The origin of eukaryotes and the ring of life

The latest issue of Philosophical Transactions of the Royal Society B (Sept. 26, 2015) is devoted to Eukaryotic origins: progress and challenges. There are 16 articles and anyone interested in this subject has to read all of them.

Many (most) of you aren't going to do that so let me try and summarize the problem and the best current ideas on how to solve it. We begin with the introduction to the issue by the editors, Tom Williams, Martin Embley (Williams and Embly, 2015). Here's the abstract ...

The origin of eukaryotic cells is one of the most fascinating challenges in biology, and has inspired decades of controversy and debate. Recent work has led to major upheavals in our understanding of eukaryotic origins and has catalysed new debates about the roles of endosymbiosis and gene flow across the tree of life. Improved methods of phylogenetic analysis support scenarios in which the host cell for the mitochondrial endosymbiont was a member of the Archaea, and new technologies for sampling the genomes of environmental prokaryotes have allowed investigators to home in on closer relatives of founding symbiotic partners. The inference and interpretation of phylogenetic trees from genomic data remains at the centre of many of these debates, and there is increasing recognition that trees built using inadequate methods can prove misleading, whether describing the relationship of eukaryotes to other cells or the root of the universal tree. New statistical approaches show promise for addressing these questions but they come with their own computational challenges. The papers in this theme issue discuss recent progress on the origin of eukaryotic cells and genomes, highlight some of the ongoing debates, and suggest possible routes to future progress.

The problem is that most people think the origin of eukaryotes was solved by Carl Woese when he published the Three Domain Hypothesis. According to the ribosomal RNA tree, eukaryotes and Archaea are sister groups that are distantly related to Eubacteria (see "a" below).

ThemeThe Three Domain Hypothesis
The data doesn't support such a simple interpretation and that's why the Three Domain Hypothesis has been abandoned. We now know that only one-third of the ancient genes in eukaryotes are more closely related to Archaea than to Eubacteria (Bacteria). Most of the genes have closer homologues in Bacteria. That's because eukaryotes arose from a fusion of a primitive archaebacterium and a primitive eubacterium—the Endosymbiotic Hypothesis. The primitive eubacterium became mitochondria and transferred most of its genes to the archaebacterial genome, which became the nuclear genome. (In the beginning, you couldn't tell which genome was going to become the biggest.)

That's the view shown in part "b" of the figure. This is not consistent with the view of eukaryotic origins promoted by Woese and his colleagues.

The other part of the problem has to do with the relationships of the eukaryotic genes that have bacterial homologues. The ones derived from eubacteria map to the alphaproteobacteria branch of the tree indicating that eukaryotes arose, in part, from within the Eubacterial Domain [see Eukaryotic genes come from alphaproteobacteria, cynaobacteria, and two groups of Archaea]. The genes of Archaeal origin should not come from a species of Archaea if the Three Domain Hypothesis is to be preserved, at least in part. But that's not what the latest results show.

There is growing evidence that the Archaeal ancestor in the fusion event came from a branch within the Archaeal Domain. That branch used to be called "Eocytes" but later on it became known as "Crenarchaeota." As more and more Archaeal genomes were sequenced, it became clear that Crenarchaeota were part of a large superphylum that included Thaumarchaeota, Aigarchaeota, and Korarchaeota. The superphylum is named "TACK" after these four groups.The ancient eukaryotic genes that are related to Archaea seem to come from this group.

The best way to describe the origin of eukaryotes is to use the Ring of Life metaphor and that's the subject of a paper by McInerney et al. (2015). The various phylogenetic trees depicting the origin of eukaryotes are shown in a figure from their paper (below). Right now the data strongly supports a Ring of Life ("d") and not any of the other trees. (The second-best tree, showing the phylogeny of most of the ancient eukaryotic genes, isn't even shown in the figure. It would have eukaryotes clustered with Eubacteria.)

You might wonder why anyone bothers to make a fuss about shape of the the phylogeny. It's because how we think about these things influences the way we write and talk about the origin of eukaryotes. For example, those people who were brainwashed convinced by Woese and his colleagues to adopt the Three Domain view of life will often maintain that the most important eukaryotic genes are Archaeal-related (e.g. "information" genes) and thus, the Three Domain view is still the best way to think of eukaryote origins.

McInerney et al. make a good case for rejecting that view. They advocate a "domain-free" view of life.

To conclude, it is clear that eukaryotes cannot be correctly defined as ‘derived’ Archaebacteria, or as ‘derived’ Eubacteria. Indeed, to view eukaryotes as being from either the archaebacterial or the eubacterial lineages is an over-simplification. Each human is derived equally from both parents. They would not exist without a genetic contribution from both, and it does not matter if they look more like their mother or father, or which surname they carry, if any. The reality is that a human only exists as a consequence of a contribution from both parents. Analogously, eukaryotes are equally eubacterial and archaebacterial. A taxonomic debate exists in the literature on the early evolution of life, whereby hypotheses have been suggested to be characterizable either as three-domains or two-domains based (2D versus 3D hypotheses). This characterization inherently assumes the existence of a tree-like pattern of evolution, which is misleading. Because eukaryotes arose from both Archaebacteria and Eubacteria, there are only two (monophyletic) lineages of life: (i) cellular life and (ii) the eukaryotes. Monophyletic eukaryotes are nested within monophyletic life. Eukaryotes make domain-based classifications obsolete and we therefore advocate dismissing the use of this term (which can easily be replaced by the term lineage, for instance) entirely. That is, we advocate a ‘domain-free’ view of the history of life, as debates about whether there should be two domains or three are essentialist and moot. [my emphasis LAM]

In a pluralistic view of cellular life on the planet, we can see that the merging of eubacterial genes with archaebacterial genes gave rise to the halophiles and indeed it made an enormous contribution to the origins of most of the major groups of Archaebacteria. We see that photosynthesis can only be interpreted as a series of gene flows around the prokaryotic and eukaryotic worlds. We see that eukaryotes have arisen as a consequence of major flows between prokaryotes initially (eukaryogenesis), and later, between a prokaryote group and a eukaryotic group (plastid origins) [84].

Life's history is complex and we should not try to simplify it to suit our need for orderly nomenclatural systems.

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James McInerney, J., Pisani, D., O'Connell, M.J. (2015) The ring of life hypothesis for eukaryote origins is supported by multiple kinds of data. Phil Trans. R. Soc. B 370: published online Aug. 31, 2015. [doi: 10.1098/rstb.2014.0323]

Williams, T.A., and Embley, T.M. (2015) Changing ideas about eukaryotic origins. Phil Trans. R. Soc. B 370: published online Aug. 31, 2015. [doi: 10.1098/rstb.2014.0318]