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Is Carl Woese losing a Kingdom

Graham Clark G.CLARK at lshtm.ac.uk
Wed Oct 2 15:16:41 EST 1996


Larry Moran wrote:

>>There ARE good reasons, mostly revolving around co-evolution. The 
>>rRNAs do not exist in the cell on their own but as part of an 
>>organelle. While most proteins intract with one or two others
>>in their funtional role in the cell, the ribosome is made up of
>>dozens of distinct proteins many of which are involved in specific
>>protein-rRNA interactions that involve specific structures/sequences
>>in both molecules.
>
>The problem is that you could say the same thing about many gene products. 
>You are no doubt familiar with the fact that transcription initiation complexes
>involve many interacting proteins and so do DNA replication complexes. But
>there are also complexes of proteins required for metabolism and things
>like electron transport. I don't think that ribosomes are very special in
>this sense.

I disagree. Yes, many proteins are involved in multi-protein complexes. 
However, most interact directly with only one or two others. Ribosomal 
RNAs interact directly with numerous proteins, not to mention tRNAs, other 
rRNAs and mRNAs. I doubt that any one protein even comes close to interacting
with as many.

>Besides, if your argument was valid then you would expect the ribosomal
>proteins to be highly conserved but it turns out that they are not. In fact
>the ribosomal RNAs themselves are not among the most highly conserved
>gene products as you would expect if the argument was valid.

Why would you expect this? Just because sequences co-evolve doesn't mean they 
have to be conserved. In fact my argument is based on the opposite view!
I'm also not saying that the same region of rRNA interacts with several other 
molecules, although some do and those tend to be highly conserved. 

>> In other words expressing a heterologous rRNA in
>>a cell is unlikely to give rise to functional ribosomes, unless it
>>comes from a closely related organism.
>
>This is true of a large number of genes. The exceptions are spectacular,
>but they are exceptions.

Again I disagree somewhat. If what you say were true we would not be able
to clone genes by heterologous complementation of mutants, but this is quite
routinely performed in yeast and E. coli using genes from a broad range of
organisms.

>> In addition to the multiple
>>coevolved rRNA/protein interactions forming a barrier to horizontal
>>transfer, it has been shown that rRNA promoter and RNA polymerase I 
>>also coevolve rapidly in eukaryotes, such that heterologous expression
>>is not possible because of promoter incompatibility even between quite
>>closely related organisms. 
>
>This is true of most genes. Nothing special about the promoters of rRNA
>genes in eukaryotes. Similarly in bacteria there are no guarantees that
>an E. coli promoter (of any given gene) will work in cyanobacteria or
>myxobacteria.

My point here is that horizontal transfer of rRNA genes may not work even 
between fairly closely related organisms whereas other classes of genes,
transcribed by Pol II for example, WILL be transferrable over a greater 
'distance'.

>Here's another kind of example for you to ponder. Think about histones and
>nucleosomes. We hypothesize that the conservation of histone amino acid
>sequences is due to the fact that they interact to form a core particle
>and that the multiplicity of such interactions inhibits evolution. Thus
>histones are highly conserved. What does this mean? It means that histone
>gene are *more* likely to be transferred horizontally because they will
>work in most organisms. In this case the presence of a complex leads to
>exactly the opposite conclusion to the one that you propose for ribosomal
>RNAs. It's the logic of your argument that I am questioning.

I fail to follow what you are trying to say here. Is there any evidence for 
horizontal transfer of histones? I am not aware of any so your premise 
appears to be wrong. Anyway sequence conservation need not have anything to 
do with success of horizontal transfer. Perhaps I can clarify my argument.

Ribosomal RNAs are single molecules that interact with many distinct proteins
and other RNAs. Most of these interactions are likely to be important in the 
functioning of the ribosome. The sequence specific rRNA-protein interactions
coevolve. When a heterologous rRNA is expressed in a cell it is likely
that at least one of the many rRNA-protein interactions needed to make a
functional ribosome will not form. Horizontal transfer of rRNAs will thus be
selected against. Most if not all proteins interact with fewer distinct 
proteins and therefore the likelihood of horizontal transfer of a protein 
encoding gene leading to a functional product is much greater.

I stand by my view that horizontal transfer of ribosomal RNA genes is unlikely 
to be successful.

Graham Clark





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