The rise and fall ofArchezoa

As for Metazoa, advances in phylogenetic analyses have greatly modified our view of the eukaryotic tree. Originally, both morphological (Cavalier-Smith, 1987) and molecular studies (mainly based on rRNA) (Sogin, 1991) suggested that several simple lineages (e.g., devoid of mitochondrion, Golgi apparatus, or

Fig. 8.6. Most common views of the universal tree of life. A. Schematic representation of Woese's paradigm. The root is located on the bacterial branch and the mitochondrial endosymbiosis occurred relatively late during the evolution of eukaryotes. B. Woese's tree corrected for LBA artefacts. Archaea and Bacteria are sister groups, rendering prokaryotes monophyletic. The diversification of extant eukaryotes occurred relatively recently, after the mitochondrial endosymbiosis. C. Genome fusion at the origin of eukaryotes.

Fig. 8.6. Most common views of the universal tree of life. A. Schematic representation of Woese's paradigm. The root is located on the bacterial branch and the mitochondrial endosymbiosis occurred relatively late during the evolution of eukaryotes. B. Woese's tree corrected for LBA artefacts. Archaea and Bacteria are sister groups, rendering prokaryotes monophyletic. The diversification of extant eukaryotes occurred relatively recently, after the mitochondrial endosymbiosis. C. Genome fusion at the origin of eukaryotes.

peroxysome) emerged in a stepwise fashion at the base of eukaryotes, followed by an unresolved multifurcation containing all complex, often multicellular, eukaryotes. The common interpretation of the classical rRNA tree was that these simple groups (e.g., microsporidia, diplomonads, and trichomonads) were the direct descendants of genuinely primitive organisms and represented intermediate stages in the progressive complexification of eukaryotic cells. Hence, they were named Archezoa (Cavalier-Smith, 1987). This suggested that the endosymbiosis with an alpha-proteobacterium that gave rise to mitochondria (see below) had occurred relatively late in the course of eukaryotic evolution (Figure 8.6A). Therefore, the study of eukaryotes that were supposed never to have possessed mitochondria was regarded to be of prime importance for the understanding of early eukaryotic evolution (Sogin, 1991). The observation that hundreds of genes had been transferred from the protomitochondrion to the nucleus (Lang et al., 1999) further underlined the dramatic modification of eukaryotic cells due to the mitochondrial endosymbiosis.

Unfortunately, a wealth of newly established data has been demonstrating more and more solidly that the Archezoa hypothesis is incorrect and that most likely none of the premitochondriate eukaryotes had survived (Embley and Hirt, 1998;

Philippe and Adoutte, 1998). First, the use of advanced reconstruction methods and/or of protein-encoding genes revealed that early rRNA trees (Sogin, 1991) were severely biased by LBA artefacts due to the non-phylogenetic rate signal (Edlind etal., 1996; Philippe, 2000; Silberman etal., 1999; Stiller and Hall, 1999). In fact, the lineages that emerge early in the rRNA tree are simply fast-evolving organisms that are erroneously attracted towards the base by the distant outgroup (Archaea). For example, microsporidia turned out to be highly derived fungi, while they had previously been thought to be genuinely 'primitive' early eukaryotes (Keeling and Fast, 2002). Actually, the correct placement of microsporidia is difficult to recover (Brinkmann et al., 2005) because for most, but not all, of their proteins the non-phylogenetic signal (due to a high evolutionary rate) is stronger than the genuine phylogenetic signal.

8.5.2 Current view of mitochondrial origin and evolution

Since the new phylogenetic scheme places the former Archezoa back into the main eukaryotic radiation (known as the crown), it implies that the last common ancestor of extant eukaryotes (LCAEE) was much more complex than previously thought, i.e., the LCAEE probably presented all features that are typical for the crown group. Therefore, numerous independent secondary simplifications must have occurred to generate simple extant eukaryotes from such a complex common ancestor. For instance, the LCAEE likely contained a large number of spliceosomal introns, which were then massively and independently lost in most lineages (Roy and Gilbert, 2005). Similarly, ex-Archezoa were first interpreted as resulting from multiple mitochondrial losses. Accordingly, nuclear genes of mitochondrial origin found in these organisms would have been transferred to their nucleus before the loss of mitochondria (Clark and Roger, 1995; Germot et al., 1997; Roger et al., 1998). However, remnants of mitochondria, i.e., small double-membrane-bound organelles containing nuclear-encoded mitochondrial proteins, have subsequently been identified in all putatively 'amitochondriate' organisms investigated (Bui et al., 1996; Tovar et al., 1999; Tovar et al., 2003; Williams et al., 2002). This indicates that the previously called 'amitochondriate' organisms are simply lacking 'aerobic respiration', the most prominent function of mitochondria. Indeed, there are other functions performed by mitochondria that have persisted in all anaerobic eukaryotes, such as the synthesis of iron-sulphur clusters in diplomonads (Tovar et al.,2003).

8.5.3 Current view of eukaryotic evolution

Following the rejection of the Archezoa hypothesis, some progress has been achieved in the resolution of deep eukaryotic phylogeny. Consequently, the division of all extant eukaryotes into six major groups has been proposed (Adl et al., 2005; Keeling et al., 2005; Patterson, 1999; Simpson and Roger, 2004). Some of these supergroups are solidly established, i.e., Opisthokonta (animals, choanoflagellates, and fungi) and Plantae (all three primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes). Moreover, there is accumulating evidence for both Amoebozoa (containing a large part of amoebas, e.g., Dictyostelium and Entamoeba) and Chromalveolata (alveolates, stramenoplies, haptophytes, and cryptophytes); however, a final test based on the analysis of the phylogenomic data set containing representatives from all major lineages from this supergroup is still missing. The support for the monophyly of the two remaining groups (Excavata and Rhizaria) is much more tenuous and definitively requires more sequence data in the form of genome or expresseq sequence tag (EST) projects. Finally, it is noteworthy that anaerobic/amitochondriate species appear to be found in most of the six supergroups.

8.5.4 Philosophical grounds for the rejection of secondary simplification

Despite the aforementioned progress in eukaryotic phylogeny, the classical view, essentially rRNA-based, still largely prevails. Hence, we will try to explain why it is so difficult to obliterate, even in light of convincing evidence. The traditional taxonomy has been influenced by the assumption that the evolution of life was a steady rise to higher complexity, starting from 'primitive' or 'lower' (i.e., simple) organisms and ending with 'evolved' or 'higher' (i.e., complex) forms, especially humans. This conception is actually pre-Darwinian and can be traced back to Aristotle's Scala Naturae, the great chain of being (Nee, 2005). As a result, organisms having an apparently simple morphology were naturally located at the base of the tree of life. In contrast, all recent molecular phylogenetic studies demonstrate that secondary simplification constitutes a major evolutionary trend, encountered at all taxonomic levels. While this conclusion had already been drawn 60 years ago by André Lwoff (1943), its very slow acceptance by the scientific community was remarkably predicted in the very same book. Briefly, the idea of complexification is tightly linked to the concept of progress through the implicit equation 'progress = evolution towards more complexity'. Consequently, the simplification process has always been affected by a strong negative connotation tending to its denial (Lwoff, 1943). From a sociological point of view, it should be noted that the rediscovery of simplification occurred concomitantly with serious criticisms of the ideology of progress. Nevertheless, emphasizing simplification does not deny that complexification did occur, but rather means that both processes should be taken into account for the reconstruction of the evolutionary past (Forterre and Philippe, 1999; Gould, 1996).

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