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Archaea, 1:353–363
© 2005 Heron Publishing—Victoria, Canada
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Higher-level classification of the Archaea: evolution of methanogenesis and methanogens

Éric Bapteste (1, 2), Céline Brochier (3) and Yan Boucher (4)

1. Department of Biochemistry and Molecular Biology, Dalhousie University, Sir Charles Tupper Building, Halifax, NS, B3H 4H7, Canada / 2. Corresponding author ([email protected]) / 3. EA EGEE (Évolution, Génome, Environnement), Université Aix-Marseille I, Centre Saint-Charles, 13331 Marseille Cedex 3, France / 4. Department of Biological Sciences, Macquarie University, North Ryde, NSW 2109, Australia / Received January 20, 2005; accepted March 29, 2005; published online April 13, 2005

Summary

We used a phylogenetic approach to analyze the evolution of methanogenesis and methanogens. We show that 23 vertically transmitted ribosomal proteins do not support the monophyly of methanogens, and propose instead that there are two distantly related groups of extant archaea that produce methane, which we have named Class I and Class II. Based on this finding, we subsequently investigated the uniqueness of the origin of methanogenesis by studying both the enzymes of methanogenesis and the proteins that synthesize its specific coenzymes. We conclude that hydrogenotrophic methanogenesis appeared only once during evolution. Genes involved in the seven central steps of the methanogenic reduction of carbon dioxide (CO2) are ubiquitous in methanogens and share a common history. This suggests that, although extant methanogens produce methane from various substrates (CO2, formate, acetate, methylated C-1 compounds), these archaea have a core of conserved enzymes that have undergone little evolutionary change. Furthermore, this core of methanogenesis enzymes seems to originate (as a whole) from the last ancestor of all methanogens and does not appear to have been horizontally transmitted to other organisms or between members of Class I and Class II. The observation of a unique and ancestral form of methanogenesis suggests that it was preserved in two independent lineages, with some instances of specialization or added metabolic flexibility. It was likely lost in the Halobacteriales, Thermoplasmatales and Archaeoglobales. Given that fossil evidence for methanogenesis dates back 2.8 billion years, a unique origin of this process makes the methanogenic archaea a very ancient taxon.

Keywords: phylogeny, taxonomy.


ISSN 1472-3654 (Online) ISSN 1472-3646 (Print) Copyright © 2002–2007 Heron Publishing