Saturday, December 27, 2008

On the Origin of Eukaryotes


The Three Domain Hypothesis
If all you do is read the textbooks, you would think that the origin of eukaryotic cells has been discovered. Most textbooks describe the Three Domain Hypothesis as a done deal. Eukaryotes and archaebacteria share a more recent common ancestor than either group does with the remaining groups of bacteria. Thus, eukaryotes arose from archaebacteria.

The scientific literature does not reflect this confidence. In fact, there is general agreement that the classic Three Domain Hypothesis is no longer viable as a complete explanation for the origin of eukaryotic cells. The current consensus favors a more confused picture of early life with lots of gene swapping—the so-called web of life. It is not clear that eukaryotes as a group arose from any particular prokaryotic clade. It is likely that in addition to horizontal gene transfer, there were probably one or more fusion events where the cells from two separate lineages united to form a hybrid.1

This week's issue of the Proceedings of the National Acedemy of Sciences (USA) has a paper that addresses the problem, one more time. Cox et al. (2008) ask whether there is phylogenetic support for the Three Domain Hypothesis by analyzing 53 well conserved genes. The answer is no. But is there support for one of the alternatives, the Eocyte Hypothesis? The answer is, maybe.2

The commentary by John Archibald is worth reading. Here's an excerpt.
Evolving Views on the Tree of Life

Next to life itself, the origin of complex cells is one of the most fundamental, and intractable, problems in evolutionary biology. Progress in this area relies heavily on an understanding of the relationships between present-day organisms, yet despite tremendous advances over the last half-century scientists remain firmly divided on how to best classify cellular life. Many adhere to the textbook concept of 2 basic types of cells, prokaryotes and eukaryotes, as championed by Stanier and van Niel (7). Others posit that at its deepest level life is not a dichotomy but a trichotomy comprised of cells belonging to the domains Bacteria, Archaea, and Eukarya, each monophyletic and sufficiently distinct from one another to warrant equal status (5, 8). The conceptual and practical challenges associated with establishing a genealogy-based classification scheme for microbes have been fiercely debated for decades (see ref. 9 for recent review), and the literature is rich in philosophy and rhetoric.

The genomics revolution of the 1990s brought tremendous optimism to the field of microbial systematics: if enough genomes from diverse organisms could be sequenced and compared, definitive answers to questions about evolutionary relationships within and between eubacteria, archaebacteria, and eukaryotes would surely emerge. More specifically, it should be possible to discern how eukaryotes evolved from prokaryotes (if indeed that is what happened), and perhaps even who among modern-day prokaryotic lineages is our closest ancestor. Unfortunately, with the sequences of hundreds of eubacterial, archaebacterial, and eukaryotic genomes has come the realization that the number of universally distributed genes suitable for global phylogenetic analysis is frustratingly small (10). Lateral (or horizontal) gene transfer has shown itself to be a pervasive force in the evolution of both prokaryotic and eukaryotic genomes, and even if a “core” set of genes can be identified (and there is much debate on this issue), how confident are we that the phylogenetic signal in these genes reflects the vertical history of cells? How meaningful are sequence alignment-independent, gene content-based approaches to resolving the “tree of life” (11)? To what extent is a “net of life” a more accurate and useful metaphor for describing the full spectrum of life on Earth (10, 12–14)?
The bottom line is that the earliest stages of evolution are still very much open questions. It is wrong to assume that the Three Domain Hypothesis is correct and scientists, as well as textbooks writers, should stop making this assumption.

1. Most workers make the unstated assumption that eukaryotic cells are more recent than prokaryotic cells. The idea that archaebacteria could have arisen by a fusion of an early eukaryote with an early prokaryote is just as consistent with most of the data yet this possibility is almost never discussed.

2. Cox et al. use very "sophisticated" techniques for analyzing their sequence data. Much of the controversy in this field involves disputes over which computer programs give the most accurate results. What's really going on, in my opinion, is that the data isn't good enough to justify the kinds of manipulations that are being done. The trees give you a good approximation of the true phylogeny but subjecting the data to over-analysis isn't helpful.

Archibald, J.M. (2008) The eocyte hypothesis and the origin of eukaryotic cells. Proc. Natl. Acad. Sci. (USA) 105:20049-20050. [doi:10.1073/pnas.0811118106]

Cox, C.J., Foster, P.G., Hirt, R.P., Harris, S.R., and Embley, T.M. (2008) The archaebacterial origin of eukaryotes. Proc. Natl. Acad. Sci. (USA) 105:20356-20361. [doi:10.1073/pnas.0810647105].


  1. Earliest stages of evolution?
    I would have thought we are talking about biological events somewhere in the middle stages of evolution (timewise, at least).

  2. This paper deserves attention. Although it does not claim to be the definitive nail in the three-domain coffin, it's a really good start. Lake's Eocyte hypothesis was based on somewhat flimsy evidence and was a bit ahead of its time. rRNA phylogenies ruled the 80's and 90's. It has taken a long time for new data (e.g., multiple genes from multiple taxa) and advanced methods (e.g., complex mixed-model ML implementations) to emerge.