Archaea and the tree of life

List of participants

Stephen D. Bell, Jonathan Berthon, Céline Brochier-Armanet (organizer), Vincent Daubin, Elie Desmond, Arnold J.-M. Driessen, Laure Eme, Patrick Forterre (organizer), Roger Garrett, J. Peter Gogarten, Simonetta Gribaldo (organizer), Henri Grosjean, Karl-Peter Hopfner, Michel Morange, Gary J. Olsen, Anthony M. Poole, Christa Schleper, John van der Oost, Christiaan van Ooij, Finn Werner, Malcolm F. White

Review

Archaea and the tree of life
by Patrick Forterre
11 – 16 May 2009

In 1977, when he identified the Archaea as being one of the three domains of life, Carl Woese made one of the major discoveries of the XXth century in Biology. Since then, the position of Archaea in the universal tree of life has been the topic of hot debates among evolutionists. The aim of the international meeting « Archaea and the Tree of life » was to discuss this issue, based on the most recent discoveries obtained on the physiology and molecular biology of Archaea. To fulfil this goal, we gathered scientists from two distinct communities: on one side, biochemists and molecular biologists working actively on different archaeal model organisms, and on the other hand several evolutionists expert in comparative genomics and phylogenomics. The underlying idea was to encourage biochemists and molecular biologists to discuss openly their most recent data in an evolutionary context, being aware of the controversies among evolutionists as well as the different contradictory hypothesis they presently propose. In parallel, we also wished to make the evolutionists aware of the most recent data gathered by the biochemists and molecular biologists covering the whole spectrum of archaeal physiology.

The meeting « Archaea and the Tree of life » gathered 21 participants from various countries including a journalist of « Nature Reviews in Microbiology »and a scientific historian and philosopher, Michel Morange.  This meeting was one of a series of colloquia on ancient evolution that started in 1996 with a meeting on the last Universal Common Ancestor (dubbed LUCA during this meeting) and continued in 1999, 2004 and 2006 with meetings on the origin of viruses, the origin of the cellular nucleus, and the tenth anniversary of LUCA, respectively. However, in order to diversify the participation to these fascinating discussions, 15 of the 20 participants of the meeting « Archaea and the Tree of life » had never been invited previously to les Treilles.

Several nice review presentations on various aspects of archaeal molecular biology (cell division, transcription, DNA repair, membrane transport, RNA modification, RNA degradation, metabolism) were presented by some of the world leaders in these fields: Steve Bell (Oxford), Malcom White (Saint Andrew), Henry Grosjean (Orsay), John Van der Ost (Wagenigen), Arnold Driessen (Groningen), Fin Werner (London), Gary Olsen (Urbana), Karl-Peter Hopfner (Munich). These talks emphasized the extensive similarities observed at the molecular level between Archaea and Eukarya. This does not hold simply for informational systems (as currently assumed), but also for operational systems such as cell division, protein secretion or membrane vesicle formation. This last point was dramatically demonstrated by the recent finding that homologues of components of the eukaryotic vesicle-sorting system ESCRTIII are involved in archaeal cell division. Opinions sometimes diverged on the polarization of traits commons to Archaea and Eukarya: are these derived characters testifying for the sisterhood of these two domains, or are these ancestral traits that were lost or replaced in Bacteria? The current trends favours the first hypothesis, but the meeting made aware all participants that this question is still open and that more convincing arguments should be sought for in various molecular mechanisms in order to obtain a consensus on this critical question.

A few participants discussed the nature of the last common ancestor of Eukarya on one side and of the last common ancestor of Archaea on the other. From studying the evolution of the archaeal DNA replication apparatus (Jonathan Berthon, Orsay), of the  mitochondrial  ribosome (Elie Desmond, Paris), and of the eukaryal basal body (Laura Eme, Marseille), it was suggested that these ancestors were at least as complex as their present-day descendants, and even that some streamlining occurred during the subsequent evolution of Archaea and Eukarya. A breakthrough in understanding archaeal evolution was the proposal of a third archaeal phylum, the Thaumarchaeota (Céline Brochier-Armanet, Marseille). Molecular phylogenetic analyses indicate in fact that these archaea may be the first branching lineage in the archaeal tree and would  have conserved a few traits in common with Eukarya that would have been lost in the two other archaeal phyla, the Euryarchaeota and the Crenarchaeota. Data from a newly sequenced genome of Thaumarchaeota that supports the unique phylogenetic status of this archaeal group was presented at the meeting by Christa Schleper (Vienna).

The monophyly of Archaea has been disputed for a long time, some authors having suggested that Crenarchaeota share an exclusive ancestor with Eukarya, whereas others suggested that Eukarya originated from the fusion of a bacterium and an archaeon. Simonetta Gribaldo (Paris) reviewed a number of recent large-scale phylogenomic analyses published on this issue, showing that various authors obtained different results albeit using similar gene datasets. She argued for the need of new approaches to tackle this fundamental question, which remains unresolved. The nature of the universal tree of life and the problem raised (or not) by lateral gene transfers were discussed by several authors such as Peter Gogarten (Halifax), Anthony Poole (Uppsala) and Vincent Daubin (Lyon). The participants agreed that the “tree concept” is still valid, but also argue for a “coral of life” that would emphasize lost branches describing extinct lineages. Lateral gene transfers are not just pitfalls for phylogenies but can be also useful as synapomorphies (i.e. shared derived characters) for the identification of specific clades. Moreover, the stem leading to modern clades should be considered in evolutionary scenarios, especially in the case of the origin of Eukarya.

In previous meetings at Les Treilles, Patrick Forterre (Paris, Orsay) had insisted on the role that viruses might have played in early evolution. The recent discovery of giant viruses, as well as unique viruses infecting Archaea, has revigorated the old debate on the nature of viruses. Patrick Forterre presented at this meeting the discovery in Archaea of a new mechanism for the exit of virions from the infected cell and discussed the “cellular” nature of viruses. Roger Garrett (Copenhagen) emphasized the similarity between plasmids, insertion elements, and the antiviral defence mechanisms (CRISPR) found in Archaea and Bacteria. This is in striking contrast with the clear difference between Archaea and Bacteria at the molecular level. In contrast, although Eukarya resemble Archaea at the molecular level, they have unique viruses (e.g. retrovirus) and viral defence elements (siRNA) that have no counterparts in Archaea. The current evolutionary scenarios connecting Archaea to the Universal Tree of life are all difficult to reconcile with this observation, suggesting that we need more imagination to reconstruct the history of the three domains.

An exciting summary of the meeting was presented the last day by Michel Morange (Paris). He discussed in particular the validity of the various questions raised at the meeting around the notion of “origins” from a philosophical and epistemological viewpoint. As expected, several new collaborations have been initiated at the meeting « Archaea and the Tree of life », especially between molecular biologists and evolutionists. The data presented at the meeting should be published in 2010 in a special issue of the journal Research in Microbiology.

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