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crossing the great (prokaryote-eukaryote) divide

I've always enjoyed Nick Lane's writing1, so naturally an article he wrote for the ABC Science website caught my eye. Titled "Evolution of complex life on Earth, take 2?", it discusses an organism that appears to be neither prokaryote nor eukaryote, but something in-between.

There's a great divide between the cells that fit the description of 'prokaryote' and those that we view as eukaryotes. Both cell types have a cell membrane, which separates the cell's contents from its external environment; DNA & RNA (the nucleic acids); and ribosomes (where proteins are constructed from their constituent amino acids, in accordance with the information encoded in DNA). But beyond that, prokaryotic and eukaryotic cells are distinctly different.

Prokaryotes have a single, circular chromosome, with no nuclear membrane separating it from the cytoplasm. There are no membrane-bound organelles (as distinct from infoldings of the cell membrane, or 'plasma membrane'), and the cells are generally much, much smaller than a eukaryote cell.

In contrast, in a eukaryote the multiple, linear chromosome are separated from the cytoplasm & its contents by a nuclear membrane. In addition to ribosomes the cytoplasm contains a range of organelles, including mitochondria, golgi bodies, and (if they're photosynthetic cells) chloroplasts.

We spend quite a bit of time in class discussing the evolutionary origin of these more complex cells: for example, it's generally agreed that the mitochondria and chloroplasts are the results of endosymbiotic events. That is, each of these organelles originated from once-free-living prokaryote cells that were engulfed by some proto-eukaryote but not then digested (which is the usual fate for things that cells engulf). When this concept was first proposed by Lyn Margulis, back in the 1960s it received a fair bit of skepticism, but there's now plenty of evidence to support it. However, in class we've never really discussed what a cell in the process of becoming a eukaryote would look like, which is why I found Lane's article (& the original paper by Yamaguchi et al.) so interesting. In it, he discusses the organism pictured in the image below. It's a significant find because, as Yamaguchi & his colleagues point out,

[The] differences in cellular structure between prokaryotes and eukaryotes are so vast that the problem of how eukaryotes could have evolved from prokaryotes is one of the greatest enigmas in biology. If eukaryotes had indeed evolved from prokaryotes, then there must have been viable organisms with intermediate cellular structures.

Image credit: Fig 1 from Yamaguchi et al (2012), doi: 10.1093/jmicro/dfs062. CW: cell wall, N: nucleus, NM: nuclear membrane, PM: plasma (cell) membrane, E: endosymbionts (two of which were rod-shaped; the third resembled a spiral-shaped bacterium)

The image shows an ultra-thin section of a single-celled organism found on a polychaete worm that lived on a hydrothermal vent over a kilometre down in the ocean (Yamaguchi et al., 2012). Now, on first inspection that does look rather like a eukaryote cell, and Yamaguchi et al. point out that it has a volume about 100 times greater2 than that of a bacterium like E.coli. But as Lane notes:

It has a single nuclear membrane, with a few gaps. No nuclear pores. The DNA is composed of fine fibres as in bacteria, not thick eukaryotic chromosomes. There are ribosomes in the nucleus. Ribosomes in the nucleus! And ribosomes outside the nucleus too. The nuclear membrane is continuous with the cell membrane in several places. And some of the endosymbionts ... resemble corkscrew shaped bacteria on 3D reconstruction, making them look more like relatively recent bacterial acquisitions.

While it has internal membranes there is nothing resembling an endoplasmic reticulum, or the Golgi apparatus, or a cytoskeleton, all classic eukaryotic traits. In other words, this cell is actually nothing like a modern eukaryote. It just bears a superficial resemblance.

Unfortunately, as Lane notes, there's no genetic material available for a genome comparison that might help to place this enigmatic organism. This is because only one was found, and that was sliced into multiple ultra-thin sections for microscopic examination (which has, however, allowed a 3D reconstruction of what the original cell - and its endosymbionts - would have looked like).

One of the questions I've wondered about, in teaching about endosymbiosis as an origin for eukaryotes, is 'when did the nucleus develop? Before, or after, the endosymbiotic event that gave rise to mitochondria?' Yamaguchi et al. point out that the cell they've described doesn't have a fully-formed nucleus (only that single membrane and 'fibrous' genetic material), but does have internalised endosymbionts. From this, they suggest that

the nucleus was not necessarily formed when eubacteria started their endosymbiosis in the prokaryote host cell. Thus, the formation of the nucleus and transformation of bacteria into mitochondria might have proceeded independently

and with the host cell wall developing after the endosymbionts entered the host cell.

However, there are a lot of imponderables (& oh! how useful that genome would be here), & so the authors weren't really able to determine just where that unicellular organism sits among the domains of life. (That's assuming it's not simply an artefact of the sampling process.) Lane suggests three alternatives.

One is that it is a 'highly derived eukaryote' ie a cell adapted to a highly unusual environment that has lost many of the normal eukaryote structures. Of this, he says that

If Parakaryon myojinensis really is a highly derived eukaryote, then it's radically different in its basic plan to anything we've seen before. I don't think that's what it is.

The second option is that it's a sort of 'living fossil', surviving only in the unchanging deep-sea environment. This is the option favoured by Yamaguchi & his team. However, it's really really rare (a 12-year project has yielded just the single specimen): would such a rare organism have survived the ~2 billion years since eukaryotes evolved? Lane also comments that it

is not living in an unchanging environment: it is attached to the back of a segmented worm, a complex multicellular eukaryote that obviously did not exist in the early evolution of eukaryotes.

He suggests a third option:

it is a prokaryote, which has acquired endosymbionts, and is changing into a cell that resembles a eukaryote.

We certainly have evidence of endosymbiotic events in modern organisms, so why rule out the same thing happening among prokaryote cells? And Lane argues that when (not if) such events occur, their results are predictable - and are what we see here:

It is relatively large, with a genome that looks substantially larger than any other prokaryote, housed in a 'nucleus' continuous with internal membranes, and so on. These are all traits that we predict would evolve, from first principles, in prokaryotes with endosymbionts.

Obviously this one isn't settled yet. Yamaguchi et al.conclude by saying that

Of course, more specimens need to be collected and cultured to obtain the molecular data, including 16S rRNA genes, which will establish the evolutionary relationships between this microorganism and the prokaryotic and eukaryotic branches of life.

That's an important reminder: this is a big tale to hang on just a single cell. But it's is a fascinating story, nonetheless.


1 "Power, Sex & Suicide" has got to be on the list of the world's greatest book titles!

2 Modern eukaryotes are larger again by a factor of 100.

M.Yamaguchi, Y.Mori, Y.Kozuka, H.Okada, K.Uematsu, A.Tame, H.Furukawa, T.Maruyama, C.O'Driscoll Worman & K.Yokoyama (2012) Prokaryote or eukaryote? A unique microorganism from the deep sea. Journal of Electron Microscopy (preprint) doi: 10.1093/jmicro/dfs062


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Prokaryotes have a single, circular chromosome

I'm not clear on the distinction between a bacterial chromosome and its plasmids, except that "bacteria have a single chromosome" is a tenet of doctrine, so all those other elements of bacterial DNA have to be called something else.

Quite so.

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