiversity. The genomic representation of archaeal biodiversity has since significantly increased. In addition, advances in phylogenetic modeling of multi-locus datasets have resolved many recalcitrant branches of the ToL. Despite the technical advances and an expanded taxonomic representation, two important aspects of the origins and evolution of the Archaea remain controversial, even as we celebrate the 40th anniversary of the monumental discovery. These issues concern (i) the uniqueness (monophyly) of the Archaea, and (ii) the evolutionary relationships of the Archaea to the Bacteria and the Eukarya; both of these are relevant to the deep structure of the ToL. To explore the causes for this persistent ambiguity, I examine multiple datasets and different phylogenetic approaches that support contradicting conclusions. I find that the uncertainty is primarily due to a scarcity of information in standard datasets—universal core-genes datasets—to reliably resolve the conflicts. These conflicts can be resolved efficiently by comparing patterns of variation in the distribution of functional genomic signatures, which are less diffused unlike patterns of primary sequence variation. Relatively lower heterogeneity in distribution patterns minimizes uncertainties and supports statistically robust phylogenetic inferences, especially of the earliest divergences of life. This case study further highlights the limitations of primary sequence data in resolving difficult phylogenetic problems, and raises questions about evolutionary inferences drawn from the analyses of sequence alignments of a small set of core genes. In particular, the findings of this study corroborate the growing consensus that reversible substitution mutations may not be optimal phylogenetic markers for resolving early divergences in the ToL, nor for determining the polarity of evolutionary transitions across the ToL.

The deep(er) roots of Eukaryotes and Akaryotes

“…Both assertions are questionable, since (i) simulated data neither reproduce nor represent empirical distributions, and (ii) poorly resolved trees obscure evolutionary relationships. We argue that Williams et al 4 have overlooked important aspects of assessing phylogenetic signal in empirical data, and that it may be premature to reject a well-supported phylogeny [1][2][3] based on simulated data 4 .…”

“…Models of character evolution are essential to determine the evolutionary relationships of organisms. Phylogenetic models that employ protein structural domains as characters place Asgards as sister to other archaea ( Figure 1a), and archaea sister to bacteria in the "tree of life" (ToL) [1][2][3] . Whereas several analyses that employ amino-acids as characters fail to resolve the archaeal radiation (Figure 1b) or to identify a distinct ancestor of archaea 4 .…”

“…Such simple frequency distributions can be misleading. Careful and rigorous analyses of empirical datasets [1][2][3]8 that demonstrate the robustness of rooting and tree topology against many potential biases were ignored 4 . Here, we would like to clarify certain aspects of the published protein domain-based phylogenies so as to avoid further misunderstandings and to highlight their advantages for phylogenetic reconstruction.…”

“…Williams et al 4 rely on (i) simulated data to reject a robust phylogeny inferred from empirical data ( Figure 1a) that supports the evolutionary kinship of eukaryotes and akaryotes (akaryote 2D-ToL) [1][2][3] ; and (ii) the so-called bacterial rooting to interpret a partially resolved, unrooted-ToL (Figure 1b), asserting that . Different 2D "tree of life" (2D-ToL) variants supported by different types of molecular characters using the best-fitting probability models 1,4 . (a) The rooted tree (phylogeny) inferred by estimating the evolution of species-specific changes in protein domain composition.…”

“…The Asgard archaea are sister to all other archaea, with euryarchaea being the closest relatives. The phylogeny shown is a condensed form obtained after collapsing the clades of the full tree shown previously 1 . (b) The unrooted tree inferred by estimating the evolution of protein/gene-specific changes in amino acid composition.…”