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Evolution of Eukaryotes—Early or Late?

It was inevitable. In this week's Science magazine there is a Letter by Martin, Dagan, Koonin, Dipippo, Gogarten and Lake. They forcefully deconstruct a paper, "Genomics and the Irreducible Nature of Eukaryote Cell" that Kurland, Collins and Penny published last year in Science. There was some popular press that followed the original publication.

The Kurland
et al. article did not—by far—represent the consensus view of scientists working on eukaryotic origins. However, this paper has, until now, gone without much challenge in the literature (although it shows 11 citations at ISI).

Kurland
et al. argued for the (early) emergence of eukaryotes prior to prokaryotes:
"...we favor the idea that the host that acquired the mitochondrial endosymbiont was a unicellular eukaryote predator, a raptor. The emergence of unicellular raptors would have had a major ecological impact on the evolution of the gentler descendants of the common ancestor. These may have responded with several adaptive strategies: They might outproduce the raptors by rapid growth or hide from raptors by adapting to extreme environments. Thus, the hypothetical eukaryote raptors may have driven the evolution of their autotrophic, heterotrophic, and saprotrophic cousins in a reductive mode that put a premium on the relatively fast-growing, streamlined cell types we call prokaryotes."
In essence, complex eukaryotes came first, followed by prokaryotes which evolved by reduction. In today's letter, Martin et al. point out that this is a re-clothed view of eukaryotic evolution that was popular in the early 1980s. At the time, this idea was mostly centered on the origin and evolution of introns, which were assumed by some to be responsible for building the ancestral set of protein-coding genes by exon shuffling (the introns-early view); to be true, massive intron loss must have characterized the (reductive) evolution of prokaryotes. This scenario has since been thoroughly debunked. Although Kurland et al.'s hypothesis includes more than introns, it suffers from the same problems that led to the demise of introns-early.

In their response, Kurland, Collins and Penny insist that:
"...cellular and molecular biology, especially genomics, reveals signs of an ancient complexity of the eukaryotic cell. This new information was not available to older hypotheses for eukaryote origins..."
I don't find Kurland et al.'s arguments any more compelling than when I first encountered them almost twenty years ago. However, it's great to see these important questions being discussed on the pages on Science.

Picture and caption from MSNBC (Lesley Joan Collins/Science).

"This illustration shows a single-celled predator (colored brown), swallowing up much smaller and less complex single-celled bacteria (yellow and green). Researchers say such a predatory eukaryote, nicknamed "Fred the Raptor," would have had "a major ecological impact" during the early stages of cellular evolution."

5 comments:

  1. This is pretty interesting. Why did they choose to say "irreducible nature of eukaryotic cells"? A lot of creationists could misinterpret this paper as support for IC (Irreducible Complexity).

    I'm sorry if you already answered this question in your post: Do the authors of the paper believe that the mitochondrian is an ancestor of a prokaryot?

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  2. anonymous caught onto the "clever" use of words in the Kurland et al. title. Martin et al. are also a bit taken by this and they end their letter with this comment:

    "Finally, and most disturbing, if contemporary eukaryotic cells are truly of "irreducible nature," as Kurland et al.'s title declares, then no stepwise evolutionary process could have possibly brought about their origin, and processes other than evolution must be invoked. Is there a hidden message in their paper?"

    ReplyDelete
  3. It is quite clear that all 3 "urkingdoms", the Eubacterial, the Eukaryotes and the Archaebacteria are all "ancient". The nuclear genes of Eukaryotes, at least the few that I have studied, seem to be quite a bit closer to archaebacteria than to eubacteria.

    It seems wrong to me to claim that any one of the three groups is "older" than the others. They all shared a common ancestor. They more interesting question is why only 3 lineages (as far as we know) survived. In most other diversity radiation, many different lineages survived to go on to create many more.

    Perhaps it is only our bias toward studying the multicellular Eukaryotes that has prevented us from finding unicellular relatives of Eukaryotes, that would represent other branches of the tree of life?

    ReplyDelete
  4. Brian is correct in pointing out the difficulty in using the word "ancient" in describing the major lineages of life. It's an imprecise and confusing relative term that should be used with more care.

    However, I disagree about the possibilty that one or more of these lineages could be "older" than others. It all depends on where the root of tree of life (TOL) is. Suprisingly, this is not a completely resolved issue, although there is little (if any) evidence for the root placement within the Eukaryotes.

    If the TOL root is either within the Eubacteria (for which there is some evidence; see the recent paper from Tom Cavalier Smith in Biology Direct), or if it is between the Eubacteria and Archaebacteria (as the initial studies of Iwabe & Gogarten indicated in 1989), then prokaryotes are indeed "older" than eukaryotes. Regardless of the specific answer here, Eukaryotes evolved "later" than prokaryotes.

    As for "finding unicellular relatives of Eukaryotes, that would represent other branches of the tree of life", there are many researchers--myself included--who are engaged in this. The tree of eukaryotes is comprised significantly of such unicellular organisms (protists). However, the relationships among these lineages remains to be solved--including a clear determination of the deepest branch(es) on the eukaryotic TOL.

    ReplyDelete
  5. And how do Kurland, Collins, and Penny explain the prior existence of complex eukryotes? Or is that just an axiom?

    ReplyDelete

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