Talmudic Question #42

Given that horizontal gene transfer between and among prokaryotes seems to be a relatively frequent occurrence, why does it appear to be so rare between prokaryotes and eukaryotes (except perhaps in early times)?

Comments

[Welkin]

I would add something to Adam's list of reasons why, at least for multicellular euks: even when such elements make it into a germline cell, and even if they are expressed and positively selected, there is still an extremely thin probability that they will ever be "chosen" to become part of the next generation (which is a random process, at least for higher euks). An inserted element at its moment of birth is but one allele in an otherwise large gene pool.

[Adam Clore]

I think the observation that we see few HGT events between Prokaryotes and Eukaryotes compared to those seen within Prokayotes may not be due to the lack of actual gene transfer between these groups, but rather
1) as mentioned earlier, the smaller number of Euks means that the there are less interactions between Pro and Eukes than between Pros and Pros,
2) Genes not integrated into either germlines or cells that will differentiate into germlines will not be passed on, and most germlines are "hidden" from the outside of the organism...at least the multicelled ones
3) genes that do make it into the germline will be lost if not expressed and selected for. Given the differences in mechanisms of gene regulation/expression between the Pros and Eukes, this seems unlikely in most circumstances.

Taken together the chances of an individual Eukaryotic cell taking up genetic material from a Prokaryote may be equal to the chances of a Pro/Pro uptake, but the observation of the former is less likely.

[Mark O. Martin]

An on that topic, I wonder if folks have seen this article:

Rumpho ME, Worful JM, Lee J, Kannan K, Tyler MS, Bhattacharya D, Moustafa A, Manhart JR. (2008). "Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica." Proc Natl Acad Sci U S A. 105(46):17867-71.

To be sure, this is a eukaryote - eukaryote gene transfer event. But it is to the germ line!

I also recommend this paper:

Hoffmeister M, Martin W. (2003). "Interspecific evolution: microbial symbiosis, endosymbiosis and gene transfer." Environ Microbiol. 5(8):641-9.

[Mark O. Martin]

I dearly love this topic. But I think that we may suffer from what I teach the students to call "coli-centricity": the assumption that all organisms in nature have the same characteristics as the one (or ones) we study closely.

So gene transfer from prokaryotes to eukaryotes (and vice versa) may be far more common than expected:

Gladyshev EA, Meselson M, Arkhipova IR. (2008). "Massive horizontal gene transfer in bdelloid rotifers." Science 320: 1210 - 1213.

I won't even steal your joy at reading the abstract! But do have a look, if this topic captivates...

Furthermore, I wonder if Meselson and coworkers' observations could be found among other metazoans that undergo cryptobiosis: brine shrimp or tardigrades, etc.

What a wonderful Microbial Planet around and within us!

[qetzal]

Another barrier, at least for multicellular eukaryotes, is that transfer would have to involve germ-line cells to be observed evolutionarily. Transfer to somatic cells could occur fairly often, but we wouldn't detect it by typical genomic comparisons.

In fact, Walter Doerfler has published a number of papers apparently showing that plasmid or bacteriophage DNA can be fed to mice, and it will subsequently appear in selected mouse cells. THey report finding it in cell nuclei (by FISH), and also report that it may get covalently linked to mouse DNA.

They've even reported that feeding pregnant mice results in detectable transfer to the fetus, but it's apparently through some sort of transplacental pathway. They didn't observe evidence of germ-line integration or transfer.

See, e.g., http://www.ncbi.nlm.nih.gov/pubmed/9819049

[Chris Condayan]

Could this be what John is referring to? Bugs Enjoy Hamster Sex - http://www.innovations-report.de/html/berichte/biowissenschaften_chemie/bericht-6056.html

Chris,
Sharp eyes indeed!.
Elio

[Epicanis]

My first guess would be purely "mechanical". For prokaryotes, all you have to do is get the genetic material past the outer walls and membranes to get to where the genome is. Some prokaryotes even have that "natural competence" thing going on and may even help.

To perform a successful horizontal gene transfer to a eukaryote, you've got to not only get the genetic material into the cell, but then through the cytoplasm (past all of the nucleic-acid-digesting enzymes) but also through the membrane of the nucleus.

Viruses can do it, but with the receptor specificity involved in viral infection, even if you ended up with a viral particle accidentally incorporating some of its host's genome and carrying it to another host, it's still just going to be from related-eukaryote-species to related-eukaryote-species.

There's also the issue of sheer population size. In absolute terms, horizontal gene transfer seems to actually be pretty RARE even among prokaryotes. The difference is that a population of prokaryotes can be mind-bogglingly huge, so even a one-in-a-quadrillion chance event might happen every day in a really active prokaryotic population. I consider this one of the main advantages of microbiology. Making mutant mice by irradiating the population and seeing if any of the survivors happen to have the mutation you want is effectively unfeasible due to the resources needed to maintain a large enough population (not to mention the waste of mouse-lives). For a microbial culture, though, this kind of technique isn't unusual.

[Elio Schaechter]

Does anyone remember what John has in mind?

Elio

[John S. Wilkins]

Wasn't a bacterium observed inserting genetic material into a hamster cell once?