The growing tree of Archaea: new perspectives on their diversity, evolution and ecology

Abstract

The Archaea occupy a key position in the Tree of Life, and are a major fraction of microbial diversity. Abundant in soils, ocean sediments and the water column, they have crucial roles in processes mediating global carbon and nutrient fluxes. Moreover, they represent an important component of the human microbiome, where their role in health and disease is still unclear. The development of culture-independent sequencing techniques has provided unprecedented access to genomic data from a large number of so far inaccessible archaeal lineages. This is revolutionizing our view of the diversity and metabolic potential of the Archaea in a wide variety of environments, an important step toward understanding their ecological role. The archaeal tree is being rapidly filled up with new branches constituting phyla, classes and orders, generating novel challenges for high-rank systematics, and providing key information for dissecting the origin of this domain, the evolutionary trajectories that have shaped its current diversity, and its relationships with Bacteria and Eukarya. The present picture is that of a huge diversity of the Archaea, which we are only starting to explore.

Figure 1

Number of archaeal genome sequences and validly described archaeal species over the last 20 years. The orange line and histogram indicate respectively the annual and cumulative number of novel archaeal genome sequences (that is, complete genomes, chromosome, contigs and scaffolds) released in public databases (NCBI, latest update December 2016). The blue line and histogram indicate respectively the annual and cumulative number of validly described archaeal species (Source: List of Prokaryotic Names with Standing in Nomenclature with names published until July 2016—http://www.bacterio.net/).

Figure 2

Phylogeny of the Archaea. Bayesian phylogeny (PhyloBayes, CAT+GTR+ Γ4) based on a 41 gene supermatrix (8710 amino acid positions). Scale bar represents the average number of substitutions per site. Node supports refer to posterior probabilities, and ultrafast bootstrap values based on a thousand replicates calculated by maximum likelihood (IQTree, LG+C60). The 41 genes consist of 36 genes from the Phylosift marker genes list (Darling et al., 2014), plus RNA polymerase subunits A and B, and three universal ribosomal proteins (L7-L12, L30, S4) from (Liu et al., 2012). The tree is rooted according to (Raymann et al., 2015), but alternative roots are indicated with numbered red dots (see main text for discussion). Grey font indicates the clades for which no isolates are available. Currently proposed taxonomic status: C=Class; P=Phylum; SC=Super Class; SP=Super Phylum.

Figure 3

Diversity of the DPANN. Unrooted maximum likelihood phylogeny (IQTree, LG+C60) based on concatenation of the same 41 genes as in Figure 2 (9305 amino acid positions). Scale bar represents the average number of substitutions per site. Node supports refer to ultrafast bootstrap values based on a thousand replicates. The tree is only meant to describe the diversity of the DPANN, with at least seven well-supported clades. The question mark represents uncertainty on the relationships among these clades, as well as on the monophyly of the DPANN.

Figure 4

Distribution of marker genes in Archaea. Homologues were searched by Blast and HMM searches against a local database of 646 representative archaeal genomes (one per species). Alignment, phylogenetic analysis and examination of genomic synteny were performed to confirm homology when necessary. To account for the presence/absence of characters in very recent genomes added in public databases, we also checked by Blast on the NCBI. Full circles represent presence in most or all members of the taxon, empty circles absence and partial circles presence in a few members only. It should be noted, however, that absence of genes in uncultured taxa may be due to genomes incompleteness. For the ubiquitin system, we considered presence when at least two out of the three main components were found. For RNA polymerase beta and alpha genes, a single square means a fused gene and two squares a split gene. For primase, a single square means a unitary ‘fused’ primase, and two squares means the classical archaeal two subunit primase (PriS+PriL). Asterisks in the Asgard ESCRT system indicate that they are more similar to eukaryotic than archaeal homologues.