Abstract

BackgroundThe recent rise in cultivation-independent genome sequencing has provided key material to explore uncharted branches of the Tree of Life. This has been particularly spectacular concerning the Archaea, projecting them at the center stage as prominently relevant to understand early stages in evolution and the emergence of fundamental metabolisms as well as the origin of eukaryotes. Yet, resolving deep divergences remains a challenging task due to well-known tree-reconstruction artefacts and biases in extracting robust ancient phylogenetic signal, notably when analyzing data sets including the three Domains of Life. Among the various strategies aimed at mitigating these problems, divide-and-conquer approaches remain poorly explored, and have been primarily based on reconciliation among single gene trees which however notoriously lack ancient phylogenetic signal.ResultsWe analyzed sub-sets of full supermatrices covering the whole Tree of Life with specific taxonomic sampling to robustly resolve different parts of the archaeal phylogeny in light of their current diversity. Our results strongly support the existence and early emergence of two main clades, Cluster I and Cluster II, which we name Ouranosarchaea and Gaiarchaea, and we clarify the placement of important novel archaeal lineages within these two clades. However, the monophyly and branching of the fast evolving nanosized DPANN members remains unclear and worth of further study.ConclusionsWe inferred a well resolved rooted phylogeny of the Archaea that includes all recently described phyla of high taxonomic rank. This phylogeny represents a valuable reference to study the evolutionary events associated to the early steps of the diversification of the archaeal domain. Beyond the specifics of archaeal phylogeny, our results demonstrate the power of divide-and-conquer approaches to resolve deep phylogenetic relationships, which should be applied to progressively resolve the entire Tree of Life.

Highlights

  • The recent rise in cultivation-independent genome sequencing has provided key material to explore uncharted branches of the Tree of Life

  • We have shown that a divide-and-conquer approach based on character supermatrices is a reliable and promising approach to successfully resolve deep divergences by combining the phylogenetic signal brought by large supermatrices and at the same time using different sub-samplings of taxa and markers adapted to different parts of the phylogeny

  • Because methanogens are present in both clades, whether the root of the Archaea lies between Cluster I and II or before their divergence from DPANN is of primary importance to infer whether this metabolism was present in the last archaeal common ancestor

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Summary

Introduction

The recent rise in cultivation-independent genome sequencing has provided key material to explore uncharted branches of the Tree of Life. This has been spectacular concerning the Archaea, projecting them at the center stage as prominently relevant to understand early stages in evolution and the emergence of fun‐ damental metabolisms as well as the origin of eukaryotes. Resolving deep divergences remains a challenging task due to well-known tree-reconstruction artefacts and biases in extracting robust ancient phylogenetic signal, notably when analyzing data sets including the three Domains of Life. The recent rise in cultivation-independent genome sequencing has provided key material to explore the socalled ’microbial dark matter’ and led to the discovery of a myriad of new major bacterial and archaeal lineages with unexpected metabolic and ecological features. It revealed that Methanonatronarchaeia, a unique archaeal lineage of extremely halophilic, moderately thermophilic, methyl-reducing methanogens, proposed to represent evolutionary intermediates on the path from methanogens to extreme halophiles due to their supposed close relationships with Halobacteria [28], branch more deeply in the archaeal phylogeny and independently adapted to these environments [29, 30]

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