The origin and evolution of Archaea: a state of the art

Abstract

Environmental surveys indicate that the Archaea are diverse and abundant not only in extreme environments, but also in soil, oceans and freshwater, where they may fulfil a key role in the biogeochemical cycles of the planet. Archaea display unique capacities, such as methanogenesis and survival at temperatures higher than 90 degrees C, that make them crucial for understanding the nature of the biota of early Earth. Molecular, genomics and phylogenetics data strengthen Woese's definition of Archaea as a third domain of life in addition to Bacteria and Eukarya. Phylogenomics analyses of the components of different molecular systems are highlighting a core of mainly vertically inherited genes in Archaea. This allows recovering a globally well-resolved picture of archaeal evolution, as opposed to what is observed for Bacteria and Eukarya. This may be due to the fact that no rapid divergence occurred at the emergence of present-day archaeal lineages. This phylogeny supports a hyperthermophilic and non-methanogenic ancestor to present-day archaeal lineages, and a profound divergence between two major phyla, the Crenarchaeota and the Euryarchaeota, that may not have an equivalent in the other two domains of life. Nanoarchaea may not represent a third and ancestral archaeal phylum, but a fast-evolving euryarchaeal lineage. Methanogenesis seems to have appeared only once and early in the evolution of Euryarchaeota. Filling up this picture of archaeal evolution by adding presently uncultivated species, and placing it back in geological time remain two essential goals for the future.

Figure 1

SSU rRNA archaeal phylogeny (adapted from Schleper et al. 2005). Triangles are proportional to the diversity of groups. Filled triangles represent groups for which cultivated species are available. Empty triangles indicate groups represented only by environmental sequences. Asterisks indicate groups with hyperthermophilic species.

Figure 2

Unrooted maximum-likelihood (ML) trees based on a concatenation of ribosomal proteins (5809 positions) (a) and RNA polymerase subunits and transcription factors (2213 positions) (b) for which no HGTs were detected in individual analyses. For complete details about the individual and concatenated dataset construction see Brochier et al. (2004). The trees were calculated by PHYML (JTT model including a gamma correction (eight discrete classes) with an estimated alpha parameter, and an estimation of the proportion of invariant positions; Guindon & Gascuel 2003). Numbers at nodes are bootstrap values calculated from 1000 replicates by PHYML (Guindon & Gascuel 2003). The scale bar represents the per cent of substitutions per site.

Figure 3

Unrooted ML tree of a concatenation of Srp54 and SRα/FtsY proteins (641 positions). Calculation was made by PHYML as described in the legend to figure 2.

Figure 4

Unrooted ML tree of a concatenation of four exosome subunits (Rrp41, Rrp42, Rrp4 and Cs14, 1224 positions). Calculation was made by PHYML as described in the legend to figure 2.

Figure 5

A consensual phylogeny of the Archaea for which complete genome sequences are available, issued from current phylogenomics evidence.