Rooting the Domain Archaea by Phylogenomic Analysis Supports the Foundation of the New Kingdom Proteoarchaeota

Abstract

The first 16S rRNA-based phylogenies of the Archaea showed a deep division between two groups, the kingdoms Euryarchaeota and Crenarchaeota. This bipartite classification has been challenged by the recent discovery of new deeply branching lineages (e.g., Thaumarchaeota, Aigarchaeota, Nanoarchaeota, Korarchaeota, Parvarchaeota, Aenigmarchaeota, Diapherotrites, and Nanohaloarchaeota) which have also been given the same taxonomic status of kingdoms. However, the phylogenetic position of some of these lineages is controversial. In addition, phylogenetic analyses of the Archaea have often been carried out without outgroup sequences, making it difficult to determine if these taxa actually define lineages at the same level as the Euryarchaeota and Crenarchaeota. We have addressed the question of the position of the root of the Archaea by reconstructing rooted archaeal phylogenetic trees using bacterial sequences as outgroup. These trees were based on commonly used conserved protein markers (32 ribosomal proteins) as well as on 38 new markers identified through phylogenomic analysis. We thus gathered a total of 70 conserved markers that we analyzed as a concatenated data set. In contrast with previous analyses, our trees consistently placed the root of the archaeal tree between the Euryarchaeota (including the Nanoarchaeota and other fast-evolving lineages) and the rest of archaeal species, which we propose to class within the new kingdom Proteoarchaeota. This implies the relegation of several groups previously classified as kingdoms (e.g., Crenarchaeota, Thaumarchaeota, Aigarchaeota, and Korarchaeota) to a lower taxonomic rank. In addition to taxonomic implications, this profound reorganization of the archaeal phylogeny has also consequences on our appraisal of the nature of the last archaeal ancestor, which most likely was a complex organism with a gene-rich genome.

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

“…Comparison of the results obtained from the Archaea/eukaryote (A/E) and the Archaea/Bacteria (A/B) datasets robustly indicates that eukaryotes are sister to the TACK superphylum but also that this topology is strongly linked to a root for the tree of the Archaea lying within the Euryarchaeota. This topology is in contrast to the traditional root between Euryarchaeota and the TACK superphylum (17,18), which we demonstrate as likely being the product of an artifact resulting from the combination of noise introduced by fast-evolving positions and the use of an overly simplistic evolutionary model.…”

“…In particular, the emergence of important archaeal metabolic capabilities and their subsequent evolution will need to be reinvestigated, as the outcomes could have an important impact on our understanding of the emergence of key biochemical cycles and the nature of early Earth. For instance, the deep branching of Methanobacteriales and Methanococcales in Cluster I and the suggestion that the ancestor of Cluster II was a methanogen (30) A B would indicate that this key metabolism was already present in the last archaeal common ancestor, and is therefore older than what may be inferred from traditionally rooted phylogenies of the Archaea (18,21). Also, the inference of ancestral optimal growth temperatures and their changes along archaeal diversification (31, 32) should be reconsidered.…”

Early Microbial Evolution: The Age of Anaerobes

“…The reason is that one of us reported the first concatenated trees using that specific data set 15 years ago (Hansmann and Martin 2000), overlooked in Ciccarelli et al's (2006) "automated" procedure to produce a tree of life that found the same proteins, and it was immediately apparent that there are many, many saturated sites in the alignments of that data set, and that if we start removing the saturated sites or those lacking observable sequence conservation then we obtain different topologies. Investigators are still using such site stripping approaches today (Petitjean et al 2015;Raymann et al 2015), sometimes pruning alignments by hand (Spang et al 2015), but the problem is that there is no good justification for when to stop excluding either genes or sites, one just gets different likelihoods. With large concatenated data sets, the results become dependent on which fraction of the data one retains in the alignment and which model one uses to infer the tree, as seen in the Petitjean et al (2015) analysis in which the archaeal root changed from being within methanogenic lineages to being between the euryarchaeota and TACK groups after pruning.…”

“…Investigators are still using such site stripping approaches today (Petitjean et al 2015;Raymann et al 2015), sometimes pruning alignments by hand (Spang et al 2015), but the problem is that there is no good justification for when to stop excluding either genes or sites, one just gets different likelihoods. With large concatenated data sets, the results become dependent on which fraction of the data one retains in the alignment and which model one uses to infer the tree, as seen in the Petitjean et al (2015) analysis in which the archaeal root changed from being within methanogenic lineages to being between the euryarchaeota and TACK groups after pruning. There is also the problem that concatenation entails an assumption that the concatenated genes in question all share the same evolutionary history, which is actually very hard to show for real data spanning the bacterial -archaeal divide.…”

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

“…These lineages are of major ecological and evolutionary significance and include the Thaumarchaeota (2, 3), ammonia oxidizers found in soils and the open ocean, where they play a critical role in the global nitrogen cycle (3); the DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, Nanohaloarchaea) Archaea, a diverse group with small cells and genomes, whose reduced metabolic repertoires suggest that they may be symbionts or parasites of other prokaryotes (4,5); and the "Asgard" Archaea, the closest archaeal relatives of eukaryotes described to date (6,7), whose phylogenetic position and gene content are key to ongoing debates about eukaryote origins. In recent years, phylogenetic analyses have supported a clade uniting the Thaumarchaeota, Crenarchaeota, Aigarchaeota, and Korarchaeota that has been informally named the "TACK" Archaea (8) or "Proteoarchaeota" (9). The deeper relationships between the major archaeal lineages, and the root of the archaeal tree, remain matters of debate, however.…”