Wednesday, February 23, 2011

What Does "Prokaryote" Mean?

I've prepared a bunch of exam questions for students in my molecular evolution course. I gave them out two weeks before the exam and I promised them that I would post some of these questions on my blog to see how you would answer them. I'm hoping that you, dear readers, will show my students that there really is some controversy.

Here's the fourth question.
Norman Pace (2006) says,
I believe it is critical to shake loose from the prokaryote/eukaryote concept. It is outdated, a guesswork solution to an articulation of biological diversity and an incorrect model for the course of evolution. Because it has long been used by all texts of biology, it is hard to stop using the word, prokaryote. But the next time you are inclined to do so, think what you teach your students: a wrong idea.
Outline the main reasons why Pace wants to ban the word “prokaryote.” Do you agree with him?
My students have a copy of the Nature article and we've also discussed the Three Domain Hypothesis. You can learn about some of the controversy at The Three Domain Hypothesis.

Norman Pace is currently Distinguished Professor of Molecular, Cellular and Developmental Biology at the University of Colorado, Boulder.

Part of this discussion is about taxonomy and the proper way to classify organisms. We didn't talk about that in class but for completeness here's what Ernst Mayr has to say about Pace's idea (Mayr, 1998).
In contrast to a Hennigian cladification, the Darwinian classification uses two sets of criteria. Although all taxa must be monophyletic, that is, descended from the nearest common ancestor, they are ranked according to the degree of difference from each other. Therefore, one must ask, are the archaebacteria as different from the eubacteria as from the eukaryotes or are they much more similar to the eubacteria, thus justifying the inclusion of both kinds of bacteria in the prokaryotes and confirming the two-empire classification?


Mayr, E. (1999) Two empires or three? Proc. Natl. Acad. Sci. (USA) 95:9720-0723. [PNAS Free PDF]

Pace, N.R. (2009) Time for a change. Nature 441:289. [doi:10.1038/441289a]

18 comments :

  1. I have switched to the antikaryote camp.

    ReplyDelete
  2. Taxonomic debates are silly. No classification can ever faithfully reflect real world and is by necessity always arbitrary to some extent. So the guiding principle of taxonomy should be practicality. Just agree on some convention and get it over with. Using the term prokaryote does not in any way preclude "understanding the course of evolution at the most fundamental level".

    ReplyDelete
  3. All Microbiology textbooks I know classify living beings in 3 domains.
    And I don't agree with Pace.

    Despite the differences in membrane, cell wall, gene transcription and others, there are many important similarities between Archaea and Bacteria. For instance, cells of both Archaea and Bacteria do not have a defined nucleus and carry 70S rRNA. There are no organelles too. Are these negligible features?

    Furthermore, modern classification of bacteria is based on 16S rRNA. Can you be sure there was not rRNA lateral transfer between Bacteria and Archaea?

    Norman Pace also said that Carl Woese is the greatest biologist since Darwin. I Don't agree with that too.

    ReplyDelete
  4. Ben says,

    All Microbiology textbooks I know classify living beings in 3 domains.

    Sorry to hear that. Do they mention that the Three Domain Hypothesis conflicts with a great deal of evidence?

    ReplyDelete
  5. Taxonomic debates are silly. No classification can ever faithfully reflect real world and is by necessity always arbitrary to some extent.

    Not if you stick to monophyletic groups. (Note that Mayr actually means monophyletic and paraphyletic when he says "monophyletic".)

    I'm certainly against having Prokarya as a taxon, but I don't feel so strongly about the vernacular use of the term (I'm far too ignorant about the Archaea), though I agree with many of the points Pace makes in the paper showing that the term is misused. He notes that the so-called "prokaryotic transcription" and "prokaryotic protein synthesis" do not exists, as those things happen differently in Archaea and Bacteria.

    ReplyDelete
  6. From Mayr's paper:

    Although recent studies, particularly molecular analyses, have shown that the Protista are a very heterogeneous assemblage, consisting of single-celled algae (formerly plants), protozoans (formerly animals), water molds (formerly fungi), and members of many other groups, it is still convenient to speak of unicellular eukaryotes in the vernacular as protists.

    Makes me think Mayr cared very little about the "protists". Why would anyone want to talk about a group that includes incomplete linages of organisms, some with cellular wall, some and without it (some of those amoeboid); some photosynthetic, and some not; some shelled, and some not; some colonial, some not; only grouped for being eukaryotes and non-multicellular? Is that a really useful "grade"? I don't think it is useful unless you don't really want to talk about them. I suspect much of the same happens with the "prokaryotes", though I'm too ignorant of their diversity to actually defend that case.

    ReplyDelete
  7. No, Larry. One of the best and most widely used microbiology textbooks- Brock, does not say a word about the controversy. No mention to Ernst Mayr or Lynn Margulis that dispute the three-domain classification.
    At least they still maintain that both Archaea and Bacteria are prokaryotes.

    "Sorry to hear that. Do they mention that the Three Domain Hypothesis conflicts with a great deal of evidence?"

    ReplyDelete
  8. Not if you stick to monophyletic groups.

    Whatever you decide to stick to would still have to be arbitrary at some point. Fuzzy sets and all. Cf. "species".

    ReplyDelete
  9. I tend to think that prokaryote and eukaryote are general terms for different ways cell are structured, with eukaryotes having compartments completely enclosed by membranes and prokaryotes lacking such compartments (although recognizing that some certainly at least have partial compartments.) I teach (my non-majors even) about the problem with the 3-domain system and I use Doolittle's Sci-Am figure to illustrate the problem. When dealing with cell origins, I teach both about the membrane-infolding and endosymbiosis hypotheses and briefly about what the evidence has to say about them.

    ReplyDelete
  10. DK,

    Whatever you decide to stick to would still have to be arbitrary at some point. Fuzzy sets and all. Cf. "species".

    Ah... species is another problem; I'm thinking of higher taxa.

    Let me reply again to your comments.

    No classification can ever faithfully reflect real world...

    True, but it can reflect the best of our knowledge. Isn't that desirable?

    ...and is by necessity always arbitrary to some extent.

    and Fuzzy sets and all.

    I wasn't entirely clear. If you use the Linnaean system you will get ambiguous situations and "fuzzy-like" groups, even if you limit yourself to monophyletic groups. But if you use the phylogenetic system and define taxon names using phylogenetic nomenclature group membership will be resolved straightforwardly from your phylogenetic hypothesis). Clades are real and exist independently of our opinions. You get to decide what clades to name and what names you choose, that is arbitrary, but I don't see much of a problem with it. The classification itself is not arbitrary, as it's supposed to map the One True Phylogeny (TM).

    ReplyDelete
  11. I'm not yet convinced Eubacteria are not paraphyletic*; if they are (as one would expect considering the cell biology and evolution of those things), then the Archaea no longer deserve any special "domain" status, since the divergence between things like, say, proteobacteria and cyanobacteria, would be deeper and more significant. In that case, it would make make perfect sense to categorise things into euk/proke, since it's just convenient. But, phylogeny aside, as a cell biologist – the difference in cell structure between a prokaryote and a eukaryote is perhaps among the most profound distinctions between any two groups in the living world. (Archaeans are NOT as special as many love to profess) Thus, it is perfectly justifiable to keep using those terms, and I, for one, will continue doing so.

    Lastly, maybe I'll pay more attention to bacteriologists once they recognise those of us studying microbial eukaryotes as fellow microbiologists, and stop using the term solely for prokaryotic microbes (while claiming it entails both). Until then, we can justifiably ignore their whining ;p

    *to my knowledge, the devout belief in monophyly comes from Woese's SSU trees, which are very, very fallible (particularly in our area of the tree – ie protists). There's also huge potential for significant artefacts from the fact we're trying to resolve divergences that may be at least a couple billion years old. There's no strong molecular support for paraphyly either that I know of, but I wish people would stop simply assuming Woese's Three Domains without any questioning. /rant
    (To show that I'm not cookoo, or at least not alone in being so, see Cavalier-Smith 2006 Phil Trans R Soc B (and others ) for a more detailed argument)

    ReplyDelete
  12. @Physeter "Protist" is still a very useful term for political reasons. If we disband 'Protistology' to 'non-Animal/Plant/Fungal Eukaryotic biology', it just becomes awkward; mixing us in with the rest of eukaryote-studying biologists would make us effectively disappear in the vastness of non-protistologists, and many of the individual supergroups, eg Rhizaria and Excavata, are too damn little known by those outside the field to warrant being their own subjects. So while we recognise our field is rather paraphyletic, the phylogenetic distance is easily overcome by the bonds that tie a small group of people who study a fascinating subject the vast majority has never even heard of...

    At least it's not polyphyletic ;-)

    ReplyDelete
  13. @Physeter:

    Ah... species is another problem; I'm thinking of higher taxa.

    The fundamental problems encountered in classifying species are equally found in classifying higher taxa. There is a continuum but we insist on breaking it with artificial boundaries.

    True, but it (classification) can reflect the best of our knowledge. Isn't that desirable?

    Sure. And so it is done for all the obvious cases. But there is a point of diminishing returns when you start considering murky ones. There, there result is endless useless debates - not about knowledge per se but about set of arbitrary rules (AKA taxonomy).

    I wasn't entirely clear. If you use the Linnaean system you will get ambiguous situations and "fuzzy-like" groups, even if you limit yourself to monophyletic groups. But if you use the phylogenetic system and define taxon names using phylogenetic nomenclature group membership will be resolved straightforwardly from your phylogenetic hypothesis). Clades are real and exist independently of our opinions.

    I don't understand why you think there are hard boundaries between clades. There aren't. Clades are real but they are fuzzy. E.g., green algae transition smoothly into plants.

    the One True Phylogeny (TM).

    A lot of people are convinced that taxonomy must reflect "true" phylogeny. That may be a good ideal but there are alternatives. In fact, it does not matter how you sort things, what's much more important is that you sort them reliably and unambiguously. Practicality should rule over unachievable dreams. What are lichens in your True Phylogeny? Polyphyletic, maybe? If so, what are eukaryotes themselves? Suddenly the nirvana of monophyletic taxonomy is not as close as it seemed. One good illustration of practicality is Protista. A grouping done by convention and based on considerations of convenience. I'd think it would be a waste of time to star battles over "true" protist taxonomy.

    ReplyDelete
  14. Chris Caprette says,

    I teach (my non-majors even) about the problem with the 3-domain system and I use Doolittle's Sci-Am figure to illustrate the problem.

    I'm glad to hear that. I wish other teachers would point out that the Three Domain Hypothesis is just that—hypothesis. It is not a proven fact and there's good reason to believe that it may not be correct—at least the part about eukaryotes and archaebacteria forming a clade may not be correct.

    One of the problems with Pace's essay in Nature is that he assumes that his favorite hypothesis is proven. What if archaebacteria and the other bacteria are more closely related to each other than either is to eukaryotes?

    I'm not saying that it's more likely but until we know for sure there's no reason to say, "But the next time you are inclined to do so, think what you teach your students: a wrong idea."

    We still don't know what's right and what's wrong when it comes to the relationship of prokaryotes and eukaryotes.

    ReplyDelete
  15. Psi Wavefunction,

    OK, that's sounds good reason! Though a sad one.

    P.S: Thanks for the TC-S paper

    ReplyDelete
  16. Larry said:
    It is not a proven fact and there's good reason to believe that it may not be correct—at least the part about eukaryotes and archaebacteria forming a clade may not be correct.
    ...
    We still don't know what's right and what's wrong when it comes to the relationship of prokaryotes and eukaryotes
    .

    The main controversy here is were to place the root of the tree of life (and if it is possible to place at all). One does not have to accept that Eukarya and Archaea are a clade, or that the tree of Life must be a neatly bifurcating structure to accept that Archaea are a valid evolutionary lineage (despite considerable LGT). This is not established but certainly not controversial.

    By continuing to use the term prokaryote one conversely propogates the common conception that Bacteria and Archaea are obviously more closely related, and the placement of the root of the tree of life the controversy.

    Therefore, on balance I believe that the most prudent approach is to refer to the three domains distinctly if you are refering to evolutionary lineages and to use the term "microbe" (as Pace suggests) to refere to unicellular, microscopic life, which is the underlying meaning when most say "prokaryote".

    ReplyDelete
  17. @Aaron and Rikke

    Microbe includes eukaryotes though. The problem with Pace's use of 'microbe' is that there is a much more biologically substantial difference between prokaryotic and eukaryotic microbes than between microbes and non-microbes. Perhaps to an ecologist, they're all the same whether they have an endomembrane system (incl. nucleus) and cytoskeleton or not, but from the perspective of cell biology that difference is non-trivial. I suspect a biochemist might also find a greater difference between euks and prokes than between microbes and macrobes.

    That said, I'm personally totally ok with unofficial paraphyletic taxa. "Prokaryote", to my knowledge, is unofficial. (to be honest, I wouldn't care much about official paraphyletic taxa either – as long as they're convenient for those of us who *apply* taxonomy ;-) )

    To me, the euk-proke distinction is more of a structural nature than a phylogenetic/taxonomic one. I'd think those to whom this part of phylogeny is relevant would also be inclined to use it in a similar manner...


    @Physeter Interesting, you're familiar with the TC-S abbreviation... ;-)

    ReplyDelete
  18. Aaron and Rikke say,

    One does not have to accept that Eukarya and Archaea are a clade, or that the tree of Life must be a neatly bifurcating structure to accept that Archaea are a valid evolutionary lineage (despite considerable LGT). This is not established but certainly not controversial.

    There are many valid evolutionary lineages (clades) within the prokaryotes. I'm particularly fond of the cyanobacteria, for example.

    There are several groups that branch off very early in bacterial evolution (e.g. Thermotoga, Aquifex). It's not clear that the very first split was between archaebacteria and all other bacteria.

    If eukaryotes arose because of a fusion between a primitive archaebacterium and a primitive gram negative bacterium then the distinction between prokaryotes and eukaryotes becomes messy but prokaryotes is still a valid cladistic taxon.

    Pace's argument depends on the validity of the strict Three Domain Hypothesis and there's a lot of questions about that.

    ReplyDelete