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Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota

Key Points

  • The archaeal domain is currently divided into two major phyla, the Euryarchaeota and the Crenarchaeota, based on the RNA component of the small ribosomal subunit (SSU rRNA).

  • During the past few years, uncultivated mesophilic crenarchaeota from marine and terrestrial environments have been identifed using PCR amplification of SSU rRNA. These archaea have been affiliated with Crenarchaeota, because they form a sister group of the hyperthermophilic crenarchaeota in SSU rRNA trees.

  • It was recently recognized that uncultivated mesophilic crenarchaeota include ammonium-oxidizers that might have an important role in the global nitrogen cycle.

  • Recently, the first genome sequence of a mesophilic crenarchaeota, Cenarchaeum symbiosum, was completed. This mesophilic 'crenarchaeon' was included in archaeal phylogenies that are based on the concatenation of ribosomal protein sequences.

  • Whereas C. symbiosum and related mesophilic crenarchaeota form a weakly supported sister group of hyperthermophilic crenarchaeota in a tree that combines SSU and large subunit (LSU) rRNA sequences, they have a robust basal position in a tree that is based on a concatenation of ribosomal proteins.

  • Genome mining shows that C. symbiosum lacks the typical crenarchaeal signatures, and instead has several characteristic euryarchaeal signatures.

  • These data indicate that C. symbiosum (and related mesophilic crenarchaeota) are distinct from hyperthermophilic crenarchaeota. We suggest that these ubiquitous archaea should form a third archaeal phylum and propose to name this new phylum Thaumarchaeota (from the Greek 'thaumas', meaning wonder).

Abstract

The archaeal domain is currently divided into two major phyla, the Euryarchaeota and Crenarchaeota. During the past few years, diverse groups of uncultivated mesophilic archaea have been discovered and affiliated with the Crenarchaeota. It was recently recognized that these archaea have a major role in geochemical cycles. Based on the first genome sequence of a crenarchaeote, Cenarchaeum symbiosum, we show that these mesophilic archaea are different from hyperthermophilic Crenarchaeota and branch deeper than was previously assumed. Our results indicate that C. symbiosum and its relatives are not Crenarchaeota, but should be considered as a third archaeal phylum, which we propose to name Thaumarchaeota (from the Greek 'thaumas', meaning wonder).

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Figure 1: Maximum likelihood tree based on the concatenation of 226 SSU and LSU sequences from Archaea and Bacteria.
Figure 2: Maximum likelihood tree based on the concatenation of 53 R proteins from complete archaeal genomes.
Figure 3

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Acknowledgements

The authors thank G. Sezonov for suggesting the name Thaumarchaeota, E. Koonin for unpublished communications and the referees for useful comments and suggestions.

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Correspondence to Céline Brochier-Armanet.

Supplementary information

Supplementary information S1 (Table)

Test of three placements for mesophilic crenarchaeota (PDF 193 kb)

Supplementary information S2 (Table) (PDF 279 kb)

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DATABASES

Entrez Genome Project

Aeropyrum pernix

Caldivirga maquilingensis

Candidatus Methanoregula boonei

Cenarchaeum symbiosum

Halorubrum lacusprofundi

Haloquadratum walsbyi

Hyperthermus butylicus

Ignicoccus hospitalis

Metallosphaera sedula

Methanococcus aeolicus

Methanococcus vannielii

Methanocorpusculum labreanum

Methanoculleus marisnigri

Methanopyrus kandleri

Methanosaeta thermophila

Methanosphaera stadtmanae

Methanospirillum hungatei

Methanothermobacterthermautotrophicus

Nanoarchaeum equitans

Natronomonas pharaonis

Pyrobaculum aerophilum

Pyrobaculum arsenaticum

Pyrobaculum calidifontis

Pyrobaculum islandicum

Staphylothermus marinus

Thermofilum pendens

FURTHER INFORMATION

Céline Brochier-Armanet's homepage

Céline Brochier-Armanet's laboratory website

NCBI COGs database

Glossary

Hyperthermophile

An organism that has an optimal growth temperature of at least 80°C.

Paraphyletic

A group of organisms or sequences that includes an ancestor and some, but not all, of its descendants.

Sister groups

In a phylogeny, two lineages that share an exclusive common ancestor.

Monophyletic group

Includes an ancestor and all its descendants.

Clade

A monophyletic group.

Long-branch attraction artefact

A phylogenetic artefact that is induced by differences in evolutionary rates, and results in the artificial grouping of lineages that have long branches in a phylogenetic tree.

Mesophile

This term is normally restricted to organisms that have optimal growth temperatures of between 20 and 50°C. Here, however, the term mesophilic crenarchaeota is given to all non-hyperthermophilic crenarchaeota, even though some of them (presently uncultivated) are psychrophiles (optimal growth temperature of between O and 20°C) or moderate thermophiles (optimal growth temperature of between 50 and 70°C).

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Brochier-Armanet, C., Boussau, B., Gribaldo, S. et al. Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6, 245–252 (2008). https://doi.org/10.1038/nrmicro1852

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