A divide-and-conquer phylogenomic approach based on character supermatrices resolves early steps in the evolution of the Archaea.

Altiarchaea Asgard DPANN Diaforarchaea Root Stygia

Journal

BMC ecology and evolution
ISSN: 2730-7182
Titre abrégé: BMC Ecol Evol
Pays: England
ID NLM: 101775613

Informations de publication

Date de publication:
05 01 2022
Historique:
received: 21 06 2021
accepted: 22 11 2021
entrez: 6 1 2022
pubmed: 7 1 2022
medline: 26 4 2022
Statut: epublish

Résumé

The 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. We 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. We 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.

Sections du résumé

BACKGROUND
The 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.
RESULTS
We 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.
CONCLUSIONS
We 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.

Identifiants

pubmed: 34986784
doi: 10.1186/s12862-021-01952-0
pii: 10.1186/s12862-021-01952-0
pmc: PMC8734073
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1

Informations de copyright

© 2022. The Author(s).

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Auteurs

Monique Aouad (M)

Université de Lyon, Université Lyon 1, CNRS, UMR5558, Laboratoire de Biométrie et Biologie Évolutive, 43 bd du 11 novembre 1918, 69622, Villeurbanne, France.
École Supérieure de Biologie-Biochimie-Biotechnologies, Université Catholique de Lyon, 10 place des archives, 69002, Lyon, France.

Jean-Pierre Flandrois (JP)

Université de Lyon, Université Lyon 1, CNRS, UMR5558, Laboratoire de Biométrie et Biologie Évolutive, 43 bd du 11 novembre 1918, 69622, Villeurbanne, France.

Frédéric Jauffrit (F)

Université de Lyon, Université Lyon 1, CNRS, UMR5558, Laboratoire de Biométrie et Biologie Évolutive, 43 bd du 11 novembre 1918, 69622, Villeurbanne, France.
Technology Research Department, Innovation Unit, bioMérieux SA, Marcy Étoile, France.

Manolo Gouy (M)

Université de Lyon, Université Lyon 1, CNRS, UMR5558, Laboratoire de Biométrie et Biologie Évolutive, 43 bd du 11 novembre 1918, 69622, Villeurbanne, France.

Simonetta Gribaldo (S)

Department of Microbiology, Unit "Evolutionary Biology of the Microbial Cell", UMR2001, Institut Pasteur, Paris, France. simonetta.gribaldo@pasteur.fr.

Céline Brochier-Armanet (C)

Université de Lyon, Université Lyon 1, CNRS, UMR5558, Laboratoire de Biométrie et Biologie Évolutive, 43 bd du 11 novembre 1918, 69622, Villeurbanne, France. celine.brochier-armanet@univ-lyon1.fr.

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