The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Nat Rev Microbiol 8:743-752

Institut Pasteur, Department of Microbiology, Paris, France.
Nature Reviews Microbiology (Impact Factor: 23.57). 10/2010; 8(10):743-52. DOI: 10.1038/nrmicro2426
Source: PubMed


The origin of eukaryotes and their evolutionary relationship with the Archaea is a major biological question and the subject of intense debate. In the context of the classical view of the universal tree of life, the Archaea and the Eukarya have a common ancestor, the nature of which remains undetermined. Alternative views propose instead that the Eukarya evolved directly from a bona fide archaeal lineage. Several recent large-scale phylogenomic studies using an array of approaches are divided in supporting either one or the other scenario, despite analysing largely overlapping data sets of universal genes. We examine the reasons for such a lack of consensus and consider how alternative approaches may enable progress in answering this fascinating and as-yet-unresolved question.

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    • "However, at least since Reanney (1974) it has been questioned which direction the change occurred—akaryotes to eukaryotes, eukaryotes to akaryotes, or were both forms equally old? The question as to whether eukaryotes are oldest has been raised quite a few times (Carlile 1982; Blake 1983; Forterre 1994; Jeffares et al. 1998; Brinkmann and Philippe 1999; Caetano-Anollés 2002; de Duve 2007; Desmond et al. 2011; Gribaldo et al. 2010) and this 'protoeukaryote' question has never been satisfactorily addressed by advocates of the alternative 'akaryotes old' viewpoint. And they might be correct—but we need to evaluate all the ideas scientifically. "
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    ABSTRACT: The Last Eukaryote Common Ancestor (LECA) appears to have the genetics required for meiosis, mitosis, nucleus and nuclear substructures, an exon/intron gene structure, spliceosomes, many centres of DNA replication, etc. (and including mitochondria). Most of these features are not generally explained by models for the origin of the Eukaryotic cell based on the fusion of an Archeon and a Bacterium. We find that the term 'prokaryote' is ambiguous and the non-phylogenetic term akaryote should be used in its place because we do not yet know the direction of evolution between eukaryotes and akaryotes. We use the term 'protoeukaryote' for the hypothetical stem group ancestral eukaryote that took up a bacterium as an endosymbiont that formed the mitochondrion. It is easier to make detailed models with a eukaryote to an akaryote transition, rather than vice versa. So we really are at a phylogenetic impasse in not being confident about the direction of change between eukaryotes and akaryotes.
    Journal of Molecular Evolution 09/2014; 79(5-6). DOI:10.1007/s00239-014-9643-y · 1.68 Impact Factor
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    • "Yet, the plethora of phylogenetic studies that has tried to resolve this conundrum has thus far failed to reach consensus, prompting some to even speak of a " phylogenomic impasse " (Gribaldo et al. 2010). Clearly, the phylogenomic approaches taken to resolve these deep evolutionary relationships have to be performed with great care as they are prone to all sorts of biases and artifacts (Delsuc et al. 2005; Gribaldo et al. 2010). Some of those, such as compositional bias and varying evolutionary rates (heterotachy ), are inherent in the nature of biological sequence data. "
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    ABSTRACT: The origin of the eukaryotic cell can be regarded as one of the hallmarks in the history of life on our planet. The apparent genomic chimerism in eukaryotic genomes is currently best explained by invoking a cellular fusion at the root of the eukaryotes that involves one archaeal and one or more bacterial components. Here, we use a phylogenomics approach to reevaluate the evolutionary affiliation between Archaea and eukaryotes, and provide further support for scenarios in which the nuclear lineage in eukaryotes emerged from within the archaeal radiation, displaying a strong phylogenetic affiliation with, or even within, the archaeal TACK superphylum. Further taxonomic sampling of archaeal genomes in this superphylum will certainly provide a better resolution in the events that have been instrumental for the emergence of the eukaryotic lineage.
    Cold Spring Harbor perspectives in biology 07/2014; 6(10). DOI:10.1101/cshperspect.a016022 · 8.68 Impact Factor
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    • "In fact, the acceptance of the " canonical " rooting in Bacteria became so deep that it has now prompted the search for the origins of Eukarya in the molecular and physiological constitutions of the putative archaeal sister group [18]. For example, Embley and coworkers generated sequence-based phylogenies using conserved proteins and advanced algorithms to show that Eukarya emerged from within Archaea [19] [20] [21] (refer to [22] for critical analysis). Importantly, these analyses suffer from technical and logical problems that are inherent in sequence-based tree reconstructions. "
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    ABSTRACT: The study of the origin of diversified life has been plagued by technical and conceptual difficulties, controversy, and apriorism. It is now popularly accepted that the universal tree of life is rooted in the akaryotes and that Archaea and Eukarya are sister groups to each other. However, evolutionary studies have overwhelmingly focused on nucleic acid and protein sequences, which partially fulfill only two of the three main steps of phylogenetic analysis, formulation of realistic evolutionary models, and optimization of tree reconstruction. In the absence of character polarization, that is, the ability to identify ancestral and derived character states, any statement about the rooting of the tree of life should be considered suspect. Here we show that macromolecular structure and a new phylogenetic framework of analysis that focuses on the parts of biological systems instead of the whole provide both deep and reliable phylogenetic signal and enable us to put forth hypotheses of origin. We review over a decade of phylogenomic studies, which mine information in a genomic census of millions of encoded proteins and RNAs. We show how the use of process models of molecular accumulation that comply with Weston's generality criterion supports a consistent phylogenomic scenario in which the origin of diversified life can be traced back to the early history of Archaea.
    Archaea 06/2014; 2014(12). DOI:10.1155/2014/590214 · 2.71 Impact Factor
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