The Evolution of Eukaryotes

Martin, William; Koonin, Eugene V.; DiPippo, Jonathan L.; Gogarten, J. Peter; Lake, James A.

doi:10.1126/science.316.5824.542c

Cited by 27 publications

(28 citation statements)

References 27 publications

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“…The extreme complexity of the eukaryotic cellular organization compared with that of archaeal and bacterial (collectively, prokaryotic) cells cries for an evolutionary explanation and even has brought the specter of "irreducible complexity" into the scientific debate (Kurland et al 2006;Martin et al 2007). The "standard model" derived primarily from the classic phylogenetic analysis of 16S RNA by Woese and coworkers has eukaryotes as the sister group of Archaea, to the exclusion of Bacteria (Woese et al 1990;Pace 1997Pace , 2006Pace , 2009.…”

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confidence: 99%

“…The parsimonious scenario of eukaryogenesis that takes into account the ancestral presence of mitochondria in eukaryotes and the hybrid composition of the eukaryotic gene complement seems to be that the first eukaryote emerged through the invasion of an archaeon by an a-proteobacterium (Martin and Muller 1998;Rivera and Lake 2004;Martin and Koonin 2006;Martin et al 2007). Under this scenario, a plausible chain of events has been proposed leading from the endosymbiosis to the evolution of eukaryotic innovations such as the endomembrane system including the nucleus and the cytoskeleton (Koonin 2006;Martin and Koonin 2006).…”

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confidence: 99%

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The Dispersed Archaeal Eukaryome and the Complex Archaeal Ancestor of Eukaryotes

Koonin

Yutin

2014

Cold Spring Harbor Perspectives in Biology

101

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The ancestral set of eukaryotic genes is a chimera composed of genes of archaeal and bacterial origins thanks to the endosymbiosis event that gave rise to the mitochondria and apparently antedated the last common ancestor of the extant eukaryotes. The proto-mitochondrial endosymbiont is confidently identified as an a-proteobacterium. In contrast, the archaeal ancestor of eukaryotes remains elusive, although evidence is accumulating that it could have belonged to a deep lineage within the TACK (Thaumarchaeota, Aigarchaeota, Crenarchaeota, Korarchaeota) superphylum of the Archaea. Recent surveys of archaeal genomes show that the apparent ancestors of several key functional systems of eukaryotes, the components of the archaeal "eukaryome," such as ubiquitin signaling, RNA interference, and actin-based and tubulin-based cytoskeleton structures, are identifiable in different archaeal groups. We suggest that the archaeal ancestor of eukaryotes was a complex form, rooted deeply within the TACK superphylum, that already possessed some quintessential eukaryotic features, in particular, a cytoskeleton, and perhaps was capable of a primitive form of phagocytosis that would facilitate the engulfment of potential symbionts. This putative group of Archaea could have existed for a relatively short time before going extinct or undergoing genome streamlining, resulting in the dispersion of the eukaryome. This scenario might explain the difficulty with the identification of the archaeal ancestor of eukaryotes despite the straightforward detection of apparent ancestors to many signature eukaryotic functional systems.

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confidence: 99%

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confidence: 99%

The Dispersed Archaeal Eukaryome and the Complex Archaeal Ancestor of Eukaryotes

Koonin

Yutin

2014

Cold Spring Harbor Perspectives in Biology

101

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“…In particular, the events that led to the emergence of Eukaryotes, and their relatedness to the other two domains, remain highly controversial (3)(4)(5)(6)(7)(8). Progress in this area requires both methodological development and the integration of new kinds of information that have previously not been used.…”

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confidence: 99%

“…[24][25][26] (but see ref. 5). Eukaryotes have also been proposed to have arisen autogenously from different eubacterial lineages, including actinobacteria (27) and the planctomyceteverrumicrobia-Chlamydia group (28)(29)(30) (but see ref.…”

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confidence: 99%

Gene similarity networks provide tools for understanding eukaryote origins and evolution

Alvarez‐Ponce

Lopez

Bapteste

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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The complexity and depth of the relationships between the three domains of life challenge the reliability of phylogenetic methods, encouraging the use of alternative analytical tools. We reconstructed a gene similarity network comprising the proteomes of 14 eukaryotes, 104 prokaryotes, 2,389 viruses and 1,044 plasmids. This network contains multiple signatures of the chimerical origin of Eukaryotes as a fusion of an archaebacterium and a eubacterium that could not have been observed using phylogenetic trees. A number of connected components (gene sets with stronger similarities than expected by chance) contain pairs of eukaryotic sequences exhibiting no direct detectable similarity. Instead, many eukaryotic sequences were indirectly connected through a "eukaryote-archaebacterium-eubacterium-eukaryote" similarity path. Furthermore, eukaryotic genes highly connected to prokaryotic genes from one domain tend not to be connected to genes from the other prokaryotic domain. Genes of archaebacterial and eubacterial ancestry tend to perform different functions and to act at different subcellular compartments, but in such an intertwined way that suggests an early rather than late integration of both gene repertoires. The archaebacterial repertoire has a similar size in all eukaryotic genomes whereas the number of eubacteriumderived genes is much more variable, suggesting a higher plasticity of this gene repertoire. Consequently, highly reduced eukaryotic genomes contain more genes of archaebacterial than eubacterial affinity. Connected components with prokaryotic and eukaryotic genes tend to include viral and plasmid genes, compatible with a role of gene mobility in the origin of Eukaryotes. Our analyses highlight the power of network approaches to study deep evolutionary events.mobile genetic elements | cellular evolution | network analysis | organelles | recombination

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“…However, the evolutionary relationships between these three domains of life are still hotly debated (Dagan and Martin, 2006;Kurland et al, 2006;Martin et al, 2007;Kurland et al, 2007). Specifically, there is still no agreement neither on where the "root" of the tree of life lies nor on the origin of eukaryotes.…”

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confidence: 99%

Evolution of protein families: Is it possible to distinguish between domains of life?

Sales‐Pardo

Chan

Amaral

et al. 2007

Gene

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Understanding evolutionary relationships between species can shed new light into the rooting of the tree of life and the origin of eukaryotes, thus, resulting in a long standing interest in accurately assessing evolutionary parameters at time scales on the order of a billion of years. Prior work suggests large variability in molecular substitution rates, however, we still do not know whether such variability is due to species-specific trends at a genomic scale, or whether it can be attributed to the fluctuations inherent in any stochastic process. Here, we study the statistical properties of gene and protein family sizes in order to quantify the long time scale evolutionary differences and similarities across species. We first determine the protein families of 209 species of bacteria and 20 species of archaea. We find that we are unable to reject the null hypothesis that the protein family sizes of these species are drawn from the same distribution. In addition, we find that for species classified in the same phylogenetic branch or in the same lifestyle group, family size distributions are not significantly more similar than for species in different branches. These two findings can be accounted for in terms of a dynamical birth, death, and innovation model that assumes identical protein family evolutionary rates for all species. Our theoretical and empirical results thus strongly suggest that the variability empirically observed in protein family size distributions is compatible with the expected stochastic fluctuations for an evolutionary process with identical genomic evolutionary rates. Our findings hold special importance for the plausibility of some theories of the origin of eukaryotes which require drastic changes in evolutionary rates for some period during the last two billion years.

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The Evolution of Eukaryotes

Cited by 27 publications

References 27 publications

The Dispersed Archaeal Eukaryome and the Complex Archaeal Ancestor of Eukaryotes

The Dispersed Archaeal Eukaryome and the Complex Archaeal Ancestor of Eukaryotes

Gene similarity networks provide tools for understanding eukaryote origins and evolution

Evolution of protein families: Is it possible to distinguish between domains of life?

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