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The hybrid nature of the Eukaryota and a consilient view of life on Earth

Nature Reviews Microbiology volume 12, pages 449–455 (2014)Cite this article

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Abstract

The origin of the eukaryotic cell, which is known as eukaryogenesis, has puzzled scientists for more than 100 years, and many hypotheses have been proposed. Recent analyses of new data enable the safe elimination of some of these hypotheses, whereas support for other hypotheses has increased. In this Opinion article, we evaluate the available theories for their compatibility with empirical observations and conclude that cellular life consists of two primary, paraphyletic prokaryotic groups and one secondary, monophyletic group that has symbiogenic origins — the eukaryotes.

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Figure 1: Competing scenarios for the origin of the eukaryotes and the highest-level structure for describing the diversity of cellular life.
Figure 2: The ring of life hypothesis.

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Acknowledgements

The authors acknowledge Science Foundation Ireland research Frontiers Program (EOB2673) to M.J.O'C., (EOB3106) to D.P. and J.O.M. and Fulbright Commission for Fulbright Scholarship to M.J.O'C.

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Authors and Affiliations

  1. Department of Biology, Bioinformatics and Molecular Evolution Unit, National University of Ireland, Maynooth, County Kildare, Ireland

    James O. McInerney

  2. Bioinformatics and Molecular Evolution Group, School of Biotechnology, Dublin City University, Glasnevin, 9, Dublin, Ireland

    Mary J. O'Connell

  3. School of Biological Sciences and School of Earth Sciences, University of Bristol, Woodland Road, Bristol, BS8 1UG, UK

    Davide Pisani

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  1. James O. McInerney
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Correspondence to James O. McInerney.

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PowerPoint slides

Glossary

Among-site rate variation

A term used to describe the fact that different nucleotide or amino acid positions in a molecular sequence can change at different rates. This is usually caused by variation in selection pressure, although it may also be caused by variation in mutation rate.

CAT mixture model

A phylogenetic model that assumes that alignment positions might evolve according to different processes. The number of processes, the equilibrium frequencies of amino acids and the assignation of sites to categories are all free parameters of this model.

Eocyte hypothesis

A hypothesis relating to nucleocytosolic genes in eukaryotes that evolutionary history has placed within the Archaebacteria in a sister-group relationship with 'Eocyte' archaebacteria. This Eocyte hypothesis implies that the Archaebacteria are not a monophyletic taxon and that eukaryotes arose from within the Archaebacteria.

Evolutionary parsimony

(Also known as 'Lakes invariants'). A method of resolving a four-taxon problem. A set of equations calculate three invariants — one for each topology. For the correct phylogenetic tree, the invariant is non-zero, whereas the invariant is zero for the other two topologies.

Heterogeneous models

Phylogenetic models that allow for different evolutionary processes in different parts of the data and evolutionary history. Heterogeneity can be allowed in evolutionary rates and sequence composition.

Homogeneous model

A phylogenetic model that implies that there has been a constant rate of evolution, a constant sequence composition, or both, for the duration of the evolutionary history of the sequences that are under consideration.

Maximum parsimony

A method that prefers phylogenetic trees that minimize the number of substitutions required to explain the observed distribution of character states in a data set.

Neighbour joining

A fast clustering approach to infer phylogenetic trees based on distance matrices that have been derived from alignments.

Node discrete compositional heterogeneity model

A model that allows different branches of a phylogenetic tree to evolve using different sequence compositions. Composition vectors are distributed throughout the tree and their placement is calculated as part of the optimization process.

Nucleomorph

A vestigial eukaryotic nucleus thought to be descended from algae that were themselves engulfed by other eukaryotes. Therefore, nucleomorphs represent secondary endosymbiotic events.

Ring of life hypothesis

A proposal that eukaryotic genomes are composed of genes that have two separate sources — one from within the Eubacteria and one from within the Archaebacteria — effectively creating a ring of life, not a tree of life.

Sequence similarity network

A network that consists of nodes that can either represent genes or genomes; the edges that connect these nodes are statements of homology. Therefore, the basic unit of a gene similarity network is a pair of nodes connected by an edge; however, these networks can be very large, consisting of connected components that embed thousands, or even millions, of nodes.

Symbiogenic

A term used to describe the merging of two separate organisms to form one new organism.

TACK group

A group of Archaebacteria that consists of four smaller groups (equivalent to phyla); these are the Thaumarchaeota, the Aigarchaeota, the Crenarchaeota and the Korarchaeota.

Three-domains hypothesis

A hypothesis that depicts the Eukaryota, the Eubacteria and the Archaebacteria as three monophyletic groups, generating a three-domains tree of life. This topology is generally recovered using nucleocytosolic informational proteins and homogeneous models of sequence evolution.

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McInerney, J., O'Connell, M. & Pisani, D. The hybrid nature of the Eukaryota and a consilient view of life on Earth. Nat Rev Microbiol 12, 449–455 (2014). https://doi.org/10.1038/nrmicro3271

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